Leah Acker; Erica N Pino; Edward S Boyden; Robert Desimone
FEF inactivation with improved optogenetic methods Journal Article
In: Proceedings of the National Academy of Sciences, 113 (46), pp. E7297–E7306, 2016.
Optogenetic methods have been highly effective for suppressing neural activity and modulating behavior in rodents, but effects have been much smaller in primates, which have much larger brains. Here, we present a suite of technologies to use optogenetics effectively in primates and apply these tools to a classic question in oculomotor control. First, we measured light absorption and heat propagation in vivo, optimized the conditions for using the red-light-shifted halorhodopsin Jaws in primates, and developed a large-volume illuminator to maximize light delivery with minimal heating and tissue displacement. Together, these advances allowed for nearly universal neuronal inactivation across more than 10 mm(3) of the cortex. Using these tools, we demonstrated large behavioral changes (i.e., up to several fold increases in error rate) with relatively low light power densities (≤100 mW/mm(2)) in the frontal eye field (FEF). Pharmacological inactivation studies have shown that the FEF is critical for executing saccades to remembered locations. FEF neurons increase their firing rate during the three epochs of the memory-guided saccade task: visual stimulus presentation, the delay interval, and motor preparation. It is unclear from earlier work, however, whether FEF activity during each epoch is necessary for memory-guided saccade execution. By harnessing the temporal specificity of optogenetics, we found that FEF contributes to memory-guided eye movements during every epoch of the memory-guided saccade task (the visual, delay, and motor periods).
Hamed Zivari Adab; Ivo D Popivanov; Wim Vanduffel; Rufin Vogels
In: Journal of Cognitive Neuroscience, 26 (10), pp. 2187–2200, 2014.
Practicing simple visual detection and discrimination tasks improves performance, a signature of adult brain plasticity. The neural mechanisms that underlie these changes in performance are still unclear. Previously, we reported that practice in discriminating the orientation of noisy gratings (coarse orientation discrimination) increased the ability of single neurons in the early visual area V4 to discriminate the trained stimuli. Here, we ask whether practice in this task also changes the stimulus tuning properties of later visual cortical areas, despite the use of simple grating stimuli. To identify candidate areas, we used fMRI to map activations to noisy gratings in trained rhesus monkeys, revealing a region in the posterior inferior temporal (PIT) cortex. Subsequent single unit record- ings in PIT showed that the degree of orientation selectivity was similar to that of area V4 and that the PIT neurons discriminated the trained orientations better than the untrained orientations. Unlike in previous single unit studies of perceptual learning in early visual cortex, more PIT neurons preferred trained compared with untrained orientations. The effects of training on the responses to the grating stimuli were also present when the animals were performing a difficult orthogo- nal task in which the grating stimuli were task-irrelevant, suggesting that the training effect does not need attention to be expressed. The PIT neurons could support orientation discrimination at low signal-to-noise levels. These findings suggest that extensive practice in discriminating simple grating stimuli not only affects early visual cortex but also changes the stimulus tuning of a late visual cortical area.
Hamed Zivari Adab; Rufin Vogels
In: Cerebral Cortex, 26 (9), pp. 3814–3827, 2016.
It is reasonable to assume that the discrimination of simple visual stimuli depends on the activity of early visual cortical neurons, because simple visual features are supposedly coded in these areas whereas more complex features are coded in late visual areas. Recently, we showed that training monkeys in a coarse orientation discrimination task modified the response properties of single neurons in the posterior inferior temporal (PIT) cortex, a late visual area. Here, we examined the contribution of PIT to coarse orientation discrimination using causal perturbation methods. Electrical stimulation (ES) of PIT with currents of at least 100 µA impaired coarse orientation discrimination in monkeys. The performance deterioration did not exclusively reflect a general impairment to perform a difficult perceptual task. However, high current (650 µA) but not low-current (100 µA) ES also impaired fine color discrimination. ES of temporal regions dorsal or anterior to PIT produced less impairment of coarse orientation discrimination than ES of PIT. Injections of the GABA agonist muscimol into PIT also impaired performance. These data suggest that the late cortical area PIT is part of the network that supports coarse orientation discrimination of a simple grating stimulus, at least after extensive training in this task at threshold.
Ramina Adam; Kevin D Johnston; Stefan Everling
In: Journal of Neurophysiology, 122 (2), pp. 672–690, 2019.
The caudal primate prefrontal cortex (PFC) is involved in target selection and visually guided saccades through both covert attention and overt orienting eye movements. Unilateral damage to the caudal PFC often leads to decreased awareness of a contralesional target alone, referred to as “neglect,” or when it is presented simultaneously with an ipsilesional target, referred to as “extinction.” In the current study, we examined whether deficits in contralesional target selection were due to contralesional oculomotor deficits, such as slower reaction times. We experimentally induced a focal ischemic lesion in the right caudal PFC of 4 male macaque monkeys using the vasoconstrictor endothelin-1 and measured saccade choice and reaction times on double-stimulus free-choice tasks and single-stimulus trials before and after the lesion. We found that 1) endothelin-1-induced lesions in the caudal PFC produced contralesional target selection deficits that varied in severity and duration based on lesion volume and location; 2) contralesional neglect-like deficits were transient and recovered by week 4 postlesion; 3) contralesional extinction-like deficits were longer lasting and recovered by weeks 8–16 postlesion; 4) contralesional reaction time returned to baseline well before the contralesional choice deficit had recovered; and 5) neither the mean reaction times nor the reaction time distributions could account for the degree of contralesional extinction on the free-choice task throughout recovery. These findings demonstrate that the saccade choice bias observed after a right caudal PFC lesion is not exclusively due to contralesional motor deficits, but instead reflects a combination of impaired motor and attentional processing.
Ramina Adam; Kevin D Johnston; Ravi S Menon; Stefan Everling
In: NeuroImage, 207 , pp. 1–17, 2020.
Visual extinction has been characterized by the failure to respond to a visual stimulus in the contralesional hemifield when presented simultaneously with an ipsilesional stimulus (Corbetta and Shulman, 2011). Unilateral damage to the macaque frontoparietal cortex commonly leads to deficits in contralesional target selection that resemble visual extinction. Recently, we showed that macaque monkeys with unilateral lesions in the caudal prefrontal cortex (PFC) exhibited contralesional target selection deficits that recovered over 2–4 months (Adam et al., 2019). Here, we investigated the longitudinal changes in functional connectivity (FC) of the frontoparietal network after a small or large right caudal PFC lesion in four macaque monkeys. We collected ultra-high field resting-state fMRI at 7-T before the lesion and at weeks 1–16 post-lesion and compared the functional data with behavioural performance on a free-choice saccade task. We found that the pattern of frontoparietal network FC changes depended on lesion size, such that the recovery of contralesional extinction was associated with an initial increase in network FC that returned to baseline in the two small lesion monkeys, whereas FC continued to increase throughout recovery in the two monkeys with a larger lesion. We also found that the FC between contralesional dorsolateral PFC and ipsilesional parietal cortex correlated with behavioural recovery and that the contralesional dorsolateral PFC showed increasing degree centrality with the frontoparietal network. These findings suggest that both the contralesional and ipsilesional hemispheres play an important role in the recovery of function. Importantly, optimal compensation after large PFC lesions may require greater recruitment of distant and intact areas of the frontoparietal network, whereas recovery from smaller lesions was supported by a normalization of the functional network.
Jordi Aguila; Javier Cudeiro; Casto Rivadulla
In: Cerebral Cortex, 26 (2), pp. 628–638, 2016.
Noninvasive brain stimulation techniques have been successfully used to modulate brain activity, have become a highly useful tool in basic and clinical research and, recently, have attracted increased attention due to their putative use as a method for neuro-enhancement. In this scenario, transcranial static magnetic stimulation (SMS) of moderate strength might represent an affordable, simple, and complementary method to other procedures, such as Transcranial Magnetic Stimulation or direct current stimulation, but its mechanisms and effects are not thoroughly understood. In this study, we show that static magnetic fields applied to visual cortex of awake primates cause reversible deficits in a visual detection task. Complementary experiments in anesthetized cats show that the visual deficits are a consequence of a strong reduction in neural activity. These results demonstrate that SMS is able to effectively modulate neuronal activity and could be considered to be a tool to be used for different purposes ranging from experimental studies to clinical applications.
Jordi Aguila; Javier F Cudeiro; Casto Rivadulla
In: Cerebral Cortex, 27 (6), pp. 3331–3345, 2017.
In awake monkeys, we used repetitive transcranial magnetic stimulation (rTMS) to focally inactivate visual cortex while measuring the responsiveness of parvocellular lateral geniculate nucleus (LGN) neurons. Effects were noted in 64/75 neurons, and could be divided into 2 main groups: (1) for 39 neurons, visual responsiveness decreased and visual latency increased without apparent shift in receptive field (RF) position and (2) a second group (n = 25, 33% of the recorded cells) whose excitability was not compromised, but whose RF position shifted an average of 4.5°. This change is related to the retinotopic correspondence observed between the recorded thalamic area and the affected cortical zone. The effect of inactivation for this group of neurons was compatible with silencing the original retinal drive and unmasking a second latent retinal drive onto the studied neuron. These results indicate novel and remarkable dynamics in thalamocortical circuitry that force us to reassess constraints on retinogeniculate transmission.
Amir-Mohammad Alizadeh; Ilse C Van Dromme; Peter Janssen
In: Journal of Neurophysiology, 120 (6), pp. 2806–2818, 2018.
Both dorsal and ventral visual pathways harbor several areas sensitive to gradients of binocular disparity (i.e., higher-order disparity). Although a wealth of information exists about disparity processing in early visual (V1, V2, and V3) and end-stage areas, TE in the ventral stream, and the anterior intraparietal area (AIP) in the dorsal stream, little is known about midlevel area TEO in the ventral pathway. We recorded single-unit responses to disparity-defined curved stimuli in a functional magnetic resonance imaging (fMRI) activation elicited by curved surfaces compared with flat surfaces in the macaque area TEO. This fMRI activation contained a small proportion of disparity- selective neurons, with very few of them second-order disparity selective. Overall, this population of TEO neurons did not preserve its three-dimensional structure selectivity across positions in depth, in- dicating a lack of higher-order disparity selectivity, but showed stronger responses to flat surfaces than to curved surfaces, as predicted by the fMRI experiment. The receptive fields of the responsive TEO cells were relatively small and generally foveal. A linear support vector machine classifier showed that this population of disparity-selective TEO neurons contains reliable information about the sign of curvature and the position in depth of the stimulus.
Amir-Mohammad Alizadeh; Ilse C Van Dromme; Bram-Ernst Verhoef; Peter Janssen
In: NeuroImage, 166 , pp. 46–59, 2018.
The cortical network processing three-dimensional (3D) object structure defined by binocular disparity spans both the ventral and dorsal visual streams. However, very little is known about the neural representation of 3D structure at intermediate levels of the visual hierarchy. Here, we investigated the neural selectivity for 3D surfaces in the macaque Posterior Intraparietal area (PIP) in the medial bank of the caudal intraparietal sulcus (IPS). We first identified a region sensitive to depth-structure information in the medial bank of the caudal IPS using functional Magnetic Resonance Imaging (fMRI), and then recorded single-cell activity within this fMRI activation in the same animals. Most PIP neurons were selective for the 3D orientation of planar surfaces (first-order disparity) at very short latencies, whereas a very small fraction of PIP neurons were selective for curved surfaces (second-order disparity). A linear support vector machine classifier could reliably identify the direction of the disparity gradient in planar and curved surfaces based on the responses of a population of disparity-selective PIP neurons. These results provide the first detailed account of the neuronal properties in area PIP, which occupies an intermediate position in the hierarchy of visual areas involved in processing depth structure from disparity.
Ken Ichi Amemori; Ann M Graybiel
In: Nature Neuroscience, 15 (5), pp. 776–785, 2012.
The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.
Ken Ichi Amemori; Satoko Amemori; Ann M Graybiel
In: Journal of Neuroscience, 35 (5), pp. 1939–1953, 2015.
The judgment of whether to accept or to reject an offer is determined by positive and negative affect related to the offer, but affect also induces motivational responses. Rewarding and aversive cues influence the firing rates of many neurons in primate prefrontal and cingulate neocortical regions, but it still is unclear whether neurons in these regions are related to affective judgment or to motivation.To address this issue, we recorded simultaneously the neuronal spike activities of single units in the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC) of macaque monkeys as they performed approach–avoidance (Ap–Av) and approach–approach (Ap–Ap) decision-making tasks that can behaviorally dissociate affective judgment and motivation. Notably, neurons having activity correlated with motivational condition could be distinguished from neurons having activity related to affective judgment, especially in the Ap–Av task. Although many neurons in both regions exhibited similar, selective patterns of task-related activity, we found a larger proportion of neurons activated in low motivational conditions in the dlPFC than in the ACC, and the onset of this activity was signifi- cantly earlier in the dlPFC than in the ACC. Furthermore, the temporal onsets of affective judgment represented by neuronal activities were significantly slower in the low motivational conditions than in the other conditions. These findings suggest that motivation and affective judgment both recruit dlPFC and ACC neurons but with differential degrees of involvement and timing.
Satoko Amemori; Ken ichi Amemori; Margaret L Cantor; Ann M Graybiel
In: Journal of Neuroscience Methods, 240 , pp. 154–160, 2015.
Background: We have developed a novel head-holding device for behaving non-human primates that affords stability suitable for reliable chronic electrophysiological recording experiments. The device is completely non-invasive, and thus avoids the risk of infection and other complications that can occur with the use of conventional, surgically implanted head-fixation devices. New method: The device consists of a novel non-invasive head mold and bar clamp holder, and is customized to the shape of each monkey's head. The head-holding device that we introduce, combined with our recording system and reflection-based eye-tracking system, allows for chronic behavioral experiments and single-electrode or multi-electrode recording, as well as manipulation of brain activity. Results and comparison with existing methods: With electrodes implanted chronically in multiple brain regions, we could record neural activity from cortical and subcortical structures with stability equal to that recorded with conventional head-post fixation. Consistent with the non-invasive nature of the device, we could record neural signals for more than two years with a single implant. Importantly, the monkeys were able to hold stable eye fixation positions while held by this device, demonstrating the possibility of analyzing eye movement data with only the gentle restraint imposed by the non-invasive head-holding device. Conclusions: We show that the head-holding device introduced here can be extended to the head holding of smaller animals, and note that it could readily be adapted for magnetic resonance brain imaging over extended periods of time.
Ken ichi Amemori; Satoko Amemori; Daniel J Gibson; Ann M Graybiel
In: Neuron, 99 (4), pp. 829–841, 2018.
Persistent thoughts inducing irrationally pessimistic and repetitive decisions are often symptoms of mood and anxiety disorders. Regional neural hyper-activities have been associated with these disorders, but it remains unclear whether there is a specific brain region causally involved in these persistent valuations. Here, we identified potential sources of such persistent states by microstimulating the striatum of macaques performing a task by which we could quantitatively estimate their subjective pessimistic states using their choices to accept or reject conflicting offers. We found that this microstimulation induced irrationally repetitive choices with negative evaluations. Local field potentials recorded in the same microstimulation sessions exhibited modulations of beta-band oscillatory activity that paralleled the persistent negative states influencing repetitive decisions. These findings demonstrate that local striatal zones can causally affect subjective states influencing persistent negative valuation and that abnormal beta-band oscillations can be associated with persistency in valuation accompanied by an anxiety-like state.
Britt Anderson; Ryan E B Mruczek; Keisuke Kawasaki; David L Sheinberg
In: Cerebral Cortex, 18 (11), pp. 2540–2552, 2008.
Long-term familiarity facilitates recognition of visual stimuli. To better understand the neural basis for this effect, we measured the local field potential (LFP) and multiunit spiking activity (MUA) from the inferior temporal (IT) lobe of behaving monkeys in response to novel and familiar images. In general, familiar images evoked larger amplitude LFPs whereas MUA responses were greater for novel images. Familiarity effects were attenuated by image rotations in the picture plane of 45 degrees. Decreasing image contrast led to more pronounced decreases in LFP response magnitude for novel, compared with familiar images, and resulted in more selective MUA response profiles for familiar images. The shape of individual LFP traces could be used for stimulus classification, and classification performance was better for the familiar image category. Recording the visual and auditory evoked LFP at multiple depths showed significant alterations in LFP morphology with distance changes of 2 mm. In summary, IT cortex shows local processing differences for familiar and novel images at a time scale and in a manner consistent with the observed behavioral advantage for classifying familiar images and rapidly detecting novel stimuli.
Britt Anderson; David L Sheinberg
In: Neuropsychologia, 46 (4), pp. 947–957, 2008.
Timing is critical. The same event can mean different things at different times and some events are more likely to occur at one time than another. We used a cued visual classification task to evaluate how changes in temporal context affect neural responses in inferior temporal cortex, an extrastriate visual area known to be involved in object processing. On each trial a first image cued a temporal delay before a second target image appeared. The animal's task was to classify the second image by pressing one of two buttons previously associated with that target. All images were used as both cues and targets. Whether an image cued a delay time or signaled a button press depended entirely upon whether it was the first or second picture in a trial. This paradigm allowed us to compare inferior temporal cortex neural activity to the same image subdivided by temporal context and expectation. Neuronal spiking was more robust and visually evoked local field potentials (LFP's) larger for target presentations than for cue presentations. On invalidly cued trials, when targets appeared unexpectedly early, the magnitude of the evoked LFP was reduced and delayed and neuronal spiking was attenuated. Spike field coherence increased in the beta-gamma frequency range for expected targets. In conclusion, different neural responses in higher order ventral visual cortex may occur for the same visual image based on manipulations of temporal attention.
Ariana R Andrei; Sorin A Pojoga; Roger Janz; Valentin Dragoi
Integration of cortical population signals for visual perception Journal Article
In: Nature Communications, 10 , pp. 3832, 2019.
Visual stimuli evoke heterogeneous responses across nearby neural populations. These signals must be locally integrated to contribute to perception, but the principles underlying this process are unknown. Here, we exploit the systematic organization of orientation preference in macaque primary visual cortex (V1) and perform causal manipulations to examine the limits of signal integration. Optogenetic stimulation and visual stimuli are used to simultaneously drive two neural populations with overlapping receptive fields. We report that optogenetic stimulation raises firing rates uniformly across conditions, but improves the detection of visual stimuli only when activating cells that are preferentially-tuned to the visual stimulus. Further, we show that changes in correlated variability are exclusively present when the optogenetically and visually-activated populations are functionally-proximal, suggesting that correlation changes represent a hallmark of signal integration. Our results demonstrate that information from functionally-proximal neurons is pooled for perception, but functionally-distal signals remain independent. Primary visual cortical neurons exhibit diverse responses to visual stimuli yet how these signals are integrated during visual perception is not well understood. Here, the authors show that optogenetic stimulation of neurons situated near the visually‐driven population leads to improved orientation detection in monkeys through changes in correlated variability.
Evan G Antzoulatos; Earl K Miller
In: eLife, 5 (NOVEMBER2016), pp. 1–22, 2016.
Categorization has been associated with distributed networks of the primate brain, including the prefrontal (PFC) and posterior parietal cortices (PPC). Although category-selective spiking in PFC and PPC has been established, the frequency-dependent dynamic interactions of frontoparietal networks are largely unexplored. We trained monkeys to perform a delayed-match-to-spatial-category task while recording spikes and local field potentials from the PFC and PPC with multiple electrodes. We found category-selective beta- and delta-band synchrony between and within the areas. However, in addition to the categories, delta synchrony and spiking activity also reflected irrelevant stimulus dimensions. By contrast, beta synchrony only conveyed information about the task-relevant categories. Further, category-selective PFC neurons were synchronized with PPC beta oscillations, while neurons that carried irrelevant information were not. These results suggest that long-range beta-band synchrony could act as a filter that only supports neural representations of the variables relevant to the task at hand.
Mari Anzai; Soich Nagao
In: Neuroscience Research, 83 , pp. 33–42, 2014.
Adaptation of the horizontal vestibulo-ocular reflex (HVOR) provides an experimental model for cerebellum-dependent motor learning. We developed an eye movement measuring system and a paradigm for induction of HVOR adaptation for the common marmoset. The HVOR gain in dark measured by 10° (peak-to-peak amplitude) and 0.11-0.5. Hz turntable oscillation was around unity. The gain-up and gain-down HVOR adaptation was induced by 1. h of sustained out-of-phase and in-phase 10°-0.33. Hz combined turntable-screen oscillation in the light, respectively. To examine the role of long-term depression (LTD) of parallel fiber-Purkinje cell synapses, we intraperitonially applied T-588 or nimesulide, which block the induction of LTD in vitro or in vivo preparations, 1. h before the test of HVOR adaptation. T-588 (3 and 5. mg/kg body weight) did not affect nonadapted HVOR gains, and impaired both gain-up and gain-down HVOR adaptation. Nimesulide (3 and 6. mg/kg) did not affect nonadapted HVOR gains, and impaired gain-up HVOR adaptation dose-dependently; however, it very little affected gain-down HVOR adaptation. These findings are consistent with the results of our study of nimesulide on the adaptation of horizontal optokinetic response in mice (. Le et al., 2010), and support the view that LTD underlies HVOR adaptation.
Paul L Aparicio; Elias B Issa; James J DiCarlo
In: Journal of Neuroscience, 36 (50), pp. 12729–12745, 2016.
While early cortical visual areas contain fine scale spatial organization of neuronal properties such as orientation preference, the spatial organization of higher-level visual areas is less well understood. The fMRI demonstration of face preferring regions in human ventral cortex (FFA, OFA) and monkey inferior temporal cortex ("face patches") raises the question of how neural selectivity for faces is organized. Here, we targeted hundreds of spatially registered neural recordings to the largest fMRI-identified face selective region in monkeys, the middle face patch (MFP) and show that the MFP contains a graded enrichment of face preferring neurons. At its center, as much as 93% of the sites we sampled responded twice as strongly to faces than to non-face objects. We estimate the maximum neurophysiological size of the MFP to be ∼6 mm in diameter, consistent with its previously reported size under fMRI. Importantly, face selectivity in the MFP varied strongly even between neighboring sites. Additionally, extremely face selective sites were ∼50x more likely to be present inside the MFP than outside. These results provide the first direct quantification of the size and neural composition of the MFP by showing that the cortical tissue localized to the fMRI defined region consists of a very high fraction of face preferring sites near its center, and a monotonic decrease in that fraction along any radial spatial axis.
Iñigo Arandia-Romero; Seiji Tanabe; Jan Drugowitsch; Adam Kohn; Rubén Moreno-Bote
In: Neuron, 89 (6), pp. 1305–1316, 2016.
Numerous studies have shown that neuronal responses are modulated by stimulus properties and also by the state of the local network. However, little is known about how activity fluctuations of neuronal populations modulate the sensory tuning of cells and affect their encoded information. We found that fluctuations in ongoing and stimulus-evoked population activity in primate visual cortex modulate the tuning of neurons in a multiplicative and additive manner. While distributed on a continuum, neurons with stronger multiplicative effects tended to have less additive modulation and vice versa. The information encoded by multiplicatively modulated neurons increased with greater population activity, while that of additively modulated neurons decreased. These effects offset each other so that population activity had little effect on total information. Our results thus suggest that intrinsic activity fluctuations may act as a "traffic light" that determines which subset of neurons is most informative.
Fabrice Arcizet; Richard J Krauzlis
Covert spatial selection in primate basal ganglia Journal Article
In: PLoS Biology, 16 (10), pp. e2005930, 2018.
The basal ganglia are important for action selection. They are also implicated in perceptual and cognitive functions that seem far removed from motor control. Here, we tested whether the role of the basal ganglia in selection extends to nonmotor aspects of behavior by recording neuronal activity in the caudate nucleus while animals performed a covert spatial attention task. We found that caudate neurons strongly select the spatial location of the relevant stimulus throughout the task even in the absence of any overt action. This spatially selective activity was dependent on task and visual conditions and could be dissociated from goal-directed actions. Caudate activity was also sufficient to correctly identify every epoch in the covert attention task. These results provide a novel perspective on mechanisms of attention by demonstrating that the basal ganglia are involved in spatial selection and tracking of behavioral states even in the absence of overt orienting movements.
Wael F Asaad; Navaneethan Santhanam; Steven McClellan; David J Freedman
In: Journal of Neurophysiology, 109 (1), pp. 249–260, 2013.
Behavioral, psychological, and physiological experiments often require the ability to present sensory stimuli, monitor and record subjects' responses, interface with a wide range of devices, and precisely control the timing of events within a behavioral task. Here, we describe our recent progress developing an accessible and full-featured software system for controlling such studies using the MATLAB environment. Compared with earlier reports on this software, key new features have been implemented to allow the presentation of more complex visual stimuli, increase temporal precision, and enhance user interaction. These features greatly improve the performance of the system and broaden its applicability to a wider range of possible experiments. This report describes these new features and improvements, current limitations, and quantifies the performance of the system in a real-world experimental setting.
Habiba Azab; Benjamin Y Hayden
In: PLoS Biology, 15 (11), pp. e2003091, 2017.
We hypothesized that during binary economic choice, decision makers use the first option they attend as a default to which they compare the second. To test this idea, we recorded activity of neurons in the dorsal anterior cingulate cortex (dACC) of macaques choosing between gambles presented asynchronously. We find that ensemble encoding of the value of the first offer includes both choice-dependent and choice-independent aspects, as if reflecting a partial decision. That is, its responses are neither entirely pre- nor post-decisional. In contrast, coding of the value of the second offer is entirely decision dependent (i.e., post-decisional). This result holds even when offer-value encodings are compared within the same time period. Additionally, we see no evidence for 2 pools of neurons linked to the 2 offers; instead, all comparison appears to occur within a single functionally homogenous pool of task-selective neurons. These observations suggest that economic choices reflect a context-dependent evaluation of attended options. Moreover, they raise the possibility that value representations reflect, to some extent, a tentative commitment to a choice.
Habiba Azab; Benjamin Y Hayden
In: European Journal of Neuroscience, 47 (8), pp. 979–993, 2018.
The anterior cingulate cortex can be divided into distinct ventral (subgenual, sgACC) and dorsal (dACC), portions. The role of dACC in value-based decision-making is hotly debated, while the role of sgACC is poorly understood. We recorded neuronal activity in both regions in rhesus macaques performing a token-gambling task. We find that both encode many of the same vari- ables; including integrated offered values of gambles, primary as well as secondary reward outcomes, number of current tokens and anticipated rewards. Both regions exhibit memory traces for offer values and putative value comparison signals. Both regions use a consistent scheme to encode the value of the attended option. This result suggests that neurones do not appear to be spe- cialized for specific offers (that is, neurones use an attentional as opposed to labelled line coding scheme). We also observed some differences between the two regions: (i) coding strengths in dACC were consistently greater than those in sgACC, (ii) neu- rones in sgACC responded especially to losses and in anticipation of primary rewards, while those in dACC showed more bal- anced responding and (iii) responses to the first offer were slightly faster in sgACC. These results indicate that sgACC and dACC have some functional overlap in economic choice, and are consistent with the idea, inspired by neuroanatomy, which sgACC may serve as input to dACC.
Habiba Azab; Benjamin Y Hayden
In: Behavioral Neuroscience, 134 (4), pp. 296–308, 2020.
Evaluation often involves integrating multiple determinants of value, such as the different possible outcomes in risky choice. A brain region can be placed either before or after a presumed evaluation stage by measuring how responses of its neurons depend on multiple determinants of value. A brain region could also, in principle, show partial integration, which would indicate that it occupies a middle position between (preevaluative) nonintegration and (postevaluative) full integration. Existing mathematical techniques cannot distinguish full from partial integration and therefore risk misidentifying regional function. Here we use a new Bayesian regression-based approach to analyze responses of neurons in dorsal anterior cingulate cortex (dACC) to risky offers. We find that dACC neurons only partially integrate across outcome dimensions, indicating that dACC cannot be assigned to either a pre- or postevaluative position. Neurons in dACC also show putative signatures of value comparison, thereby demonstrating that comparison does not require complete evaluation before proceeding.
Marzyeh Azimi; Mariann Oemisch; Thilo Womelsdorf
In: Psychopharmacology, 237 (4), pp. 997–1010, 2020.
Rationale: Nicotinic acetylcholine receptors (nAChRs) modulate attention, memory, and higher executive functioning, but it is unclear how nACh sub-receptors mediate different mechanisms supporting these functions. Objectives: We investigated whether selective agonists for the alpha-7 nAChR versus the alpha-4/beta-2 nAChR have unique functional contributions for value learning and attentional filtering of distractors in the nonhuman primate. Methods: Two adult rhesus macaque monkeys performed reversal learning following systemic administration of either the alpha-7 nAChR agonist PHA-543613 or the alpha-4/beta-2 nAChR agonist ABT-089 or a vehicle control. Behavioral analysis quantified performance accuracy, speed of processing, reversal learning speed, the control of distractor interference, perseveration tendencies, and motivation. Results: We found that the alpha-7 nAChR agonist PHA-543613 enhanced the learning speed of feature values but did not modulate how salient distracting information was filtered from ongoing choice processes. In contrast, the selective alpha-4/beta-2 nAChR agonist ABT-089 did not affect learning speed but reduced distractibility. This dissociation was dose-dependent and evident in the absence of systematic changes in overall performance, reward intake, motivation to perform the task, perseveration tendencies, or reaction times. Conclusions: These results suggest nicotinic sub-receptor specific mechanisms consistent with (1) alpha-4/beta-2 nAChR specific amplification of cholinergic transients in prefrontal cortex linked to enhanced cue detection in light of interferences, and (2) alpha-7 nAChR specific activation prolonging cholinergic transients, which could facilitate subjects to follow-through with newly established attentional strategies when outcome contingencies change. These insights will be critical for developing function-specific drugs alleviating attention and learning deficits in neuro-psychiatric diseases.
Sahand Babapoor-Farrokhran; Martin Vinck; Thilo Womelsdorf; Stefan Everling
In: Nature Communications, 8 , pp. 13967, 2017.
The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coacti- vated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3–9 Hz theta and a 12–30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta- band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of fron- toparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands.
Theda Backen; Stefan Treue; Julio C Martinez-Trujillo
In: Eneuro, 5 (1), pp. 1–19, 2018.
Single neurons in the primate lateral prefrontal cortex (LPFC) encode information about the allocation of visual attention and the features of visual stimuli. However, how this compares to the performance of neuronal ensembles at encoding the same information is poorly understood. Here, we recorded the responses of neuronal ensembles in the LPFC of two macaque monkeys while they performed a task that required attending to one of two moving random dot patterns positioned in different hemifields and ignoring the other pattern. We found single units selective for the location of the attended stimulus as well as for its motion direction. To determine the coding of both variables in the population of recorded units, we used a linear classifier and progressively built neuronal ensembles by iteratively adding units according to their individual performance (best single units), or by iteratively adding units based on their contribution to the ensemble performance (best ensemble). For both methods, ensembles of relatively small sizes (n textless 60) yielded substantially higher decoding performance relative to individual single units. However, the decoder reached similar performance using fewer neurons with the best ensemble building method compared to the best single units method. Our results indicate that neuronal ensembles within the LPFC encode more information about the attended spatial and non-spatial features of visual stimuli than individual neurons. They further suggest that efficient coding of attention can be achieved by relatively small neuronal ensembles characterized by a certain relationship between signal and noise correlation structures. Significance Statement Single neurons in the primate lateral prefrontal cortex (LPFC) are known to encode the spatial location of attended stimuli as well as other visual features. Here, we investigate how these single neuron coding properties translate into how ensembles of neurons encode information. Our results show that LPFC neuronal ensembles encode both the allocation of attention and the direction of motion of moving stimuli with higher efficiency than single units. Furthermore, relatively small ensembles reach the same decoding accuracy as the full ensembles. Our findings indicate that information coding by neuronal ensembles within the LPFC depends on complex network properties that cannot be solely estimated from coding properties of individual neurons.
Dong Hyun Baek; Jeyeon Lee; Hang Jin Byeon; Hoseok Choi; In Young Kim; Kyoung-Min Lee; James Jungho Pak; Dong Pyo Jang; Sang Hoon Lee
In: Journal of Neural Engineering, 11 (4), pp. 1–10, 2014.
Objective. Epidural electrocorticography (ECoG) activity may be more reliable and stable than single-unit-activity or local field potential. Invasive brain computer interface (BCI) devices are limited by mechanical mismatching and cellular reactive responses due to differences in the elastic modulus and the motion of stiff electrodes. We propose a mesh-shaped electrode to enhance the contactability between surface of dura and electrode. Approach. We designed a polyimide (PI) electrode with a mesh pattern for more conformal contact with a curved surface. We compared the contact capability of mesh PI electrodes with conventionally used sheet PI electrode. The electrical properties of the mesh PI electrode were evaluated for four weeks. We recorded the epidural ECoG (eECoG) activity on the surface of rhesus monkey brains while they performed a saccadic task for four months. Main results. The mesh PI electrode showed good contact with the agarose brain surface, as evaluated by visual inspection and signal measurement. It was about 87% accurate in predicting the direction of saccade eye movement. Significance. Our results indicate that the mesh PI electrode was flexible and good contact on the curved surface and can record eECoG activity maintaining close contact to dura, which was proved by in vivo and in vitro test.
Zahra Bahmani; Mohammad Reza Daliri; Yaser Merrikhi; Kelsey Clark; Behrad Noudoost
In: Neuron, 97 (4), pp. 967–979, 2018.
The online maintenance and manipulation of information in working memory (WM) is essential for guiding behavior based on our goals. Understanding how WM alters sensory processing in pursuit of different behavioral objectives is therefore crucial to establish the neural basis of our goal-directed behavior. Here we show that, in the middle temporal (MT) area of rhesus monkeys, the power of the local field potentials in the ab band (8–25 Hz) increases, reflecting the remembered location and the animal's performance. Moreover, the content of WM determines how coherently MT sites oscillate and how synchronized spikes are relative to these oscillations. These changes in spike timing are not only sufficient to carry sensory and memory information, they can also account for WM-induced sensory enhancement. These results provide a mechanistic-level understanding of how WM alters sensory processing by coordinating the timing of spikes across the neuronal population, enhancing the sensory representation of WM targets.
Pragathi Priyadharsini Balasubramani; Meghan C Pesce; Benjamin Y Hayden
In: European Journal of Neuroscience, 51 (10), pp. 2033–2051, 2020.
Stopping, or inhibition, is a form of self-control that is a core element of flexible and adaptive behavior. Its neural origins remain unclear. Some views hold that inhibition decisions reflect the aggregation of widespread and diverse pieces of information, including information arising in ostensible core reward regions (i.e., outside the canonical executive system). We recorded activity of single neurons in the orbitofrontal cortex (OFC) of macaques, a region associated with economic decisions, and whose role in inhibition is debated. Subjects performed a classic inhibition task known as the stop signal task. Ensemble decoding analyses reveal a clear firing rate pattern that distinguishes successful from failed inhibition and that begins after the stop signal and before the stop signal reaction time (SSRT). We also found a different and orthogonal ensemble pattern that distinguishes successful from failed stopping before the beginning of the trial. These signals were distinct from, and orthogonal to, value encoding, which was also observed in these neurons. The timing of the early and late signals was, respectively, consistent with the idea that neuronal activity in OFC encodes inhibition both proactively and reactively.
Sébastien Ballesta; Camillo Padoa-Schioppa
Economic decisions through circuit inhibition Journal Article
In: Current Biology, 29 (22), pp. 3814–3824, 2019.
Economic choices between goods are thought to rely on the orbitofrontal cortex (OFC), but the decision mechanisms remain poorly understood. To shed light on this fundamental issue, we recorded from the OFC of monkeys choosing between two juices offered sequentially. An analysis of firing rates across time windows revealed the presence of different groups of neurons similar to those previously identified under simultaneous offers. This observation suggested that economic decisions in the two modalities are formed in the same neural circuit. We then examined several hypotheses on the decision mechanisms. OFC neurons encoded good identities and values in a juice-based representation (labeled lines). Contrary to previous assessments, our data argued against the idea that decisions rely on mutual inhibition at the level of offer values. In fact, we showed that previous arguments for mutual inhibition were confounded by differences in value ranges. Instead, decisions seemed to involve mechanisms of circuit inhibition, whereby each offer value indirectly inhibited neurons encoding the opposite choice outcome. Our results reconcile a variety of previous findings and provide a general account for the neuronal underpinnings of economic choices.
David L Barack; Steve W C Chang; Michael L Platt
In: Neuron, 96 (2), pp. 339–347, 2017.
Foraging for resources is a fundamental behavior balancing systematic search and strategic disengagement. The foraging behavior of primates is especially complex and requires long-term memory, value comparison, strategic planning, and decision-making. Here we provide evidence from two different foraging tasks that neurons in primate posterior cingulate cortex (PCC) signal decision salience during foraging to motivate disengagement from the current strategy. In our foraging tasks, salience refers to the difference between decision thresholds and the net harvested reward. Salience signals were stronger in poor foraging contexts than rich ones, suggesting low harvest rates recruit mechanisms in PCC that regulate strategic disengagement and exploration during foraging. Barack et al. report that foraging salience motivated strategic disengagement in two distinct tasks. Posterior cingulate neurons preferentially signaled salience and forecast divergent choices when reward rates were low, suggesting a role in the strategic control of behavior.
Annamaria Barczak; Saskia Haegens; Deborah A Ross; Tammy McGinnis; Peter Lakatos; Charles E Schroeder
In: Cell Reports, 27 (12), pp. 3447–3459, 2019.
Visual physiology is traditionally investigated by presenting stimuli with gaze held constant. However, during active viewing of a scene, information is actively acquired using systematic patterns of fixations and saccades. Prior studies suggest that during such active viewing, both nonretinal, saccade-related signals and “extra-classical” receptive field inputs modulate visual processing. This study used a set of active viewing tasks that allowed us to compare visual responses with and without direct foveal input, thus isolating the contextual eye movement-related influences. Studying nonhuman primates, we find strong contextual modulation in primary visual cortex (V1): excitability and response amplification immediately after fixation onset, transiting to suppression leading up to the next saccade. Time-frequency decomposition suggests that this amplification and suppression cycle stems from a phase reset of ongoing neuronal oscillatory activity. The impact of saccade-related contextual modulation on stimulus processing makes active visual sensing fundamentally different from the more passive processes investigated in traditional paradigms. By isolating contextual eye movement-related influences during active vision, Barczak et al. show that eye movements affect excitability in V1 such that responses are amplified immediately after fixation onset and suppressed as the next saccade approaches. This amplification and suppression cycle stems from a phase reset of ambient oscillatory activity in V1.
Jalal K Baruni; Brian Lau; Daniel C Salzman
In: Nature Neuroscience, 18 (11), pp. 1656–1663, 2015.
Neural activity in visual area V4 is enhanced when attention is directed into neuronal receptive fields. However, the source of this enhancement is unclear, as most physiological studies have manipulated attention by changing the absolute reward associated with a particular location as well as its value relative to other locations. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while we independently varied the reward magnitude associated with correct discrimination at each location. Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in V4 were consistently modulated by absolute reward value, exhibiting increased activity, increased gamma-band power and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms.
Charles B Beaman; Sarah L Eagleman; Valentin Dragoi
In: Nature Communications, 8 , pp. 1308, 2017.
Cortical activity changes continuously during the course of the day. At a global scale, population activity varies between the ‘synchronized' state during sleep and ‘desynchronized' state during waking. However, whether local fluctuations in population synchrony during wakefulness modulate the accuracy of sensory encoding and behavioral performance is poorly understood. Here, we show that populations of cells in monkey visual cortex exhibit rapid fluctuations in synchrony ranging from desynchronized responses, indicative of high alertness, to highly synchronized responses. These fluctuations are local and control the trial variability in population coding accuracy and behavioral performance in a discrimination task. When local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are enhanced. These findings demonstrate that the structure of variability in local cortical populations is not noise but rather controls how sensory information is optimally integrated with ongoing processes to guide network coding and behavior.
Joachim Bellet; Chih-Yang Chen; Ziad M Hafed
In: Journal of Neurophysiology, 118 , pp. 2789–2805, 2017.
Microsaccades are tiny saccades that occur during gaze fixation. Even though visual processing has been shown to be strongly modulated close to the time of microsaccades, both at central and peripheral eccentricities, it is not clear how these eye movements might influence longer term fluctuations in brain activity and behavior. Here we found that visual processing is significantly affected and, in a rhythmic manner, even several hundreds of milliseconds after a microsaccade. Human visual detection efficiency, as measured by reaction time, exhibited coherent rhythmic oscillations in the ? - and ? -frequency bands for up to ~650–700 ms after a microsaccade. Surprisingly, the oscillations were sequentially pulsed across visual hemifields relative to microsaccade direction, first occurring in the same hemifield as the movement vector for ~400 ms and then the opposite. Such pulsing also affected perceptual detection performance. Our results suggest that visual processing is subject to long-lasting oscillations that are phase locked to microsaccade generation, and that these oscillations are dependent on microsaccade direction.
Marie E Bellet; Joachim Bellet; Hendrikje Nienborg; Ziad M Hafed; Philipp Berens
In: Journal of Neurophysiology, 121 (2), pp. 646–661, 2019.
Saccades are ballistic eye movements that rapidly shift gaze from one location of visual space to another. Detecting saccades in eye movement recordings is important not only for studying the neural mechanisms underlying sensory, motor, and cognitive processes, but also as a clinical and diagnostic tool. However, automatically detecting saccades can be difficult, particularly when such saccades are generated in coordination with other tracking eye movements, like smooth pursuits, or when the saccade amplitude is close to eye tracker noise levels, like with microsaccades. In such cases, labeling by human experts is required, but this is a tedious task prone to variability and error. We developed a convolutional neural network to automatically detect saccades at human-level accuracy and with minimal training examples. Our algorithm surpasses state of the art according to common performance metrics and could facilitate studies of neurophysiological processes underlying saccade generation and visual processing.
Giacomo Benvenuti; Yuzhi Chen; Charu Ramakrishnan; Karl Deisseroth; Wilson S Geisler; Eyal Seidemann
In: Neuron, 100 (6), pp. 1504–1512., 2018.
Humans have remarkable scale-invariant visual capabilities. For example, our orientation discrimination sensitivity is largely constant over more than two orders of magnitude of variations in stimulus spatial frequency (SF). Orientation-selective V1 neurons are likely to contribute to orientation discrimination. However, because at any V1 location neurons have a limited range of receptive field (RF) sizes, we predict that at low SFs V1 neurons will carry little orientation information. If this were the case, what could account for the high behavioral sensitivity at low SFs? Using optical imaging in behaving macaques, we show that, as predicted, V1 orientation-tuned responses drop rapidly with decreasing SF. However, we reveal a surprising coarse-scale signal that corresponds to the projection of the luminance layout of low-SF stimuli to V1's retinotopic map. This homeomorphic and distributed representation, which carries high-quality orientation information, is likely to contribute to our striking scale-invariant visual capabilities.
Narcisse P Bichot; Matthew T Heard; Robert Desimone
In: Journal of Neuroscience Methods, 199 (2), pp. 265–272, 2011.
It has been known that monkeys will repeatedly press a bar for electrical stimulation in several different brain structures. We explored the possibility of using electrical stimulation in one such structure, the nucleus accumbens, as a substitute for liquid reward in animals performing a complex task, namely visual search. The animals had full access to water in the cage at all times on days when stimulation was used to motivate them. Electrical stimulation was delivered bilaterally at mirror locations in and around the accumbens, and the animals' motivation to work for electrical stimulation was quantified by the number of trials they performed correctly per unit of time. Acute mapping revealed that stimulation over a large area successfully supported behavioral performance during the task. Performance improved with increasing currents until it reached an asymptotic, theoretically maximal level. Moreover, stimulation with chronically implanted electrodes showed that an animal's motivation to work for electrical stimulation was at least equivalent to, and often better than, when it worked for liquid reward while on water control. These results suggest that electrical stimulation in the accumbens is a viable method of reward in complex tasks. Because this method of reward does not necessitate control over water or food intake, it may offer an alternative to the traditional liquid or food rewards in monkeys, depending on the goals and requirements of the particular research project.
Narcisse P Bichot; Matthew T Heard; Ellen M DeGennaro; Robert Desimone
A source for feature-based attention in the prefrontal cortex Journal Article
In: Neuron, 88 (4), pp. 832–844, 2015.
In cluttered scenes, we can use feature-based attention to quickly locate a target object. To understand how feature attention is used to find and select objects for action, we focused on the ventral prearcuate (VPA) region of prefrontal cortex. In a visual search task, VPA cells responded selectively to search cues, maintained their feature selectivity throughout the delay and subsequent saccades, and discriminated the search target in their receptive fields with a time course earlier than in FEF or IT cortex. Inactivation of VPA impaired the animals' ability to find targets, and simultaneous recordings in FEF revealed that the effects of feature attention were eliminated while leaving the effects of spatial attention in FEF intact. Altogether, the results suggest that VPA neurons compute the locations of objects with the features sought and send this information to FEF to guide eye movements to those relevant stimuli.
Narcisse P Bichot; Rui Xu; Azriel Ghadooshahy; Michael L Williams; Robert Desimone
In: Nature Communications, 10 , pp. 5727, 2019.
When searching for an object in a cluttered scene, we can use our memory of the target object features to guide our search, and the responses of neurons in multiple cortical visual areas are enhanced when their receptive field contains a stimulus sharing target object features. Here we tested the role of the ventral prearcuate region (VPA) of prefrontal cortex in the control of feature attention in cortical visual area V4. VPA was unilaterally inactivated in monkeys performing a free-viewing visual search for a target stimulus in an array of stimuli, impairing monkeys' ability to find the target in the array in the affected hemifield, but leaving intact their ability to make saccades to targets presented alone. Simultaneous recordings in V4 revealed that the effects of feature attention on V4 responses were eliminated or greatly reduced while leaving the effects of spatial attention on responses intact. Altogether, the results suggest that feedback from VPA modulates processing in visual cortex during attention to object features.
Rasmus M Birn; Alexander K Converse; Abigail Z Rajala; Andrew L Alexander; Walter F Block; Alan B McMillan; Bradley T Christian; Caitlynn N Filla; Dhanabalan Murali; Samuel A HWIBBLEey; Rick L Jenison; Luis C Populin
In: Journal of Neuroscience, 39 (8), pp. 1436–1444, 2019.
Dopamine (DA) levels in the striatum are increased by many therapeutic drugs, such as methylphenidate (MPH), which also alters behavioral and cognitive functions thought to be controlled by the PFC dose-dependently. We linked DA changes and functional connectivity (FC) using simultaneous [18F]fallypride PET and resting-state fMRI in awake male rhesus monkeys after oral administration of various doses of MPH. We found a negative correlation between [18F]fallypride nondisplaceable binding potential (BPND) and MPH dose in the head of the caudate (hCd), demonstrating increased extracellular DA resulting from MPH administration. The decreased BPND was negatively correlated with FC between the hCd and the PFC. Subsequent voxelwise analyses revealed negative correlations with FC between the hCd and the dorsolateral PFC, hippocampus, and precuneus. These results, showing that MPH-induced changes in DA levels in the hCd predict resting-state FC, shed light on a mechanism by which changes in striatal DA could influence function in the PFC.
Kévin Blaize; Fabrice Arcizet; Marc Gesnik; Harry Ahnine; Ulisse Ferrari; Thomas Deffieux; Pierre Pouget; Frédéric Chavane; Mathias Fink; José Alain Sahel; José Alain Sahel; José Alain Sahel; Mickael Tanter; Serge Picaud
In: Proceedings of the National Academy of Sciences, 117 (25), pp. 14453–14463, 2020.
Deep regions of the brain are not easily accessible to investigation at the mesoscale level in awake animals or humans. We have recently developed a functional ultrasound (fUS) technique that enables imaging hemodynamic responses to visual tasks. Using fUS imaging on two awake nonhuman primates performing a passive fixation task, we constructed retinotopic maps at depth in the visual cortex (V1, V2, and V3) in the calcarine and lunate sulci. The maps could be acquired in a single-hour session with relatively few presentations of the stimuli. The spatial resolution of the technology is illustrated by mapping patterns similar to ocular dominance (OD) columns within superficial and deep layers of the primary visual cortex. These acquisitions using fUS suggested that OD selectivity is mostly present in layer IV but with extensions into layers II/III and V. This imaging technology provides a new mesoscale approach to the mapping of brain activity at high spatiotemporal resolution in awake subjects within the whole depth of the cortex.
T C Blanchard; John M Pearson; Benjamin Y Hayden
In: Proceedings of the National Academy of Sciences, 110 (38), pp. 15491–15496, 2013.
Intertemporal choice tasks, which pit smaller/sooner rewards against larger/later ones, are frequently used to study time preferences and, by extension, impulsivity and self-control. When used in animals, many trials are strung together in sequence and an adjusting buffer is added after the smaller/sooner option to hold the total duration of each trial constant. Choices of the smaller/sooner option are not reward maximizing and so are taken to indicate that the animal is discounting future rewards. However, if animals fail to correctly factor in the duration of the postreward buffers, putative discounting behavior may instead reflect constrained reward maximization. Here, we report three results consistent with this discounting-free hypothesis. We find that (i) monkeys are insensitive to the association between the duration of postreward delays and their choices; (ii) they are sensitive to the length of postreward delays, although they greatly underestimate them; and (iii) increasing the salience of the postreward delay biases monkeys toward the larger/later option, reducing measured discounting rates. These results are incompatible with standard discounting-based accounts but are compatible with an alternative heuristic model. Our data suggest that measured intertemporal preferences in animals may not reflect impulsivity, or even mental discounting of future options, and that standard human and animal intertemporal choice tasks measure unrelated mental processes.
T C Blanchard; Benjamin Y Hayden
In: Journal of Neuroscience, 34 (2), pp. 646–655, 2014.
The dorsal anterior cingulate cortex (dACC) is a key hub of the brain's executive control system. Although a great deal is known about its role in outcome monitoring and behavioral adjustment, whether and how it contributes to the decision process remain unclear. Some theories suggest that dACC neurons track decision variables (e.g., option values) that feed into choice processes and is thus "predecisional." Other theories suggest that dACC activity patterns differ qualitatively depending on the choice that is made and is thus "postdecisional." To compare these hypotheses, we examined responses of 124 dACC neurons in a simple foraging task in which monkeys accepted or rejected offers of delayed rewards. In this task, options that vary in benefit (reward size) and cost (delay) appear for 1 s; accepting the option provides the cued reward after the cued delay. To get at dACC neurons' contributions to decisions, we focused on responses around the time of choice, several seconds before the reward and the end of the trial. We found that dACC neurons signal the foregone value of the rejected option, a postdecisional variable. Neurons also signal the profitability (that is, the relative value) of the offer, but even these signals are qualitatively different on accept and reject decisions, meaning that they are also postdecisional. These results suggest that dACC can be placed late in the decision process and also support models that give it a regulatory role in decision, rather than serving as a site of comparison.
Tommy C Blanchard; Andreas Wilke; Benjamin Y Hayden
Hot-hand bias in rhesus monkeys Journal Article
In: Journal of Experimental Psychology: Animal Behavior Processes, 40 (3), pp. 280–286, 2014.
Human decision-makers often exhibit the hot-hand phenomenon, a tendency to perceive positive serial autocorrelations in independent sequential events. The term is named after the observation that basketball fans and players tend to perceive streaks of high accuracy shooting when they are demonstrably absent. That is, both observing fans and participating players tend to hold the belief that a player's chance of hitting a shot are greater following a hit than following a miss. We hypothesize that this bias reflects a strong and stable tendency among primates (including humans) to perceive positive autocorrelations in temporal sequences, that this bias is an adaptation to clumpy foraging environments, and that it may even be ecologically rational. Several studies support this idea in humans, but a stronger test would be to determine whether nonhuman primates also exhibit a hot-hand bias. Here we report behavior of 3 monkeys performing a novel gambling task in which correlation between sequential gambles (i.e., temporal clumpiness) is systematically manipulated. We find that monkeys have better performance (meaning, more optimal behavior) for clumped (positively correlated) than for dispersed (negatively correlated) distributions. These results identify and quantify a new bias in monkeys' risky decisions, support accounts that specifically incorporate cognitive biases into risky choice, and support the suggestion that the hot-hand phenomenon is an evolutionary ancient bias.
Tommy C Blanchard; Lauren S Wolfe; Ivo Vlaev; Joel S Winston; Benjamin Y Hayden
Biases in preferences for sequences of outcomes in monkeys Journal Article
In: Cognition, 130 (3), pp. 289–299, 2014.
Movies, vacations, and meals are all examples of events composed of a sequence of smaller events. How do we go from our evaluations of each scene in a movie to an evaluation of the sequence as a whole$alpha$ In theory, we should simply average the values of the individual events. In practice, however, we are biased towards sequences where each element tends to be better than the previous, where the last value is large, and we overweight the best (or worst) part of the sequence. To study how general these biases are we examined monkeys' preferences for sequences of rewards in a novel reward repeat task. Monkeys were first given a sequence of rewards and then chose between repeating the sequence or receiving a standard comparator sequence. We found that, like humans, monkeys overweight events that happen later in a sequence, so much so that adding a small reward to the end of a sequence can paradoxically reduce its value. Monkeys were also biased towards sequences with large peak values (the highest value in the sequence), but only following a working memory challenge, suggesting that this preference may be driven by memory limitations. These results demonstrate the cross-species nature of biases in preferences for sequences of outcomes. In addition, monkeys' consistent preference for sequences in which large values occur later challenges the generality of discounting models of intertemporal choice in animals.
Tommy C Blanchard; Benjamin Y Hayden
In: PLoS ONE, 10 (2), pp. e0117057, 2015.
Studies of animal impulsivity generally find steep subjective devaluation, or discounting, of delayed rewards - often on the order of a 50% reduction in value in a few seconds. Because such steep discounting is highly disfavored in evolutionary models of time preference, we hypothesize that discounting tasks provide a poor measure of animals' true time preferences. One prediction of this hypothesis is that estimates of time preferences based on these tasks will lack external validity, i.e. fail to predict time preferences in other contexts. We examined choices made by four rhesus monkeys in a computerized patch-leaving foraging task interleaved with a standard intertemporal choice task. Monkeys were significantly more patient in the foraging task than in the intertemporal choice task. Patch-leaving behavior was well fit by parameter-free optimal foraging equations but poorly fit by the hyperbolic discount parameter obtained from the intertemporal choice task. Day-to-day variation in time preferences across the two tasks was uncorrelated with each other. These data are consistent with the conjecture that seemingly impulsive behavior in animals is an artifact of their difficulty understanding the structure of intertemporal choice tasks, and support the idea that animals are more efficient rate maximizers in the multi-second range than intertemporal choice tasks would suggest.
Tommy C Blanchard; Caleb E Strait; Benjamin Y Hayden
In: Journal of Neurophysiology, 114 (4), pp. 2439–2449, 2015.
We frequently need to commit to a choice to achieve our goals; however, the neural processes that keep us motivated in pursuit of delayed goals remain obscure. We examined ensemble responses of neurons in macaque dorsal anterior cingulate cortex (dACC), an area previously implicated in self-control and persistence, in a task that requires commitment to a choice to obtain a reward. After reward receipt, dACC neurons signaled reward amount with characteristic ensemble firing rate patterns; during the delay in anticipation of the reward, ensemble activity smoothly and gradually came to resemble the postreward pattern. On the subset of risky trials, in which a reward was anticipated with 50% certainty, ramping ensemble activity evolved to the pattern associated with the anticipated reward (and not with the anticipated loss) and then, on loss trials, took on an inverted form anticorrelated with the form associated with a win. These findings enrich our knowledge of reward processing in dACC and may have broader implications for our understanding of persistence and self-control.
Amarender R Bogadhi; Anil Bollimunta; David A Leopold; Richard J Krauzlis
In: Current Biology, 29 (5), pp. 726–736, 2019.
Spatial neglect is a common clinical syndrome involving disruption of the brain's attention-related circuitry, including the dorsocaudal temporal cortex. In macaques, the attention deficits associated with neglect can be readily modeled, but the absence of evidence for temporal cortex involvement has suggested a fundamental difference from humans. To map the neurological expression of neglect-like attention deficits in macaques, we measured attention-related fMRI activity across the cerebral cortex during experimental induction of neglect through reversible inactivation of the superior colliculus and frontal eye fields. During inactivation, monkeys exhibited hallmark attentional deficits of neglect in tasks using either motion or non-motion stimuli. The behavioral deficits were accompanied by marked reductions in fMRI attentional modulation that were strongest in a small region on the floor of the superior temporal sulcus; smaller reductions were also found in frontal eye fields and dorsal parietal cortex. Notably, direct inactivation of the mid-superior temporal sulcus (STS) cortical region identified by fMRI caused similar neglect-like spatial attention deficits. These results identify a putative macaque homolog to temporal cortex structures known to play a central role in human neglect.
Amarender R Bogadhi; Antimo Buonocore; Ziad M Hafed
In: Journal of Neuroscience, 40 (49), pp. 9496–9506, 2020.
Covert and overt spatial selection behaviors are guided by both visual saliency maps derived from early visual features as well as priority maps reflecting high-level cognitive factors. However, whether mid-level perceptual processes associated with visual form recognition contribute to covert and overt spatial selection behaviors remains unclear. We hypothesized that if peripheral visual forms contribute to spatial selection behaviors, then they should do so even when the visual forms are task-irrelevant. We tested this hypothesis in male and female human subjects as well as in male macaque monkeys performing a visual detection task. In this task, subjects reported the detection of a suprathreshold target spot presented on top of one of two peripheral images, and they did so with either a speeded manual button press (humans) or a speeded saccadic eye movement response (humans and monkeys). Crucially, the two images, one with a visual form and the other with a partially phase-scrambled visual form, were completely irrelevant to the task. In both manual (covert) and oculomotor (overt) response modalities, and in both humans and monkeys, response times were faster when the target was congruent with a visual form than when it was incongruent. Importantly, incongruent targets were associated with almost all errors, suggesting that forms automatically captured selection behaviors. These findings demonstrate that mid-level perceptual processes associated with visual form recognition contribute to covert and overt spatial selection. This indicates that neural circuits associated with target selection, such as the superior colliculus, may have privileged access to visual form information. SIGNIFICANCE STATEMENT Spatial selection of visual information either with (overt) or without (covert) foveating eye movements is critical to primate behavior. However, it is still not clear whether spatial maps in sensorimotor regions known to guide overt and covert spatial selection are influenced by peripheral visual forms. We probed the ability of humans and monkeys to perform overt and covert target selection in the presence of spatially congruent or incongruent visual forms. Even when completely task-irrelevant, images of visual objects had a dramatic effect on target selection, acting much like spatial cues used in spatial attention tasks. Our results demonstrate that traditional brain circuits for orienting behaviors, such as the superior colliculus, likely have privileged access to visual object representations.
Amarender R Bogadhi; Leor N Katz; Anil Bollimunta; David A Leopold; Richard J Krauzlis
The evolution of the primate brain is marked by a dramatic increase in the number of neocortical areas that process visual information 1. This cortical expansion supports two hallmarks of high-level primate vision - the ability to selectively attend to particular visual features 2 and the ability to recognize a seemingly limitless number of complex visual objects 3. Given their prominent roles in high-level vision for primates, it is commonly assumed that these cortical processes supersede the earlier versions of these functions accomplished by the evolutionarily older brain structures that lie beneath the cortex. Contrary to this view, here we show that the superior colliculus (SC), a midbrain structure conserved across all vertebrates 4, is necessary for the normal expression of attention-related modulation and object selectivity in a newly identified region of macaque temporal cortex. Using a combination of psychophysics, causal perturbations and fMRI, we identified a localized region in the temporal cortex that is functionally dependent on the SC. Targeted electrophysiological recordings in this cortical region revealed neurons with strong attention-related modulation that was markedly reduced during attention deficits caused by SC inactivation. Many of these neurons also exhibited selectivity for particular visual objects, and this selectivity was also reduced during SC inactivation. Thus, the SC exerts a causal influence on high-level visual processing in cortex at a surprisingly late stage where attention and object selectivity converge, perhaps determined by the elemental forms of perceptual processing the SC has supported since before there was a neocortex.
Anil Bollimunta; Amarender R Bogadhi; Richard J Krauzlis
In: Nature Communications, 9 , pp. 3553, 2018.
The causal roles of the frontal eye fields (FEF) and superior colliculus (SC) in spatial selective attention have not been directly compared. Reversible inactivation is an established method for testing causality but comparing results between FEF and SC is complicated by differences in size and morphology of the two brain regions. Here we exploited the fact that inactivation of FEF and SC also changes the metrics of saccadic eye movements, providing an independent benchmark for the strength of the causal manipulation. Using monkeys trained to covertly perform a visual motion-change detection task, we found that inactivation of either FEF or SC could cause deficits in attention task performance. However, SC-induced attention deficits were found with saccade changes half the size needed to get FEF-induced attention deficits. Thus, performance in visual attention tasks is vulnerable to loss of signals from either structure, but suppression of SC activity has a more devastating effect.
Yehudit Botschko; Merav Yarkoni; Mati Joshua
In: Frontiers in Systems Neuroscience, 12 , pp. 1–11, 2018.
When animal behavior is studied in a laboratory environment, the animals are often extensively trained to shape their behavior. A crucial question is whether the behavior observed after training is part of the natural repertoire of the animal or represents an outlier in the animal's natural capabilities. This can be investigated by assessing the extent to which the target behavior is manifested during the initial stages of training and the time course of learning. We explored this issue by examining smooth pursuit eye movements in monkeys naïve to smooth pursuit tasks. We recorded the eye movements of monkeys from the first days of training on a step-ramp paradigm. We used bright spots, monkey pictures and scrambled versions of the pictures as moving targets. We found that during the initial stages of training, the pursuit initiation was largest for the monkey pictures and in some direction conditions close to target velocity. When the pursuit initiation was large, the monkeys mostly continued to track the target with smooth pursuit movements while correcting for displacement errors with small saccades. Two weeks of training increased the pursuit eye velocity in all stimulus conditions, whereas further extensive training enhanced pursuit slightly more. The training decreased the coefficient of variation of the eye velocity. Anisotropies that grade pursuit across directions were observed from the first day of training and mostly persisted across training. Thus, smooth pursuit in the step-ramp paradigm appears to be part of the natural repertoire of monkeys' behavior and training adjusts monkeys' natural predisposed behavior.
Chadwick B Boulay; Florian Pieper; Matthew L Leavitt; Julio C Martinez-Trujillo; Adam J Sachs
In: Journal of Neurophysiology, 115 (1), pp. 486–499, 2016.
Neurons in the lateral prefrontal cortex (LPFC) encode sensory and cognitive signals, as well as commands for goal-directed actions. Therefore, the LPFC might be a good signal source for a goal-selection brain-computer interface (BCI) that decodes the intended goal of a motor action previous to its execution. As a first step in the development of a goal-selection BCI, we set out to determine if we could decode simple behavioral intentions to direct gaze to eight different locations in space from single-trial LPFC neural activity. We recorded neuronal spiking activity from microelectrode arrays implanted in area 8A of the LPFC of two adult macaques while they made visually guided saccades to one of eight targets in a center-out task. Neuronal activity encoded target location immediately after target presentation, during a delay epoch, during the execution of the saccade, and every combination thereof. Many (40%) of the neurons that encoded target location during multiple epochs preferred different locations during different epochs. Despite heterogeneous and dynamic responses, the neuronal feature set that best predicted target location was the averaged firing rates from the entire trial and it was best classified using linear discriminant analysis (63.6$backslash$textendash96.9% in 12 sessions, mean 80.3%; information transfer rate: 21$backslash$textendash59, mean 32.8 bits/min). Our results demonstrate that it is possible to decode intended saccade target location from single-trial LPFC activity and suggest that the LPFC is a suitable signal source for a goal-selection cognitive BCI.
Scott L Brincat; Earl K Miller
In: Nature Neuroscience, 18 (4), pp. 576–581, 2015.
Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical. HPC-PFC interactions have rarely been studied in monkeys, whose cognitive and mnemonic abilities are akin to those of humans. We found functional differences and frequency-specific interactions between HPC and PFC of monkeys learning object pair associations, an animal model of human explicit memory. PFC spiking activity reflected learning in parallel with behavioral performance, whereas HPC neurons reflected feedback about whether trial-and-error guesses were correct or incorrect. Theta-band HPC-PFC synchrony was stronger after errors, was driven primarily by PFC to HPC directional influences and decreased with learning. In contrast, alpha/beta-band synchrony was stronger after correct trials, was driven more by HPC and increased with learning. Rapid object associative learning may occur in PFC, whereas HPC may guide neocortical plasticity by signaling success or failure via oscillatory synchrony in different frequency bands.
Scott L Brincat; Earl K Miller
In: Journal of Neuroscience, 36 (37), pp. 9739–9754, 2016.
As we learn about items in our environment, their neural representations become increasingly enriched with our acquired knowledge. But there is little understanding of how network dynamics and neural processing related to external information changes as it becomes laden with "internal" memories. We sampled spiking and local field potential activity simultaneously from multiple sites in the lateral prefrontal cortex (PFC) and the hippocampus (HPC)-regions critical for sensory associations-of monkeys performing an object paired-associate learning task. We found that in the PFC, evoked potentials to, and neural information about, external sensory stimulation decreased while induced beta-band (∼11-27 Hz) oscillatory power and synchrony associated with "top-down" or internal processing increased. By contrast, the HPC showed little evidence of learning-related changes in either spiking activity or network dynamics. The results suggest that during associative learning, PFC networks shift their resources from external to internal processing.
Sophie Brulé; Bastien Herlin; Pierre Pouget; Marcus Missal
Ketamine reduces temporal expectation in the rhesus monkey Journal Article
In: Psychopharmacology, pp. 1–9, 2020.
Rationale: Ketamine, a well-known general dissociative anesthetic agent that is a non-competitive antagonist of the N-methyl-D-aspartate receptor, perturbs the perception of elapsed time and the expectation of upcoming events. Objective: The objective of this study was to determine the influence of ketamine on temporal expectation in the rhesus monkey. Methods: Two rhesus monkeys were trained to make a saccade between a central warning stimulus and an eccentric visual target that served as imperative stimulus. The delay between the warning and the imperative stimulus could take one of four different values randomly with the same probability (variable foreperiod paradigm). During experimental sessions, a subanesthetic low dose of ketamine (0.25–0.35 mg/kg) was injected i.m. and the influence of the drug on movement latency was measured. Results: We found that in the control conditions, saccadic latencies strongly decreased with elapsed time before the appearance of the visual target showing that temporal expectation built up during the delay period between the warning and the imperative stimulus. However, after ketamine injection, temporal expectation was significantly reduced in both subjects. In addition, ketamine also increased average movement latency but this effect could be dissociated from the reduction of temporal expectation. Conclusion: In conclusion, a subanesthetic dose of ketamine could have two independent effects: increasing reaction time and decreasing temporal expectation. This alteration of temporal expectation could explain cognitive deficits observed during ketamine use.
Kelly R Bullock; Florian Pieper; Adam J Sachs; Julio C Martinez-Trujillo
In: Journal of Neurophysiology, 118 (1), pp. 15–28, 2017.
Common trends observed in many visual and oculomotor-related cortical areas include retinotopically organized receptive and movement fields exhibiting a Gaussian shape and increasing size with eccentricity. These trends are demonstrated in the frontal eye fields (FEF), many visual areas, and the superior colliculus (SC), but have not been thoroughly characterized in prearcuate area 8Ar of the prefrontal cortex. This is important since area 8Ar, located anterior to the FEF, is more cytoarchitectonically similar to prefrontal areas than premotor areas. Here we recorded the responses of 166 neurons in area 8Ar of two male macaques while the animals made visually guided saccades to a peripheral sine-wave grating stimulus positioned at one of 40 possible locations (8 angles along 5 eccentricities). To characterize the neurons' receptive and movement fields, we fit a bivariate Gaussian model to the baseline-subtracted average firing rate during stimulus presentation (early and late visual epoch) and prior to saccade onset (presaccadic epoch). 121/166 neurons showed spatially selective visual and presaccadic responses. Of the visually selective neurons, 76% preferred the contralateral visual hemifield, whereas 24% preferred the ipsilateral hemifield. The angular width of visual and movement-related fields scaled positively with increasing eccentricity. Moreover, responses of neurons with visual receptive fields were modulated by target contrast exhibiting sigmoid tuning curves that resemble those of visual neurons in upstream areas such as MT and V4. Finally, we found that neurons with receptive fields at similar spatial locations were clustered within the area; however, this organization did not appear retinotopic.
Timothy J Buschman; Eric L Denovellis; Cinira Diogo; Daniel Bullock; Earl K Miller
In: Neuron, 76 (4), pp. 838–846, 2012.
Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at " beta" (19-40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased " alpha" (6-16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits.
Brittany N Bushnell; Philip J Harding; Yoshito Kosai; Wyeth Bair; Anitha Pasupathy
Equiluminance cells in visual cortical area V4 Journal Article
In: Journal of Neuroscience, 31 (35), pp. 12398–12412, 2011.
We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These "equiluminance" cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature-some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4.
Brittany N Bushnell; Philip J Harding; Yoshito Kosai; Anitha Pasupathy
In: Journal of Neuroscience, 31 (11), pp. 4012–4024, 2011.
Past studies of shape coding in visual cortical area V4 have demonstrated that neurons can accurately represent isolated shapes in terms of their component contour features. However, rich natural scenes contain many partially occluded objects, which have "accidental" contours at the junction between the occluded and occluding objects. These contours do not represent the true shape of the occluded object and are known to be perceptually discounted. To discover whether V4 neurons differentially encode accidental contours, we studied the responses of single neurons in fixating monkeys to complex shapes and contextual stimuli presented either in isolation or adjoining each other to provide a percept of partial occlusion. Responses to preferred contours were suppressed when the adjoining context rendered those contours accidental. The observed suppression was reversed when the partial occlusion percept was compromised by introducing a small gap between the component stimuli. Control experiments demonstrated that these results likely depend on contour geometry at T-junctions and cannot be attributed to mechanisms based solely on local color/luminance contrast, spatial proximity of stimuli, or the spatial frequency content of images. Our findings provide novel insights into how occluded objects, which are fundamental to complex visual scenes, are encoded in area V4. They also raise the possibility that the weakened encoding of accidental contours at the junction between objects could mark the first step of image segmentation along the ventral visual pathway.
Brittany N Bushnell; Anitha Pasupathy
Shape encoding consistency across colors in primate V4 Journal Article
In: Journal of Neurophysiology, 108 (5), pp. 1299–1308, 2012.
Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations.
Charles F Cadieu; Ha Hong; Daniel L K Yamins; Nicolas Pinto; Diego Ardila; Ethan A Solomon; Najib J Majaj; James J DiCarlo
In: PLoS Computational Biology, 10 (12), pp. e1003963, 2014.
The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of ‘‘kernel analysis'' that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio- inspired models, that possibility cannot be ruled out merely on representational performance grounds.
X Cai; Camillo Padoa-Schioppa
In: Journal of Neuroscience, 32 (11), pp. 3791–3808, 2012.
We examined the activity of individual cells in the primate anterior cingulate cortex during an economic choice task. In the experiments, monkeys chose between different juices offered in variables amounts and subjective values were inferred from the animals' choices. We analyzed neuronal firing rates in relation to a large number of behaviorally relevant variables. We report three main results. First, there were robust differences between the dorsal bank (ACCd) and the ventral bank (ACCv) of the cingulate sulcus. Specifically, neurons in ACCd but not in ACCv were modulated by the movement direction. Furthermore, neurons in ACCd were most active before movement initiation, whereas neurons in ACCv were most active after juice delivery. Second, neurons in both areas encoded the identity and the subjective value of the juice chosen by the animal. In contrast, neither region encoded the value of individual offers. Third, the population of value-encoding neurons in both ACCd and ACCv underwent range adaptation. With respect to economic choice, it is interesting to compare these areas with the orbitofrontal cortex (OFC), previously examined. While neurons in OFC encoded both pre-decision and post-decision variables, neurons in ACCd and ACCv only encoded post-decision variables. Moreover, the encoding of the choice outcome (chosen value and chosen juice) in ACCd and ACCv trailed that found in OFC. These observations indicate that economic decisions (i.e., value comparisons) take place upstream of ACCd and ACCv. The coexistence of choice outcome and movement signals in ACCd suggests that this area constitutes a gateway through which the choice system informs motor systems.
Xinying Cai; Camillo Padoa-Schioppa
In: Neuron, 81 (5), pp. 1140–1151, 2014.
Previous work indicates that economic decisions can be made independently of the visuomotor contingencies of the choice task (space of goods). However, the neuronal mechanisms through which the choice outcome (the chosen good) is transformed into a suitable action plan remain poorly understood. Here we show that neurons in lateral prefrontal cortex reflect the early stages of this good-to-action transformation. Monkeys chose between different juices. The experimental design dissociated in space and time the presentation of the offers and the saccade targets associated with them. We recorded from the orbital, ventrolateral, and dorsolateral prefrontal cortices (OFC, LPFCv, and LPFCd, respectively). Prior to target presentation, neurons in both LPFCv and LPFCd encoded the choice outcome in goods space. After target presentation, they gradually came to encode the location of the targets and the upcoming action plan. Consistent with the anatomical connectivity, all spatial and action-related signals emerged in LPFCv before LPFCd.
Xinying Cai; Camillo Padoa-Schioppa
In: Nature Communications, 10 , pp. 393, 2019.
Previous work showed that economic decisions can be made independently of spatial contingencies. However, when goods available for choice bear different action costs, the decision necessarily reflects aspects of the action. One possibility is that "stimulus values" are combined with the corresponding action costs in a motor representation, and decisions are then made in actions space. Alternatively, action costs could be integrated with other determinants of value in a non-spatial representation. If so, decisions under variable action costs could take place in goods space. Here, we recorded from orbitofrontal cortex while monkeys chose between different juices offered in variable amounts. We manipulated action costs by varying the saccade amplitude, and we dissociated in time and space offer presentation from action planning. Neurons encoding the binary choice outcome did so well before the presentation of saccade targets, indicating that decisions were made in goods space.
Irene Caprara; Peter Janssen; Maria C Romero
In: Journal of Visualized Experiments, (138), pp. 1–10, 2018.
Previous studies have shown that neurons in parieto-frontal areas of the macaque brain can be highly selective for real-world objects, disparity-defined curved surfaces, and images of real-world objects (with and without disparity) in a similar manner as described in the ventral visual stream. In addition, parieto-frontal areas are believed to convert visual object information into appropriate motor outputs, such as the pre-shaping of the hand during grasping. To better characterize object selectivity in the cortical network involved in visuomotor transformations, we provide a battery of tests intended to analyze the visual object selectivity of neurons in parieto-frontal regions.
Irene Caprara; Elsie Premereur; Maria C Romero; Pedro Faria; Peter Janssen
In: NeuroImage, 179 , pp. 298–312, 2018.
The primate dorsal visual stream processes object shape to guide actions involving an object, but the transmission of shape information beyond posterior parietal cortex remains largely unknown. To clarify the information flow between parietal and frontal cortex, we applied electrical microstimulation during functional Magnetic Resonance Imaging (fMRI) in a shape-selective patch in the posterior part of the Anterior Intraparietal area (pAIP) to chart its connectivity. Subsequently, we recorded single-unit responses to images of objects in the fMRI activation in prefrontal cortex, corresponding to area 45B, elicited by pAIP microstimulation. Neurons in area 45B had properties similar to neurons in pAIP, responding selectively to shape contours and to very small shape fragments measuring less than one deg at exceedingly short latencies. However, contrary to the prevailing view on the hierarchical organization of cortical areas, neurons in area 45B preferred even smaller shape fragments and had smaller receptive fields than neurons in pAIP. These findings provide the first evidence for ultra-fast shape processing in prefrontal cortex, and suggest that the pathway from pAIP to area 45B may not be important for object grasping.
Valeria C Caruso; Daniel S Pages; Marc A Sommer; Jennifer M Groh
In: Journal of Neurophysiology, 115 (6), pp. 3162–3173, 2016.
Saccadic eye movements can be elic- ited by more than one type of sensory stimulus. This implies substantial transformations of signals originating in different sense organs as they reach a common motor output pathway. In this study, we compared the prevalence and magnitude of auditory- and visually evoked activity in a structure implicated in oculomotor processing, the primate frontal eye fields (FEF). We recorded from 324 single neurons while 2 monkeys performed delayed saccades to visual or auditory targets. We found that 64% of FEF neurons were active on presenta- tion of auditory targets and 87% were active during auditory-guided saccades, compared with 75 and 84% for visual targets and saccades. As saccade onset approached, the average level of population activity in the FEF became indistinguishable on visual and auditory trials. FEF activity was better correlated with the movement vector than with the target location for both modalities. In summary, the large proportion of auditory-responsive neurons in the FEF, the similarity between visual and auditory activity levels at the time of the saccade, and the strong correlation between the activity and the saccade vector suggest that auditory signals undergo tailoring to match roughly the strength of visual signals present in the FEF, facilitating accessing of a common motor output pathway.
Aaron L Cecala; Ivan Smalianchuk; Sanjeev B Khanna; Matthew A Smith; Neeraj J Gandhi
In: Journal of Neurophysiology, 114 (1), pp. 570–584, 2015.
When the head does not move, rapid movements of the eyes called saccades are used to redirect the line of sight. Saccades are defined by a series of metrical and kinematic (evolution of a movement as a function of time) relationships. For example, the amplitude of a saccade made from one visual target to another is roughly 90% of the distance between the initial fixation point (T0) and the peripheral target (T1). However, this stereotypical relationship between saccade amplitude and initial retinal error (T1-T0) may be altered, either increased or decreased, by surreptitiously displacing a visual target during an ongoing saccade. This form of motor learning (called saccadic adaptation) has been described in both humans and monkeys. Recent experiments in humans and monkeys have suggested that internal (proprioceptive) and external (target shape, color, and/or motion) cues may be used to produce context-dependent adaptation. We tested the hypothesis that an external contextual cue (target color) could be used to evoke differential gain (actual saccade/initial retinal error) states in rhesus monkeys. We did not observe differential gain states correlated with target color regardless of whether targets were displaced along the same vector as the primary saccade or perpendicular to it. Furthermore, this observation held true regardless of whether adaptation trials using various colors and intrasaccade target displacements were randomly intermixed or presented in short or long blocks of trials. These results are consistent with hypotheses that state that color cannot be used as a contextual cue and are interpreted in light of previous studies of saccadic adaptation in both humans and monkeys.
Jason L Chan; Michael J Koval; Thilo Womelsdorf; Stephen G Lomber; Stefan Everling
In: Cerebral Cortex, 25 (12), pp. 4704–4714, 2015.
Cognitive control requires the selection and maintenance of task-relevant stimulus-response associations, or rules. The dorsolateral prefrontal cortex (DLPFC) has been implicated by lesion, functional imaging, and neurophysiological studies to be involved in encoding rules, but the mechanisms by which it modulates other brain areas are poorly understood. Here, the functional relationship of the DLPFC with the superior colliculus (SC) was investigated by bilaterally deactivating the DLPFC while recording local field potentials (LFPs) in the SC in monkeys performing an interleaved pro- and antisaccade task. Event-related LFPs showed differences between pro- and antisaccades and responded prominently to stimulus presentation. LFP power after stimulus onset was higher for correct saccades than erroneous saccades. Deactivation of the DLPFC did not affect stimulus onset related LFP activity, but reduced high beta (20-30 Hz) and high gamma (60-150 Hz) power during the preparatory period for both pro- and antisaccades. Spike rate during the preparatory period was positively correlated with gamma power and this relationship was attenuated by DLPFC deactivation. These results suggest that top-down control of the SC by the DLPFC may be mediated by beta oscillations.
Jason L Chan; Michael J Koval; Kevin D Johnston; Stefan Everling
In: Journal of Neurophysiology, 118 , pp. 2156–2170, 2017.
Successful task switching requires a network of brain areas to select, maintain, implement, and execute the appropriate task. Although frontoparietal brain areas are thought to play a critical role in task switching by selecting and encoding task rules and exerting top-down control, how brain areas closer to the execution of tasks participate in task switching is unclear. The superior colliculus (SC) integrates information from various brain areas to generate saccades and is likely influenced by task switching. Here, we investigated switch costs in nonhuman primates and their neural correlates in the activity of SC saccade-related neurons in monkeys performing cued, randomly interleaved pro- and anti-saccade trials. We predicted that behavioral switch costs would be associated with differential modulations of SC activity in trials on which the task was switched vs. repeated, with activity on the current trial resembling that associated with the task set of the previous trial when a switch occurred. We observed both error rate and reaction time switch costs and changes in the discharge rate and timing of activity in SC neurons between switch and repeat trials. These changes were present later in the task only after fixation on the cue stimuli but before saccade onset. These results further establish switch costs in macaque monkeys and suggest that SC activity is modulated by task-switching processes in a manner inconsistent with the concept of task set inertia.
Steve W C Chang; Amy A Winecoff; Michael L Platt
Vicarious reinforcement in rhesus macaques (Macaca mulatta) Journal Article
In: Frontiers in Neuroscience, 5 , pp. 1–10, 2011.
What happens to others profoundly influences our own behavior. Such other-regarding outcomes can drive observational learning, as well as motivate cooperation, charity, empathy, and even spite. Vicarious reinforcement may serve as one of the critical mechanisms mediating the influence of other-regarding outcomes on behavior and decision-making in groups. Here we show that rhesus macaques spontaneously derive vicarious reinforcement from observing rewards given to another monkey, and that this reinforcement can motivate them to subsequently deliver or withhold rewards from the other animal. We exploited Pavlovian and instrumental conditioning to associate rewards to self (M1) and/or rewards to another monkey (M2) with visual cues. M1s made more errors in the instrumental trials when cues predicted reward to M2 compared to when cues predicted reward to M1, but made even more errors when cues predicted reward to no one. In subsequent preference tests between pairs of conditioned cues, M1s preferred cues paired with reward to M2 over cues paired with reward to no one. By contrast, M1s preferred cues paired with reward to self over cues paired with reward to both monkeys simultaneously. Rates of attention to M2 strongly predicted the strength and valence of vicarious reinforcement. These patterns of behavior, which were absent in non-social control trials, are consistent with vicarious reinforcement based upon sensitivity to observed, or counterfactual, outcomes with respect to another individual. Vicarious reward may play a critical role in shaping cooperation and competition, as well as motivating observational learning and group coordination in rhesus macaques, much as it does in humans. We propose that vicarious reinforcement signals mediate these behaviors via homologous neural circuits involved in reinforcement learning and decision-making.
Steve W C Chang; Joseph W Barter; Becket R Ebitz; Karli K Watson; Michael L Platt
In: Proceedings of the National Academy of Sciences, 109 (3), pp. 959–964, 2012.
People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms.
Steve W C Chang; Jean-François Gariépy; Michael L Platt
In: Nature Neuroscience, 16 (2), pp. 243–250, 2013.
Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.
Steve W C Chang; Nicholas A Fagan; Koji Toda; Amanda V Utevsky; John M Pearson; Michael L Platt
In: Proceedings of the National Academy of Sciences, 112 (52), pp. 16012–16017, 2015.
SignificanceMaking social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions. Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.
Ting Yu Chang; Raymond Doudlah; Byounghoon Kim; Adhira Sunkara; Lowell W Thompson; Meghan E Lowe; Ari Rosenberg
In: eLife, 9 , pp. 1–27, 2020.
Three-dimensional (3D) representations of the environment are often critical for selecting actions that achieve desired goals. The success of these goal-directed actions relies on 3D sensorimotor transformations that are experience-dependent. Here we investigated the relationships between the robustness of 3D visual representations, choice-related activity, and motor-related activity in parietal cortex. Macaque monkeys performed an eight-alternative 3D orientation discrimination task and a visually guided saccade task while we recorded from the caudal intraparietal area using laminar probes. We found that neurons with more robust 3D visual representations preferentially carried choice-related activity. Following the onset of choice-related activity, the robustness of the 3D representations further increased for those neurons. We additionally found that 3D orientation and saccade direction preferences aligned, particularly for neurons with choice-related activity, reflecting an experience-dependent sensorimotor association. These findings reveal previously unrecognized links between the fidelity of ecologically relevant object representations, choice-related activity, and motor-related activity.
Ting Yu Chang; Lowell Thompson; Raymond Doudlah; Byounghoon Kim; Adhira Sunkara; Ari Rosenberg
In: eNeuro, 7 (1), pp. 1–18, 2020.
Reconstructing three-dimensional (3D) scenes from two-dimensional (2D) retinal images is an ill-posed problem. Despite this, 3D perception of the world based on 2D retinal images is seemingly accurate and precise. The integration of distinct visual cues is essential for robust 3D perception in humans, but it is unclear whether this is true for non-human primates (NHPs). Here, we assessed 3D perception in macaque monkeys using a planar surface orientation discrimination task. Perception was accurate across a wide range of spatial poses (orientations and distances), but precision was highly dependent on the plane's pose. The monkeys achieved robust 3D perception by dynamically reweighting the integration of stereoscopic and perspective cues according to their pose-dependent reliabilities. Errors in performance could be explained by a prior resembling the 3D orientation statistics of natural scenes. We used neural network simulations based on 3D orientation-selective neurons recorded from the same monkeys to assess how neural computation might constrain perception. The perceptual data were consistent with a model in which the responses of two independent neuronal populations representing stereoscopic cues and perspective cues (with perspective signals from the two eyes combined using nonlinear canonical computations) were optimally integrated through linear summation. Perception of combined-cue stimuli was optimal given this architecture. However, an alternative architecture in which stereoscopic cues, left eye perspective cues, and right eye perspective cues were represented by three independent populations yielded two times greater precision than the monkeys. This result suggests that, due to canonical computations, cue integration for 3D perception is optimized but not maximized.
Mircea I Chelaru; Valentin Dragoi
Negative correlations in visual cortical networks Journal Article
In: Cerebral Cortex, 26 (1), pp. 246–256, 2016.
The amount of information encoded by cortical circuits depends critically on the capacity of nearby neurons to exhibit trial-to-trial (noise) correlations in their responses. Depending on their sign and relationship to signal correlations, noise correlations can either increase or decrease the population code accuracy relative to uncorrelated neuronal firing. Whereas positive noise correlations have been extensively studied using experimental and theoretical tools, the functional role of negative correlations in cortical circuits has remained elusive. We addressed this issue by performing multiple-electrode recording in the superficial layers of the primary visual cortex (V1) of alert monkey. Despite the fact that positive noise correlations decayed exponentially with the difference in the orientation preference between cells, negative correlations were uniformly distributed across the population. Using a statistical model for Fisher Information estimation, we found that a mild increase in negative correlations causes a sharp increase in network accuracy even when mean correlations were held constant. To examine the variables controlling the strength of negative correlations, we implemented a recurrent spiking network model of V1. We found that increasing local inhibition and reducing excitation causes a decrease in the firing rates of neurons while increasing the negative noise correlations, which in turn increase the population signal-to-noise ratio and network accuracy. Altogether, these results contribute to our understanding of the neuronal mechanism involved in the generation of negative correlations and their beneficial impact on cortical circuit function.
Xiaodong Chen; Feng Han; Mu-ming Poo; Yang Dan
In: Proceedings of the National Academy of Sciences, 104 (48), pp. 19120–19125, 2007.
An essential step in understanding visual processing is to characterize the neuronal receptive fields (RFs) at each stage of the visual pathway. However, RF characterization beyond simple cells in the primary visual cortex (V1) remains a major challenge. Recent application of spike-triggered covariance (STC) analysis has greatly facilitated characterization of complex cell RFs in anesthetized animals. Here we apply STC to RF characterization in awake monkey V1. We found up to nine subunits for each cell, including one or two dominant excitatory subunits as described by the standard model, along with additional excitatory and suppressive subunits with weaker contributions. Compared with the dominant subunits, the nondominant excitatory subunits prefer similar orientations and spatial frequencies but have larger spatial envelopes. They contribute to response invariance to small changes in stimulus orientation, position, and spatial frequency. In contrast, the suppressive subunits are tuned to orientations 45 degrees -90 degrees different from the excitatory subunits, which may underlie cross-orientation suppression. Together, the excitatory and suppressive subunits form a compact description of RFs in awake monkey V1, allowing prediction of the responses to arbitrary visual stimuli.
Xiaomo Chen; Katherine Wilson Scangos; Veit Stuphorn
In: Journal of Neuroscience, 30 (44), pp. 14657–14675, 2010.
Adaptive behavior requires the ability to flexibly control actions. This can occur either proactively to anticipate task requirements, or reactively in response to sudden changes. Here we report neuronal activity in the supplementary motor area (SMA) that is correlated with both forms of behavioral control. Single-unit and multiunit activity and intracranial local field potentials (LFPs) were recorded in macaque monkeys during a stop-signal task, which elicits both proactive and reactive behavioral control. The LFP power in high- (60-150 Hz) and low- (25-40 Hz) frequency bands was significantly correlated with arm movement reaction time, starting before target onset. Multiunit and single-unit activity also showed a significant regression with reaction time. In addition, LFPs and multiunit and single-unit activity changed their activity level depending on the trial history, mirroring adjustments on the behavioral level. Together, these findings indicate that neuronal activity in the SMA exerts proactive control of arm movements by adjusting the level of motor readiness. On trials when the monkeys successfully canceled arm movements in response to an unforeseen stop signal, the LFP power, particularly in a low (10-50 Hz) frequency range, increased early enough to be causally related to the inhibition of the arm movement on those trials. This indicated that neuronal activity in the SMA is also involved in response inhibition in reaction to sudden task changes. Our findings indicate, therefore, that SMA plays a role in the proactive control of motor readiness and the reactive inhibition of unwanted movements.
Chih Yang Chen; Ziad M Hafed
Postmicrosaccadic enhancement of slow eye movements Journal Article
In: Journal of Neuroscience, 33 (12), pp. 5375–5386, 2013.
Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades.
Ming Chen; Peichao Li; Shude Zhu; Chao Han; Haoran Xu; Yang Fang; Jiaming Hu; Anna W Roe; Haidong D Lu
An orientation map for motion boundaries in macaque V2 Journal Article
In: Cerebral Cortex, 26 (1), pp. 279–287, 2016.
The ability to extract the shape of moving objects is fundamental to visual perception. However, where such computations are processed in the visual system is unknown. To address this question, we used intrinsic signal optical imaging in awake monkeys to examine cortical response to perceptual contours defined by motion contrast (motion boundaries, MBs). We found that MB stimuli elicit a robust orientation response in area V2. Orientation maps derived from subtraction of orthogonal MB stimuli aligned well with the orientation maps obtained with luminance gratings (LGs). In contrast, area V1 responded well to LGs, but exhibited a much weaker orientation response to MBs. We further show that V2 direction domains respond to motion contrast, which is required in the detection of MB in V2. These results suggest that V2 represents MB information, an important prerequisite for shape recognition and figure-ground segregation.
Chih Yang Chen; Lukas Sonnenberg; Simone Weller; Thede Witschel; Ziad M Hafed
Spatial frequency sensitivity in macaque midbrain Journal Article
In: Nature Communications, 9 , pp. 2852, 2018.
Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. However, visual sensation is an active process, and if there are any brain areas that ought to be particularly in tune with natural scene statistics, it would be sensory-motor areas critical for guiding behavior. Here we found that the rhesus macaque superior colliculus, a structure instrumental for rapid visual exploration with saccades, detects low spatial frequencies, which are the most prevalent in natural scenes, much more rapidly than high spatial frequencies. Importantly, this accelerated detection happens independently of whether a neuron is more or less sensitive to low spatial frequencies to begin with. At the population level, the superior colliculus additionally over-represents low spatial frequencies in neural response sensitivity, even at near-foveal eccentricities. Thus, the superior colliculus possesses both temporal and response gain mechanisms for efficient gaze realignment in low-spatial-frequency-dominated natural environments.
Chih Yang Chen; Klaus Peter Hoffmann; Claudia Distler; Ziad M Hafed
In: Current Biology, 29 (13), pp. 2109–2119, 2019.
A defining feature of the primate visual system is its foveated nature. Processing of foveal retinal input is important not only for high-quality visual scene analysis but also for ensuring precise, albeit tiny, gaze shifts during high-acuity visual tasks. The representations of foveal retinal input in the primate lateral geniculate nucleus and early visual cortices have been characterized. However, how such representations translate into precise eye movements remains unclear. Here, we document functional and structural properties of the foveal visual representation of the midbrain superior colliculus. We show that the superior colliculus, classically associated with extra-foveal spatial representations needed for gaze shifts, is highly sensitive to visual input impinging on the fovea. The superior colliculus also represents such input in an orderly and very specific manner, and it magnifies the representation of foveal images in neural tissue as much as the primary visual cortex does. The primate superior colliculus contains a high-fidelity visual representation, with large foveal magnification, perfectly suited for active visuomotor control and perception. Chen et al. show that superior colliculus (SC) is highly sensitive to foveal visual input and that it magnifies foveal image representation much more than previously anticipated. Their topography data, with large foveal magnification, show that tiny foveal stimuli can activate a large portion of SC neural tissue due to fixational eye movements.
Chih-Yang Chen; Denis Matrov; Richard Veale; Hirotaka Onoe; Masatoshi Yoshida; Kenichiro Miura; Tadashi Isa
In: Journal of Neurophysiology, 2020.
The saccade is a stereotypic behavior whose investigation improves our understanding of how primate brains implement precise motor control. Furthermore, saccades offer an important window into the cognitive and attentional state of the brain. Historically, saccade studies have largely relied on macaque. However, the cortical network giving rise to the saccadic command is difficult to study in macaque because relevant cortical areas lie in sulci and are difficult to access. Recently, a New World monkey – the marmoset – has garnered attention as an attractive alternative to macaque because of its smooth cortical surface, its smaller body, and its amenability to transgenic technology. However, adoption of marmoset for oculomotor research has been limited due to a lack of in-depth descriptions of marmoset saccade kinematics and their ability to perform psychophysical and cognitive tasks. Here, we directly compare free-viewing and visually-guided behavior of marmoset, macaque, and human engaged in identical tasks under similar conditions. In video free-viewing task, all species exhibited qualitatively similar saccade kinematics including saccade main sequence up to 25° in amplitude. Furthermore, the conventional bottom-up saliency model predicted gaze targets at similar rates for all species. We further verified their visually-guided behavior by training them with step and gap saccade tasks. All species showed similar gap effect and express saccades in the gap paradigm. Our results suggest that the three species have similar natural and task-guided visuomotor behavior. The marmoset can be trained on saccadic tasks and thus can serve as a model for oculomotor, attention, and cognitive research.
Xiaomo Chen; Marc Zirnsak; Gabriel M Vega; Eshan Govil; Stephen G Lomber; Tirin Moore
In: Neuron, 106 (1), pp. 177–187, 2020.
Unique stimuli stand out. Despite an abundance of competing sensory stimuli, the detection of the most salient ones occurs without effort, and that detection contributes to theguidanceof adaptive behavior. Neurons sensitive to the salience of visual stimuli are wide-spread throughout the primate visual system and are thought to shape the selection of visual targets. However, a neural source of salience remains elusive. In an attempt to identify a source of visual salience, we reversibly inactivated parietal cortex and simultaneously recorded salience signals in prefrontal cortex. Inactivation of parietal cortex not only caused pronounced and selective reductions of salience signals in prefrontal cortex but also diminished the influence of salience on visually guided behavior. These observations demonstrate a causal role of parietal cortex in regulating salience signals within the brain and in controlling salience-driven behavior.
Xiaomo Chen; Marc Zirnsak; Gabriel M Vega; Tirin Moore
In: Progress in Neurobiology, 195 , pp. 1–10, 2020.
The consequences of individual actions are typically unknown until well after they are executed. This fact necessitates a mechanism that bridges delays between specific actions and reward outcomes. We looked for the presence of such a mechanism in the post-movement activity of neurons in the frontal eye field (FEF), a visuomotor area in prefrontal cortex. Monkeys performed an oculomotor gamble task in which they made eye movements to different locations associated with dynamically varying reward outcomes. Behavioral data showed that monkeys tracked reward history and made choices according to their own risk preferences. Consistent with previous studies, we observed that the activity of FEF neurons is correlated with the expected reward value of different eye movements before a target appears. Moreover, we observed that the activity of FEF neurons continued to signal the direction of eye movements, the expected reward value, and their interaction well after the movements were completed and when targets were no longer within the neuronal response field. In addition, this post-movement information was also observed in local field potentials, particularly in low-frequency bands. These results show that neural signals of prior actions and expected reward value persist across delays between those actions and their experienced outcomes. These memory traces may serve a role in reward-based learning in which subjects need to learn actions predicting delayed reward.
Hoseok Choi; Seho Lee; Jeyeon Lee; Kyeongran Min; Seokbeen Lim; Jinsick Park; Kyoung ha Ahn; In Young Kim; Kyoung-Min Lee; Dong Pyo Jang
In: Journal of Neuroscience Methods, 308 , pp. 261–268, 2018.
Background: A screw-shaped electrode can offer a compromise between signal quality and invasiveness. However, the standard screw electrode can be vulnerable to electrical noise while directly contact with the skull or skin, and the feasibility and stability for chronic implantation in primate have not been fully evaluated. New Method: We designed a novel screw electrocorticogram (ECoG) electrode composed of three parts: recording electrode, insulator, and nut. The recording electrode was made of titanium with high biocompatibility and high electrical conductivity. Zirconia is used for insulator and nut to prevent electrical noise. Result: In computer simulations, the screw ECoG with insulator showed a significantly higher performance in signal acquisition compared to the condition without insulator. In a non-human primate, using screw ECoG, clear visual-evoked potential (VEP) waveforms were obtained, VEP components were reliably maintained, and the electrode's impedance was stable during the whole evaluation period. Moreover, it showed higher SNR and wider frequency band compared to the electroencephalogram (EEG). We also observed the screw ECoG has a higher sensitivity that captures different responses on various stimuli than the EEG. Comparison: The screw ECoG showed reliable electrical characteristic and biocompatibility for three months, that shows great promise for chronic implants. These results contrasted with previous reports that general screw electrode was only applicable for acute applications. Conclusion: The suggested electrode can offer whole-brain monitoring with high signal quality and minimal invasiveness. The screw ECoG can be used to provide more in-depth understanding, not only relationship between functional networks and cognitive behavior, but also pathomechanisms in brain diseases.
Jan Churan; Farhan A Khawaja; James M G Tsui; Christopher C Pack
In: Current Biology, 18 (22), pp. 1–6, 2008.
Intuitively one might think that larger objects should be easier to see, and indeed performance on visual tasks generally improves with increasing stimulus size [1,2]. Recently, a remarkable exception to this rule was reported : when a high-contrast, moving stimulus is presented very briefly, motion perception deteriorates as stimulus size increases. This psychophysical surround suppression has been interpreted as a correlate of the neuronal surround suppression that is commonly found in the visual cortex [3-5]. However, many visual cortical neurons lack surround suppression, and so one might expect that the brain would simply use their outputs to discriminate the motion of large stimuli. Indeed previous work has generally found that observers rely on whichever neurons are most informative about the stimulus to perform similar psychophysical tasks . Here we show that the responses of neurons in the middle temporal (MT) area of macaque monkeys provide a simple resolution to this paradox. We find that surround-suppressed MT neurons integrate motion signals relatively quickly, so that by comparison non-suppressed neurons respond poorly to brief stimuli. Thus, psychophysical surround suppression for brief stimuli can be viewed as a consequence of a strategy that weights neuronal responses according to how informative they are about a given stimulus. If this interpretation is correct, then it follows that any psychophysical experiment that uses brief motion stimuli will effectively probe the responses of MT neurons that have strong surround suppression.
Jan Churan; Daniel Guitton; Christopher C Pack
In: Journal of Neurophysiology, 106 (4), pp. 1862–1874, 2011.
Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.
Jan Churan; Daniel Guitton; Christopher C Pack
In: PLoS ONE, 7 (12), pp. e52195, 2012.
Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.
Jan Churan; Doris I Braun; Karl R Gegenfurtner; Frank Bremmer
In: Journal of Eye Movement Research, 11 (4), pp. 1–15, 2018.
Direct comparison of results of humans and monkeys is often complicated by differences in experimental conditions. We replicated in head unrestrained macaques experiments of a recent study comparing human directional precision during smooth pursuit eye movements (SPEM) and saccades to moving targets (Braun & Gegenfurtner, 2016). Directional precision of human SPEM follows an exponential decay function reaching optimal values of 1.5°-3° within 300 ms after target motion onset, whereas precision of initial saccades to moving targets is slightly better. As in humans, we found general agreement in the development of directional precision of SPEM over time and in the differences between directional precision of initial saccades and SPEM initiation. However, monkeys showed overall lower precision in SPEM compared to humans. This was most likely due to differences in experimental conditions, such as in the stabilization of the head, which was by a chin and a head rest in human subjects and unrestrained in monkeys.
Evy Cleeren; Cindy Casteels; Karolien Goffin; Peter Janssen; Wim Van Paesschen
In: Epilepsia, 56 (9), pp. 1366–1375, 2015.
OBJECTIVE: Amygdala kindling is a widely used animal model for studying mesial temporal lobe epileptogenesis. In the macaque monkey, electrical amygdala kindling develops slowly and provides an opportunity for investigating ictal perfusion changes during epileptogenesis. METHODS: Two rhesus monkeys were electrically kindled through chronically implanted electrodes in the right amygdala over a period of 16 and 17 months. Ictal perfusion single photon emission computed tomography (SPECT) imaging was performed during each of the four predefined clinical stages. RESULTS: Afterdischarge duration increased slowly over 477 days for monkey K and 515 days for monkey S (18 ± 8 s in stage I; 52 ± 13 s in stage IV). During this time, the animals progressed through four clinical stages ranging from interrupting ongoing behavior to bilateral convulsions. Ictal SPECT perfusion imaging showed well-localized but widely distributed regions of hyperperfusion and hypoperfusion, in both cortical and subcortical structures, at every seizure stage. A large portion of the ictal network was involved in the early stages of epileptogenesis and subsequently expanded over time as seizure severity evolved. SIGNIFICANCE: Our data indicate that the different mesial temporal lobe seizure types occur within a common network affecting several parts of the brain, and that seizure severity may be determined by seizure-induced epileptogenesis within a bihemispheric network that is implicated from the start of the process.
E Cleeren; I D Popivanov; W Van Paesschen; Peter Janssen
In: Scientific Reports, 10 , pp. 1–11, 2020.
Visual information reaches the amygdala through the various stages of the ventral visual stream. There is, however, evidence that a fast subcortical pathway for the processing of emotional visual input exists. To explore the presence of this pathway in primates, we recorded local field potentials in the amygdala of four rhesus monkeys during a passive fixation task showing images of ten object categories. Additionally, in one of the monkeys we also obtained multi-unit spiking activity during the same task. We observed remarkably fast medium and high gamma responses in the amygdala of the four monkeys. These responses were selective for the different stimulus categories, showed within-category selectivity, and peaked as early as 60 ms after stimulus onset. Multi-unit responses in the amygdala were lagging the gamma responses by about 40 ms. Thus, these observations add further evidence that selective visual information reaches the amygdala of nonhuman primates through a very fast route.
Michael Colombo; James S Magnuson
In: Journal of Experimental Psychology: Animal Learning and Cognition, 40 (2), pp. 178–184, 2014.
On sequential response tasks, a long pause preceding the first response is thought to reflect participants taking time to plan a sequence of responses. By tracking the eye movements of two monkeys (Macaca fascicularis), Scarf and Colombo (2009, Eye Movements During List Execution Reveal No Planning in Monkeys [Macaca fascicularis], Journal of Experimental Psychology: Animal Behavior Processes, Vol. 35, pp. 587–592) demonstrated that, at least with respect to monkeys, the long pause preceding the first response is not necessarily the product of planning. In the present experiment, we tracked the eye movements of adult humans using the paradigm employed by Scarf and Colombo and found that, in contrast to monkeys, the pause preceding the first item is indicative of planning in humans. These findings highlight the fact that similar response time profiles, displayed by human and nonhuman animals, do not necessarily reflect similar underlying cognitive operations.
Katherine E Conen; X Camillo Padoa-Schioppa
In: Journal of Neuroscience, 39 (18), pp. 3498 –3513, 2019.
Values available for choice in different behavioral contexts can vary immensely. To compensate for this variability, neuronal circuits underlying economic decisions undergo adaptation. In orbitofrontal cortex (OFC), neurons encode the subjective value of offered and chosen goods in a quasilinear way. Previous experiments found that the gain of the encoding is lower when the value range is wider. However, the parameters OFC neurons adapted to remained unclear. Furthermore, previous studies did not examine additive changes in neuronal responses. Computational considerations indicate that these factors can directly impact choice behavior. Here we investigated how OFC neurons adapt to changes in the value range. We recorded from two male rhesus monkeys during a juice choice task. Each session was divided into two blocks of trials. In each block, juices were offered within a set range of values, and ranges changed between blocks. Across blocks, neuronal responses adapted to both the maximum and the minimum value, but only partially. As a result, the minimum neural activity was elevated in some value ranges relative to others. Through simulation of a linear decision model, we showed that increasing the minimum response increases choice variability, lowering the expected payoff. This effect is modulated by the balance between cells with positive and negative encoding. The presence of these two populations induces a non-monotonic relationship between the value range and choice efficacy, such that the expected payoff is highest for decisions in an intermediate value range.
Benjamin W Corrigan; Roberto A Gulli; Guillaume Doucet; Julio C Martinez-Trujillo
In: Journal of Vision, 17 (12), pp. 1–22, 2017.
Virtual environments (VE) allow testing complex behaviors in naturalistic settings by combining highly controlled visual stimuli with spatial navigation and other cognitive tasks. They also allow for the recording of eye movements using high-precision eye tracking techniques, which is important in electrophysiological studies examining the response properties of neurons in visual areas of nonhuman primates. However, during virtual navigation, the pattern of retinal stimulation can be highly dynamic which may influence eye movements. Here we examine whether and how eye movement patterns change as a function of dynamic visual stimulation during virtual navigation tasks, relative to standard oculomotor tasks. We trained two rhesus macaques to use a joystick to navigate in a VE to complete two tasks. To contrast VE behavior with classic measurements, the monkeys also performed a simple Cued Saccade task. We used a robust algorithm for rapid classification of saccades, fixations, and smooth pursuits. We then analyzed the kinematics of saccades during all tasks, and specifically during different phases of the VE tasks. We found that fixation to smooth pursuit ratios were smaller in VE tasks (4:5) compared to the Cued Saccade task (7:1), reflecting a more intensive use of smooth pursuit to foveate targets in VE than in a standard visually guided saccade task or during spontaneous fixations. Saccades made to rewarded targets (exploitation) tended to have increased peak velocities compared to saccades made to unrewarded objects (exploration). VE exploitation saccades were 6% slower than saccades to discrete targets in the Cued Saccade task. Virtual environments represent a technological advance in experimental design for nonhuman primates. Here we provide a framework to study the ways that eye movements change between and within static and dynamic displays.