EyeLink Non-Human Primate Publications
All EyeLink non-human primate research publications up until 2021 (with some early 2022s) are listed below by year. You can search the publications using keywords such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate articles, please email us!
2020 |
Kaleb A. Lowe; Wolf Zinke; Anthony M. Phipps; Josh Cosman; Micala Maddox; Jeffrey D. Schall; Charles F. Caskey Visuomotor transformations are modulated by focused ultrasound over frontal eye field Journal Article In: Ultrasound in Medicine & Biology, pp. 1–14, 2020. @article{Lowe2020,Neuromodulation with focused ultrasound (FUS) is being widely explored as a non-invasive tool to stimulate focal brain regions because of its superior spatial resolution and coverage compared with other neuro- modulation methods. The precise effects of FUS stimulation on specific regions of the brain are not yet fully understood. Here, we characterized the behavioral effects of FUS stimulation directly applied through a craniot- omy over the macaque frontal eye field (FEF). In macaque monkeys making directed eye movements to perform visual search tasks with direct or arbitrary responses, focused ultrasound was applied through a craniotomy over the FEF. Saccade response times (RTs) and error rates were determined for trials without or with FUS stim- ulation with pulses at a peak negative pressure of either 250 or 425 kPa. Both RTs and error rates were affected by FUS. Responses toward a target located contralateral to the FUS stimulation were approximately 3 ms slower in the presence of FUS in both monkeys studied, while only one exhibited a slowing of responses for ipsilateral targets. Error rates were lower in one monkey in this study. In another search task requiring making eye move- ments toward a target (pro-saccades) or in the opposite direction (anti-saccades), the RT for pro-saccades increased in the presence of FUS stimulation. Our results indicate the effectiveness of FUS to modulate saccadic responses when stimulating FEF in awake, behaving non-human primates. (E-mail: |
Liya Ma; Janahan Selvanayagam; Maryam Ghahremani; Lauren K. Hayrynen; Kevin D. Johnston; Stefan Everling Single-unit activity in marmoset posterior parietal cortex in a gap saccade task Journal Article In: Journal of Neurophysiology, vol. 123, no. 3, pp. 896–911, 2020. @article{Ma2020,Abnormal saccadic eye movements can serve as biomarkers for patients with several neuropsychiatric disorders. The common marmoset (Callithrix jacchus) is becoming increasingly popular as a nonhuman primate model to investigate the cortical mechanisms of saccadic control. Recently, our group demonstrated that microstimulation in the posterior parietal cortex (PPC) of marmosets elicits contralateral saccades. Here we recorded single-unit activity in the PPC of the same two marmosets using chronic microelectrode arrays while the monkeys performed a saccadic task with gap trials (target onset lagged fixation point offset by 200 ms) interleaved with step trials (fixation point disappeared when the peripheral target appeared). Both marmosets showed a gap effect, shorter saccadic reaction times (SRTs) in gap vs. step trials. On average, stronger gap-period responses across the entire neuronal population preceded shorter SRTs on trials with contralateral targets although this correlation was stronger among the 15% “gap neurons,” which responded significantly during the gap. We also found 39% “target neurons” with significant saccadic target-related responses, which were stronger in gap trials and correlated with the SRTs better than the remaining neurons. Compared with saccades with relatively long SRTs, short-SRT saccades were preceded by both stronger gap-related and target-related responses in all PPC neurons, regardless of whether such response reached significance. Our findings suggest that the PPC in the marmoset contains an area that is involved in the modulation of saccadic preparation. NEW & NOTEWORTHY As a primate model in systems neuroscience, the marmoset is a great complement to the macaque monkey because of its unique advantages. To identify oculomotor networks in the marmoset, we recorded from the marmoset posterior parietal cortex during a saccadic task and found single-unit activities consistent with a role in saccadic modulation. This finding supports the marmoset as a valuable model for studying oculomotor control. |
Tatiana Malevich; Antimo Buonocore; Ziad M. Hafed Rapid stimulus-driven modulation of slow ocular position drifts Journal Article In: eLife, vol. 9, pp. 1–22, 2020. @article{Malevich2020,The eyes are never still during maintained gaze fixation. When microsaccades are not occurring, ocular position exhibits continuous slow changes, often referred to as drifts. Unlike microsaccades, drifts remain to be viewed as largely random eye movements. Here we found that ocular position drifts can, instead, be very systematically stimulus-driven, and with very short latencies. We used highly precise eye tracking in three well trained macaque monkeys and found that even fleeting ($sim$8 ms duration) stimulus presentations can robustly trigger transient and stimulus-specific modulations of ocular position drifts, and with only approximately 60 ms latency. Such drift responses are binocular, and they are most effectively elicited with large stimuli of low spatial frequency. Intriguingly, the drift responses exhibit some image pattern selectivity, and they are not explained by convergence responses, pupil constrictions, head movements, or starting eye positions. Ocular position drifts have very rapid access to exogenous visual information. |
Vahid Mehrpour; Julio C. Martinez-Trujillo; Stefan Treue Attention amplifies neural representations of changes in sensory input at the expense of perceptual accuracy Journal Article In: Nature Communications, vol. 11, pp. 2128, 2020. @article{Mehrpour2020,Attention enhances the neural representations of behaviorally relevant stimuli, typically by a push–pull increase of the neuronal response gain to attended vs. unattended stimuli. This selectively improves perception and consequently behavioral performance. However, to enhance the detectability of stimulus changes, attention might also distort neural representations, compromising accurate stimulus representation. We test this hypothesis by recording neural responses in the visual cortex of rhesus monkeys during a motion direction change detection task. We find that attention indeed amplifies the neural representation of direction changes, beyond a similar effect of adaptation. We further show that humans overestimate such direction changes, providing a perceptual correlate of our neurophysiological observations. Our results demonstrate that attention distorts the neural representations of abrupt sensory changes and consequently perceptual accuracy. This likely represents an evolutionary adaptive mechanism that allows sensory systems to flexibly forgo accurate representation of stimulus features to improve the encoding of stimulus change. |
Jeff T. Mohl; John M. Pearson; Jennifer M. Groh Monkeys and humans implement causal inference to simultaneously localize auditory and visual stimuli Journal Article In: Journal of Neurophysiology, vol. 124, no. 3, pp. 715–727, 2020. @article{Mohl2020,The environment is sampled by multiple senses, which are woven together to produce a unified perceptual state. However, optimally unifying such signals requires assigning particular signals to the same or different underlying objects or events. Many prior studies (especially in animals) have assumed fusion of cross-modal information, whereas recent work in humans has begun to probe the appropriateness of this assumption. Here we present results from a novel behavioral task in which both monkeys (Macaca mulatta) and humans localized visual and auditory stimuli and reported their perceived sources through saccadic eye movements. When the locations of visual and auditory stimuli were widely separated, subjects made two saccades, while when the two stimuli were presented at the same location they made only a single saccade. Intermediate levels of separation produced mixed response patterns: a single saccade to an intermediate position on some trials or separate saccades to both locations on others. The distribution of responses was well described by a hierarchical causal inference model that accu- rately predicted both the explicit “same vs. different” source judg- ments as well as biases in localization of the source(s) under each of these conditions. The results from this task are broadly consistent with prior work in humans across a wide variety of analogous tasks, extending the study of multisensory causal inference to nonhuman primates and to a natural behavioral task with both a categorical assay of the number of perceived sources and a continuous report of the perceived position of the stimuli. |
Atsushi Noritake; Taihei Ninomiya; Masaki Isoda Representation of distinct reward variables for self and other in primate lateral hypothalamus Journal Article In: Proceedings of the National Academy of Sciences, vol. 117, no. 10, pp. 5516–5524, 2020. @article{Noritake2020,The lateral hypothalamus (LH) has long been implicated in maintaining behavioral homeostasis essential for the survival of an individual. However, recent evidence suggests its more widespread roles in behavioral coordination, extending to the social domain. The neuronal and circuit mechanisms behind the LH processing of social information are unknown. Here, we show that the LH represents distinct reward variables for “self” and “other” and is causally involved in shaping socially motivated behavior. During a Pavlovian conditioning procedure incorporating ubiquitous social experiences where rewards to others affect one's motivation, LH cells encoded the subjective value of self-rewards, as well as the likelihood of self- or other-rewards. The other-reward coding was not a general consequence of other's existence, but a specific effect of other's reward availability. Coherent activity with and top-down information flow from the medial prefrontal cortex, a hub of social brain networks, contributed to signal encoding in the LH. Furthermore, deactivation of LH cells eliminated the motivational impact of other-rewards. These results indicate that the LH constitutes a subcortical node in social brain networks and shapes one's motivation by integrating cortically derived, agent-specific reward information. |
Monica N. O'Connell; Annamaria Barczak; Tammy McGinnis; Kieran Mackin; Todd Mowery; Charles E. Schroeder; Peter Lakatos The role of motor and environmental visual rhythms in structuring auditory cortical excitability Journal Article In: iScience, vol. 23, no. 8, pp. 101374, 2020. @article{OConnell2020,Previous studies indicate that motor sampling patterns modulate neuronal excit- ability in sensory brain regions by entraining brain rhythms, a process termed mo- tor-initiated entrainment. In addition, rhythms of the external environment are also capable of entraining brain rhythms. Our first goal was to investigate the properties ofmotor-initiatedentrainment in theauditory systemusingaprominent visualmotor sampling pattern in primates, saccades. Second, we wanted to determine whether/ how motor-initiated entrainment interacts with visual environmental entrainment. Weexamined laminar profiles of neuronal ensemble activity in primary auditory cor- tex and found that whereasmotor-initiated entrainment has a suppressive effect, vi- sual environmental entrainment has an enhancive effect. We also found that these processes are temporally coupled, and their temporal relationship ensures that their effect on excitability is complementary rather than interfering. Altogether, our re- sults demonstrate that motor and sensory systems continuously interact in orches- tratingthebrain's context for theoptimal samplingofourmultisensoryenvironment. INTRODUCTION |
Wei Song Ong; Seth Madlon-Kay; Michael L. Platt Neuronal correlates of strategic cooperation in monkeys Journal Article In: Nature Neuroscience, vol. 24, pp. 116–128, 2020. @article{Ong2020,We recorded neural activity in male monkeys playing a variant of the game ‘chicken' in which they made decisions to cooperate or not cooperate to obtain rewards of different sizes. Neurons in the middle superior temporal sulcus (mSTS)—previously implicated in social perception—signaled strategic information, including payoffs, intentions of the other player, reward outcomes and predictions about the other player. Moreover, a subpopulation of mSTS neurons selectively signaled cooperatively obtained rewards. Neurons in the anterior cingulate gyrus, previously implicated in vicarious reinforcement and empathy, carried less information about strategic variables, especially cooperative reward. Strategic signals were not reducible to perceptual information about the other player or motor contingencies. These findings suggest that the capacity to compute models of other agents has deep roots in the strategic social behavior of primates and that the anterior cingulate gyrus and the mSTS support these computations. |
Sorin A. Pojoga; Natasha Kharas; Valentin Dragoi Perceptually unidentifiable stimuli influence cortical processing and behavioral performance Journal Article In: Nature Communications, vol. 11, pp. 6109, 2020. @article{Pojoga2020,Our daily behavior is dynamically influenced by conscious and unconscious processes. Although the neural bases of conscious experience have been extensively investigated over the past several decades, how unconscious information impacts neural circuitry and behavior remains unknown. Here, we recorded populations of neurons in macaque primary visual cortex (V1) to find that perceptually unidentifiable stimuli repeatedly presented in the absence of awareness are encoded by neural populations in a way that facilitates their future processing in the context of a behavioral task. Such exposure increases stimulus sensitivity and information encoded in cell populations, even though animals are unaware of stimulus identity. This phenomenon is consistent with a Hebbian mechanism underlying an increase in functional connectivity specifically for the neurons activated by subthreshold stimuli. This form of unsupervised adaptation may constitute a vestigial pre-attention system using the mere frequency of stimulus occurrence to change stimulus representations even when sensory inputs are perceptually invisible. |
Joern K. Pomper; Silvia Spadacenta; Friedemann Bunjes; Daniel Arnstein; Martin A. Giese; Peter Thier Representation of the observer's predicted outcome value in mirror and nonmirror neurons of macaque F5 ventral premotor cortex Journal Article In: Journal of Neurophysiology, vol. 124, no. 3, pp. 941–961, 2020. @article{Pomper2020,In the search for the function of mirror neurons, a previous study reported that F5 mirror neuron responses are modulated by the value that the observing monkey associates with the grasped object. Yet we do not know whether mirror neurons are modulated by the expected reward value for the observer or also by other variables, which are causally dependent on value (e.g., motivation, attention directed at the observed action, arousal). To clarify this, we trained two rhesus macaques to observe a grasping action on an object kept constant, followed by four fully predictable outcomes of different values (2 outcomes with positive and 2 with negative emotional valence). We found a consistent order in population activity of both mirror and nonmirror neurons that matches the order of the value of this predicted outcome but that does not match the order of the above-mentioned value-dependent variables. These variables were inferred from the probability not to abort a trial, saccade latency, modulation of eye position during action observation, heart rate, and pupil size. Moreover, we found subpopulations of neurons tuned to each of the four predicted outcome values. Multidimensional scaling revealed equal normalized distances of 0.25 between the two positive and between the two negative outcomes suggesting the representation of a relative value, scaled to the task setting. We conclude that F5 mirror neurons and nonmirror neurons represent the observer's predicted outcome value, which in the case of mirror neurons may be transferred to the observed object or action. NEW & NOTEWORTHY Both the populations of F5 mirror neurons and nonmirror neurons represent the predicted value of an outcome resulting from the observation of a grasping action. Value-dependent motivation, arousal, and attention directed at the observed action do not provide a better explanation for this representation. The population activity's metric suggests an optimal scaling of value representation to task setting. |
Pierre Pouget; Stephen Frey; Harry Ahnine; David Attali; Julien Claron; Charlotte Constans; Jean Francois Aubry; Fabrice Arcizet In: Frontiers in Physiology, vol. 11, pp. 1042, 2020. @article{Pouget2020,Since the late 2010s, Transcranial Ultrasound Stimulation (TUS) has been used experimentally to carryout safe, non-invasive stimulation of the brain with better spatial resolution than Transcranial Magnetic Stimulation (TMS). This innovative stimulation method has emerged as a novel and valuable device for studying brain function in humans and animals. In particular, single pulses of TUS directed to oculomotor regions have been shown to modulate visuomotor behavior of non-human primates during 100 ms ultrasound pulses. In the present study, a sustained effect was induced by applying 20-s trains of neuronavigated repetitive Transcranial Ultrasound Stimulation (rTUS) to oculomotor regions of the frontal cortex in three non-human primates performing an antisaccade task. With the help of MRI imaging and a frame-less stereotactic neuronavigation system (SNS), we were able to demonstrate that neuronavigated TUS (outside of the MRI scanner) is an efficient tool to carry out neuromodulation procedures in non-human primates. We found that, following neuronavigated rTUS, saccades were significantly modified, resulting in shorter latencies compared to no-rTUS trials. This behavioral modulation was maintained for up to 20 min. Oculomotor behavior returned to baseline after 18–31 min and could not be significantly distinguished from the no-rTUS condition. This study is the first to show that neuronavigated rTUS can have a persistent effect on monkey behavior with a quantified return-time to baseline. The specificity of the effects could not be explained by auditory confounds. |
R. Becket Ebitz; Jiaxin Cindy Tu; Benjamin Y. Hayden Rules warp feature encoding in decision-making circuits Journal Article In: PLOS Biology, vol. 18, no. 11, pp. 1–38, 2020. @article{Ebitz2020,We have the capacity to follow arbitrary stimulus–response rules, meaning simple policies that guide our behavior. Rule identity is broadly encoded across decision-making circuits, but there are less data on how rules shape the computations that lead to choices. One idea is that rules could simplify these computations. When we follow a rule, there is no need to encode or compute information that is irrelevant to the current rule, which could reduce the metabolic or energetic demands of decision-making. However, it is not clear if the brain can actually take advantage of this computational simplicity. To test this idea, we recorded from neurons in 3 regions linked to decision-making, the orbitofrontal cortex (OFC), ventral striatum (VS), and dorsal striatum (DS), while macaques performed a rule-based decision-making task. Rule-based decisions were identified via modeling rules as the latent causes of decisions. This left us with a set of physically identical choices that maximized reward and information, but could not be explained by simple stimulus–response rules. Contrasting rule-based choices with these residual choices revealed that following rules (1) decreased the energetic cost of decision-making; and (2) expanded rule-relevant coding dimensions and compressed rule-irrelevant ones. Together, these results suggest that we use rules, in part, because they reduce the costs of decision-making through a distributed representational warping in decision-making circuits. |
Steven P. Errington; Geoffrey F. Woodman; Jeffrey D. Schall Dissociation of medial frontal $beta$-bursts and executive control Journal Article In: Journal of Neuroscience, vol. 40, no. 48, pp. 9272–9282, 2020. @article{Errington2020,The neural mechanisms of executive and motor control concern both basic researchers and clinicians. In human studies, preparation and cancellation of movements are accompanied by changes in the $beta$-frequency band (15-29 Hz) of electroencephalogram (EEG). Previous studies with human participants performing stop signal (countermanding) tasks have described reduced frequency of transient $beta$-bursts over sensorimotor cortical areas before movement initiation and increased $beta$-bursting over medial frontal areas with movement cancellation. This modulation has been interpreted as contributing to the trial-by-trial control of behavior. We performed identical analyses of EEG recorded over the frontal lobe of macaque monkeys (one male, one female) performing a saccade countermanding task. While we replicate the occurrence and modulation of $beta$-bursts associated with initiation and cancellation of saccades, we found that $beta$-bursts occur too infrequently to account for the observed stopping behavior. We also found $beta$-bursts were more common after errors, but their incidence was unrelated to response time (RT) adaptation. These results demonstrate the homology of this EEG signature between humans and macaques but raise questions about the current interpretation of $beta$ band functional significance. |
Armin Najarpour Foroushani; Sujaya Neupane; Pablo De Heredia Pastor; Christopher C. Pack; Mohamad Sawan Spatial resolution of local field potential signals in macaque V4 Journal Article In: Journal of Neural Engineering, vol. 17, no. 2, pp. 1–23, 2020. @article{Foroushani2020,Objective. An important challenge for the development of cortical visual prostheses is to generate spatially localized percepts of light, using artificial stimulation. Such percepts are called phosphenes, and the goal of prosthetic applications is to generate a pattern of phosphenes that matches the structure of the retinal image. A preliminary step in this process is to understand how the spatial positions of phosphene-like visual stimuli are encoded in the distributed activity of cortical neurons. The spatial resolution with which the distributed responses discriminate positions puts a limit on the capability of visual prosthesis devices to induce phosphenes at multiple positions. While most previous prosthetic devices have targeted the primary visual cortex, the extrastriate cortex has the advantage of covering a large part of the visual field with a smaller amount of cortical tissue, providing the possibility of a more compact implant. Here, we studied how well ensembles of Local Field Potentials (LFPs) and Multiunit activity (MUA) responses from extrastriate cortical visual area V4 of a behaving macaque monkey can discriminate between two-dimensional spatial positions. Approach. We used support vector machines (SVM) to determine the capabilities of LFPs and MUA to discriminate responses to phosphene-like stimuli (probes) at different spatial separations. We proposed a selection strategy based on the combined responses of multiple electrodes and used the linear learning weights to find the minimum number of electrodes for fine and coarse discriminations. We also measured the contribution of correlated trial-to-trial variability in the responses to the discrimination performance for MUA and LFP. Main results. We found that despite the large receptive field sizes in V4, the combined responses from multiple sites, whether MUA or LFP, are capable of fine and coarse discrimination of positions. Our electrode selection procedure significantly increased discrimination performance while reducing the required number of electrodes. Analysis of noise correlations in MUA and LFP responses showed that noise correlations in LFPs carry more information about spatial positions. Significance. This study determined the coding strategy for fine discrimination, suggesting that spatial positions could be well localized with patterned stimulation in extrastriate area V4. It also provides a novel approach to build a compact prosthesis with relatively few electrodes, which has the potential advantage of reducing tissue damage in real applications. |
Mathilda Froesel; Quentin Goudard; Marc Hauser; Maëva Gacoin; Suliann Ben Hamed Automated video-based heart rate tracking for the anesthetized and behaving monkey Journal Article In: Scientific Reports, vol. 10, pp. 17940, 2020. @article{Froesel2020,Heart rate (HR) is extremely valuable in the study of complex behaviours and their physiological correlates in non-human primates. However, collecting this information is often challenging, involving either invasive implants or tedious behavioural training. In the present study, we implement a Eulerian video magnification (EVM) heart tracking method in the macaque monkey combined with wavelet transform. This is based on a measure of image to image fluctuations in skin reflectance due to changes in blood influx. We show a strong temporal coherence and amplitude match between EVM-based heart tracking and ground truth ECG, from both color (RGB) and infrared (IR) videos, in anesthetized macaques, to a level comparable to what can be achieved in humans. We further show that this method allows to identify consistent HR changes following the presentation of conspecific emotional voices or faces. EVM is used to extract HR in humans but has never been applied to non-human primates. Video photoplethysmography allows to extract awake macaques HR from RGB videos. In contrast, our method allows to extract awake macaques HR from both RGB and IR videos and is particularly resilient to the head motion that can be observed in awake behaving monkeys. Overall, we believe that this method can be generalized as a tool to track HR of the awake behaving monkey, for ethological, behavioural, neuroscience or welfare purposes. |
Roberto A. Gulli; Lyndon R. Duong; Benjamin W. Corrigan; Guillaume Doucet; Sylvain Williams; Stefano Fusi; Julio C. Martinez-Trujillo Context-dependent representations of objects and space in the primate hippocampus during virtual navigation Journal Article In: Nature Neuroscience, vol. 23, no. 1, pp. 103–112, 2020. @article{Gulli2020,The hippocampus is implicated in associative memory and spatial navigation. To investigate how these functions are mixed in the hippocampus, we recorded from single hippocampal neurons in macaque monkeys navigating a virtual maze during a foraging task and a context–object associative memory task. During both tasks, single neurons encoded information about spatial position; a linear classifier also decoded position. However, the population code for space did not generalize across tasks, particularly where stimuli relevant to the associative memory task appeared. Single-neuron and population-level analyses revealed that cross-task changes were due to selectivity for nonspatial features of the associative memory task when they were visually available (perceptual coding) and following their disappearance (mnemonic coding). Our results show that neurons in the primate hippocampus nonlinearly mix information about space and nonspatial elements of the environment in a task-dependent manner; this efficient code flexibly represents unique perceptual experiences and correspondent memories. |
Ziad M. Hafed; Laurent Goffart Gaze direction as equilibrium: More evidence from spatial and temporal aspects of small-saccade triggering in the rhesus macaque monkey Journal Article In: Journal of Neurophysiology, vol. 123, no. 1, pp. 308–322, 2020. @article{Hafed2020,Rigorous behavioral studies made in human subjects have shown that small-eccentricity target displacements are associated with increased saccadic reaction times, but the reasons for this remain unclear. Before characterizing the neurophysiological foundations underlying this relationship between the spatial and temporal aspects of saccades, we tested the triggering of small saccades in the male rhesus macaque monkey. We also compared our results to those obtained in human subjects, both from the existing literature and through our own additional measurements. Using a variety of behavioral tasks exercising visual and nonvisual guidance of small saccades, we found that small saccades consistently require more time than larger saccades to be triggered in the nonhuman primate, even in the absence of any visual guidance and when valid advance information about the saccade landing position is available. We also found a strong asymmetry in the reaction times of small upper versus lower visual field visually guided saccades, a phenomenon that has not been described before for small saccades, even in humans. Following the suggestion that an eye movement is not initiated as long as the visuo-oculomotor system is within a state of balance, in which opposing commands counterbalance each other, we propose that the longer reaction times are a signature of enhanced times needed to create the symmetry-breaking condition that puts downstream premotor neurons into a push-pull regime necessary for rotating the eyeballs. Our results provide an important catalog of nonhuman primate oculomotor capabilities on the miniature scale, allowing concrete predictions on underlying neurophysiological mechanisms. NEW & NOTEWORTHY Leveraging a multitude of neurophysiological investigations in the rhesus macaque monkey, we generated and tested hypotheses about small-saccade latencies in this animal model. We found that small saccades always take longer, on average, than larger saccades to trigger, regardless of visual and cognitive context. Moreover, small downward saccades have the longest latencies overall. Our results provide an important documentation of oculomotor capabilities of an indispensable animal model for neuroscientific research in vision, cognition, and action. |
Eric Hart; Alexander C. Huk Recurrent circuit dynamics underlie persistent activity in the macaque frontoparietal network Journal Article In: eLife, vol. 9, pp. 1–22, 2020. @article{Hart2020,During delayed oculomotor response tasks, neurons in the lateral intraparietal area (LIP) and the frontal eye fields (FEF) exhibit persistent activity that reflects the active maintenance of behaviorally relevant information. Despite many computational models of the mechanisms of persistent activity, there is a lack of circuit-level data from the primate to inform the theories. To fill this gap, we simultaneously recorded ensembles of neurons in both LIP and FEF while macaques performed a memory-guided saccade task. A population encoding model revealed strong and symmetric long-timescale recurrent excitation between LIP and FEF. Unexpectedly, LIP exhibited stronger local functional connectivity than FEF, and many neurons in LIP had longer network and intrinsic timescales. The differences in connectivity could be explained by the strength of recurrent dynamics in attractor networks. These findings reveal reciprocal multi-area circuit dynamics in the frontoparietal network during persistent activity and lay the groundwork for quantitative comparisons to theoretical models. |
Christopher A. Henry; Adam Kohn Spatial contextual effects in primary visual cortex limit feature representation under crowding Journal Article In: Nature Communications, vol. 11, pp. 1687, 2020. @article{Henry2020,Crowding is a profound loss of discriminability of visual features, when a target stimulus is surrounded by distractors. Numerous studies of human perception have characterized how crowding depends on the properties of a visual display. Yet, there is limited understanding of how and where stimulus information is lost in the visual system under crowding. Here, we show that macaque monkeys exhibit perceptual crowding for target orientation that is similar to humans. We then record from neuronal populations in monkey primary visual cortex (V1). These populations show an appreciable loss of information about target orientation in the presence of distractors, due both to divisive and additive modulation of responses to targets by distractors. Our results show that spatial contextual effects in V1 limit the discriminability of visual features and can contribute substantively to crowding. |
James P. Herman; Fabrice Arcizet; Richard J. Krauzlis Attention-related modulation of caudate neurons depends on superior colliculus activity Journal Article In: eLife, vol. 9, pp. 1–26, 2020. @article{Herman2020,Recent work has implicated the primate basal ganglia in visual perception and attention, in addition to their traditional role in motor control. The basal ganglia, especially the caudate nucleus “head” (CDh) of the striatum, receive indirect anatomical connections from the superior colliculus, a midbrain structure that is known to play a crucial role in the control of visual attention. To test the possible functional relationship between these subcortical structures, we recorded CDh neuronal activity of macaque monkeys before and during unilateral superior colliculus (SC) inactivation in a spatial attention task. SC inactivation significantly altered the attention-related modulation of CDh neurons and strongly impaired the classification of task epochs based on CDh activity. Only inactivation of SC on the same side of the brain as recorded CDh neurons, not the opposite side, had these effects. These results demonstrate a novel interaction between SC activity and attention-related visual processing in the basal ganglia. |
Ahmad Jezzini; Camillo Padoa-Schioppa Neuronal activity in the primate amygdala during economic choice Journal Article In: Journal of Neuroscience, vol. 40, no. 6, pp. 1286–1301, 2020. @article{Jezzini2020,Multiple lines of evidence link economic choices to the orbitofrontal cortex (OFC), but other brain regions may contribute to the computation and comparison of economic values. A particularly strong candidate is the basolateral amygdala (BLA). Amygdala lesions impair performance in reinforcer devaluation tasks, suggesting that the BLA contributes to value computation. Furthermore, previous studies of the BLA have found neuronal activity consistent with a value representation. Here, we recorded from the BLA of two male rhesus macaques choosing between different juices. Offered quantities varied from trial to trial, and relative values were inferred from choices. Approximately one-third of BLA cells were task-related. Our analyses revealed the presence of three groups of neurons encoding variables offer value, chosen value, and chosen juice. In this respect, the BLA appeared similar to the OFC. The two areas differed for the proportion of neurons in each group, as the fraction of chosen value cells was significantly higher in the BLA. Importantly, the activity of these neurons reflected the subjective nature of value. Firing rates in the BLA were sustained throughout the trial and maximal after juice delivery. In contrast, firing rates in the OFC were phasic and maximal shortly after offer presentation. Our results suggest that the BLA supports economic choice and reward expectation. |
Sanjeev B Khanna; Jonathan A Scott; Matthew A Smith Dynamic shifts of visual and saccadic signals in prefrontal cortical regions 8Ar and FEF Journal Article In: Journal of Neurophysiology, vol. 124, no. 6, pp. 1774–1791, 2020. @article{Khanna2020,Active vision is a fundamental process by which primates gather information about the external world. Multiple brain regions have been studied in the context of simple active vision tasks in which a visual target's appearance is temporally separated from saccade execution. Most neurons have tight spatial registration between visual and saccadic signals, and in areas such as prefrontal cortex (PFC), some neurons show persistent delay activity that links visual and motor epochs and has been proposed as a basis for spatial working memory. Many PFC neurons also show rich dynamics, which have been attributed to alternative working memory codes and the representation of other task variables. Our study investigated the transition between processing a visual stimulus and generating an eye movement in populations of PFC neurons in macaque monkeys performing a memory guided saccade task. We found that neurons in two subregions of PFC, the frontal eye fields (FEF) and area 8Ar, differed in their dynamics and spatial response profiles. These dynamics could be attributed largely to shifts in the spatial profile of visual and motor responses in individual neurons. This led to visual and motor codes for particular spatial locations that were instantiated by different mixtures of neurons, which could be important in PFC's flexible role in multiple sensory, cognitive, and motor tasks.NEW & NOTEWORTHY A central question in neuroscience is how the brain transitions from sensory representations to motor outputs. The prefrontal cortex contains neurons that have long been implicated as important in this transition and in working memory. We found evidence for rich and diverse tuning in these neurons, which was often spatially misaligned between visual and saccadic responses. This feature may play an important role in flexible working memory capabilities. |
Ricardo Kienitz; Michele A. Cox; Kacie Dougherty; Richard C. Saunders; Joscha T. Schmiedt; David A. Leopold; Alexander Maier; Michael C. Schmid Theta, but not gamma oscillations in area V4 depend on input from primary visual cortex Journal Article In: Current Biology, pp. 1–12, 2020. @article{Kienitz2020,Theta (3–9 Hz) and gamma (30–100 Hz) oscillations have been observed at different levels along the hierarchy of cortical areas and across a wide set of cognitive tasks. In the visual system, the emergence of both rhythms in primary visual cortex (V1) and mid-level cortical areas V4 has been linked with variations in perceptual reaction times.1–5 Based on analytical methods to infer causality in neural activation patterns, it was concluded that gamma and theta oscillations might both reflect feedforward sensory processing from V1 to V4.6–10 Here, we report on experiments in macaque monkeys in which we experimentally assessed the presence of both oscillations in the neural activity recorded from multi-electrode arrays in V1 and V4 before and after a permanent V1 lesion. With intact cortex, theta and gamma oscillations could be reliably elicited in V1 and V4 when monkeys viewed a visual contour illusion and showed phase-to-amplitude coupling. Laminar analysis in V1 revealed that both theta and gamma oscillations occurred primarily in the supragranular layers, the cortical output compartment of V1. However, there was a clear dissociation between the two rhythms in V4 that became apparent when the major feedforward input to V4 was removed by lesioning V1: although V1 lesioning eliminated V4 theta, it had little effect on V4 gamma power except for delaying its emergence by >100 ms. These findings suggest that theta is more tightly associated with feedforward processing than gamma and pose limits on the proposed role of gamma as a feedforward mechanism. |
Daniel L. Kimmel; Gamaleldin F. Elsayed; John P. Cunningham; William T. Newsome Value and choice as separable and stable representations in orbitofrontal cortex Journal Article In: Nature Communications, vol. 11, pp. 3466, 2020. @article{Kimmel2020,Value-based decision-making requires different variables—including offer value, choice, expected outcome, and recent history—at different times in the decision process. Orbitofrontal cortex (OFC) is implicated in value-based decision-making, but it is unclear how downstream circuits read out complex OFC responses into separate representations of the relevant variables to support distinct functions at specific times. We recorded from single OFC neurons while macaque monkeys made cost-benefit decisions. Using a novel analysis, we find separable neural dimensions that selectively represent the value, choice, and expected reward of the present and previous offers. The representations are generally stable during periods of behavioral relevance, then transition abruptly at key task events and between trials. Applying new statistical methods, we show that the sensitivity, specificity and stability of the representations are greater than expected from the population's low-level features—dimensionality and temporal smoothness—alone. The separability and stability suggest a mechanism—linear summation over static synaptic weights—by which downstream circuits can select for specific variables at specific times. |
Paul Henri Prévot; Kevin Gehere; Fabrice Arcizet; Himanshu Akolkar; Mina A. Khoei; Kévin Blaize; Omar Oubari; Pierre Daye; Marion Lanoë; Manon Valet; Sami Dalouz; Paul Langlois; Elric Esposito; Valérie Forster; Elisabeth Dubus; Nicolas Wattiez; Elena Brazhnikova; Céline Nouvel-Jaillard; Yannick LeMer; Joanna Demilly; Claire Maëlle Fovet; Philippe Hantraye; Morgane Weissenburger; Henri Lorach; Elodie Bouillet; Martin Deterre; Ralf Hornig; Guillaume Buc; José Alain Sahel; Guillaume Chenegros; Pierre Pouget; Ryad Benosman; Serge Picaud Behavioural responses to a photovoltaic subretinal prosthesis implanted in non-human primates Journal Article In: Nature Biomedical Engineering, vol. 4, no. 2, pp. 172–180, 2020. @article{Prevot2020,Retinal dystrophies and age-related macular degeneration related to photoreceptor degeneration can cause blindness. In blind patients, although the electrical activation of the residual retinal circuit can provide useful artificial visual perception, the resolutions of current retinal prostheses have been limited either by large electrodes or small numbers of pixels. Here we report the evaluation, in three awake non-human primates, of a previously reported near-infrared-light-sensitive photovoltaic subretinal prosthesis. We show that multipixel stimulation of the prosthesis within radiation safety limits enabled eye tracking in the animals, that they responded to stimulations directed at the implant with repeated saccades and that the implant-induced responses were present two years after device implantation. Our findings pave the way for the clinical evaluation of the prosthesis in patients affected by dry atrophic age-related macular degeneration. |
Sina Salehi; Mohammad Reza A. Dehaqani; Behrad Noudoost; Hossein Esteky Distinct mechanisms of face representation by enhancive and suppressive neurons of the inferior temporal cortex Journal Article In: Journal of Neurophysiology, vol. 124, no. 4, pp. 1216–1228, 2020. @article{Salehi2020,Face-selective neurons in the inferior temporal (IT) cortex respond to faces by either increasing (ENH) or decreasing (SUP) their spiking activities compared with their baseline. Although nearly half of IT face neurons are selectively suppressed by face stimulation, their role in face representation is not clear. To address this issue, we recorded the spiking activities and local field potential (LFP) from IT cortex of three monkeys while they viewed a large set of visual stimuli. LFP high-gamma (HG-LFP) power indicated the presence of both ENH and SUP face-selective neural clusters in IT cortex. The magnitude of HG-LFP power of the recording sites was correlated with the magnitude of change in the evoked spiking activities of its constituent neurons for both ENH and SUP face clusters. Spatial distribution of the ENH and SUP face clusters suggests the presence of a complex and heterogeneous face hypercluster organization in IT cortex. Importantly, ENH neurons conveyed more face category and SUP neurons conveyed more face identity information at both the single-unit and neuronal population levels. Onset and peak of suppressive single-unit, neuronal population, and HG-LFP power activities lagged those of the ENH ones. These results demonstrate that IT neuronal code for face representation is optimized by increasing sparseness through selective suppression of a subset of face neurons. We suggest that IT cortex contains spatial clusters of both ENH and SUP face neurons with distinct specialized functional role in face representation. NEW & NOTEWORTHY Electrophysiological and imaging studies have suggested that face information is encoded by a network of clusters of enhancive face-selective neurons in the visual cortex of man and monkey. We show that nearly half of face-selective neurons are suppressed by face stimulation. The suppressive neurons form spatial clusters and convey more face identity information than the enhancive face neurons. Our results suggest the presence of two neuronal subsystems for coarse and fine face information processing. |
David J. Schaeffer; Janahan Selvanayagam; Kevin D. Johnston; Ravi S. Menon; Winrich A. Freiwald; Stefan Everling Face selective patches in marmoset frontal cortex Journal Article In: Nature Communications, vol. 11, pp. 4856, 2020. @article{Schaeffer2020,In humans and macaque monkeys, socially relevant face processing is accomplished via a distributed functional network that includes specialized patches in frontal cortex. It is unclear whether a similar network exists in New World primates, who diverged $sim$35 million years from Old World primates. The common marmoset is a New World primate species ideally placed to address this question given their complex social repertoire. Here, we demonstrate the existence of a putative high-level face processing network in marmosets. Like Old World primates, marmosets show differential activation in anterior cingulate and lateral prefrontal cortices while they view socially relevant videos of marmoset faces. We corroborate the locations of these frontal regions by demonstrating functional and structural connectivity between these regions and temporal lobe face patches. Given the evolutionary separation between macaques and marmosets, our results suggest this frontal network specialized for social face processing predates the separation between Platyrrhini and Catarrhini. |
Philipp Schwedhelm; Daniel Baldauf; Stefan Treue The lateral prefrontal cortex of primates encodes stimulus colors and their behavioral relevance during a match-to-sample task Journal Article In: Scientific Reports, vol. 10, pp. 4216, 2020. @article{Schwedhelm2020,The lateral prefrontal cortex of primates (lPFC) plays a central role in complex cognitive behavior, in decision-making as well as in guiding top-down attention. However, how and where in lPFC such behaviorally relevant signals are computed is poorly understood. We analyzed neural recordings from chronic microelectrode arrays implanted in lPFC region 8Av/45 of two rhesus macaques. The animals performed a feature match-to-sample task requiring them to match both motion and color information in a test stimulus. This task allowed to separate the encoding of stimulus motion and color from their current behavioral relevance on a trial-by-trial basis. We found that upcoming motor behavior can be robustly predicted from lPFC activity. In addition, we show that 8Av/45 encodes the color of a visual stimulus, regardless of its behavioral relevance. Most notably, whether a color matches the searched-for color can be decoded independent of a trial's motor outcome and while subjects detect unique feature conjunctions of color and motion. Thus, macaque area 8Av/45 computes, among other task-relevant information, the behavioral relevance of visual color features. Such a signal is most critical for both the selection of responses as well as the deployment of top-down modulatory signals, like feature-based attention. |
H. N. Schwerdt; K. Amemori; D. J. Gibson; L. L. Stanwicks; T. Yoshida; N. P. Bichot; S. Amemori; R. Desimone; R. Langer; M. J. Cima; A. M. Graybiel Dopamine and beta-band oscillations differentially link to striatal value and motor control Journal Article In: Science Advances, vol. 6, no. 39, pp. eabb9226, 2020. @article{Schwerdt2020,Parkinson's disease is characterized by decreased dopamine and increased beta-band oscillatory activity accompanying debilitating motor and mood impairments. Coordinate dopamine-beta opposition is considered a normative rule for basal ganglia function. We report a breakdown of this rule. We developed multimodal systems allowing the first simultaneous, chronic recordings of dopamine release and beta-band activity in the striatum of nonhuman primates during behavioral performance. Dopamine and beta signals were anticorrelated over secondslong time frames, in agreement with the posited rule, but at finer time scales, we identified conditions in which these signals were modulated with the same polarity. These measurements demonstrated that task-elicited beta suppressions preceded dopamine peaks and that relative dopamine-beta timing and polarity depended on reward value, performance history, movement, and striatal domain. These findings establish a new view of coordinate dopamine and beta signaling operations, critical to guide novel strategies for diagnosing and treating Parkinson's disease and related neurodegenerative disorders. |
Caspar M. Schwiedrzik; Sandrin S. Sudmann Pupil diameter tracks statistical structure in the environment to increase visual sensitivity Journal Article In: Journal of Neuroscience, vol. 40, no. 23, pp. 4565–4575, 2020. @article{Schwiedrzik2020,Pupil diameter determines how much light hits the retina, and thus, how much information is available for visual processing. This is regulated by a brainstem reflex pathway. Here, we investigate whether this pathway is under control of internal models about the environment. This would allow adjusting pupil dynamics to environmental statistics to augment information transmission. We present image sequences containing internal temporal structure to humans of either sex and male macaque monkeys. We then measure whether the pupil tracks this temporal structure not only at the rate of luminance variations, but also at the rate of statistics not available from luminance information alone. We find entrainment to environmental statistics in both species. This entrainment directly affects visual processing by increasing sensitivity at the environmentally relevant temporal frequency. Thus, pupil dynamics are matched to the temporal structure of the environment to optimize perception, in line with an active sensing account. |
Katharine A. Shapcott; Joscha T. Schmiedt; Kleopatra Kouroupaki; Ricardo Kienitz; Andreea Lazar; Wolf Singer; Michael C. Schmid Reward-related suppression of neural activity in macaque visual area v4 Journal Article In: Cerebral Cortex, vol. 30, no. 9, pp. 4871–4881, 2020. @article{Shapcott2020,In order for organisms to survive, they need to detect rewarding stimuli, for example, food or a mate, in a complex environment with many competing stimuli. These rewarding stimuli should be detected even if they are nonsalient or irrelevant to the current goal. The value-driven theory of attentional selection proposes that this detection takes place through reward-associated stimuli automatically engaging attentional mechanisms. But how this is achieved in the brain is not very well understood. Here, we investigate the effect of differential reward on the multiunit activity in visual area V4 of monkeys performing a perceptual judgment task. Surprisingly, instead of finding reward-related increases in neural responses to the perceptual target, we observed a large suppression at the onset of the reward indicating cues. Therefore, while previous research showed that reward increases neural activity, here we report a decrease. More suppression was caused by cues associated with higher reward than with lower reward, although neither cue was informative about the perceptually correct choice. This finding of reward-associated neural suppression further highlights normalization as a general cortical mechanism and is consistent with predictions of the value-driven attention theory. |
Zhenhua Shi; Xiaomo Chen; Changming Zhao; He He; Veit Stuphorn; Dongrui Wu Multi-view broad learning system for primate oculomotor decision decoding Journal Article In: IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 28, no. 9, pp. 1908–1920, 2020. @article{Shi2020a,Multi-view learning improves the learning performance by utilizing multi-view data: data collected from multiple sources, or feature sets extracted from the same data source. This approach is suitable for primate brain state decoding using cortical neural signals. This is because the complementary components of simultaneously recorded neural signals, local field potentials (LFPs) and action potentials (spikes), can be treated as two views. In this paper, we extended broad learning system (BLS), a recently proposed wide neural network architecture, from single-view learning to multi-view learning, and validated its performance in decoding monkeys' oculomotor decision from medial frontal LFPs and spikes. We demonstrated that medial frontal LFPs and spikes in non-human primate do contain complementary information about the oculomotor decision, and that the proposed multi-view BLS is a more effective approach for decoding the oculomotor decision than several classical and state-of-the-art single-view and multi-view learning approaches. |
Ramona Siebert; Nick Taubert; Silvia Spadacenta; Peter W. Dicke; Martin A. Giese; Peter Thier A naturalistic dynamic monkey head avatar elicits species-typical reactions and overcomes the uncanny valley Journal Article In: eNeuro, vol. 7, no. 4, pp. 1–17, 2020. @article{Siebert2020,Research on social perception in monkeys may benefit from standardized, controllable, and ethologically valid renditions of conspecifics offered by monkey avatars. However, previous work has cautioned that monkeys, like humans, show an adverse reaction toward realistic synthetic stimuli, known as the “uncanny valley” effect. We developed an improved naturalistic rhesus monkey face avatar capable of producing facial expressions (fear grin, lip smack and threat), animated by motion capture data of real monkeys. For validation, we addition-ally created decreasingly naturalistic avatar variants. Eight rhesus macaques were tested on the various videos and avoided looking at less naturalistic avatar variants, but not at the most naturalistic or the most unnaturalis-tic avatar, indicating an uncanny valley effect for the less naturalistic avatar versions. The avoidance was deepened by motion and accompanied by physiological arousal. Only the most naturalistic avatar evoked facial expressions comparable to those toward the real monkey videos. Hence, our findings demonstrate that the uncanny valley reaction in monkeys can be overcome by a highly naturalistic avatar. |
Cheng Tang; Roger Herikstad; Aishwarya Parthasarathy; Camilo Libedinsky; Shih Cheng Yen Minimally dependent activity subspaces for working memory and motor preparation in the lateral prefrontal cortex Journal Article In: eLife, vol. 9, pp. 1–23, 2020. @article{Tang2020,The lateral prefrontal cortex is involved in the integration of multiple types of information, including working memory and motor preparation. However, it is not known how downstream regions can extract one type of information without interference from the others present in the network. Here, we show that the lateral prefrontal cortex of non-human primates contains two minimally dependent low-dimensional subspaces: one that encodes working memory information, and another that encodes motor preparation information. These subspaces capture all the information about the target in the delay periods, and the information in both subspaces is reduced in error trials. A single population of neurons with mixed selectivity forms both subspaces, but the information is kept largely independent from each other. A bump attractor model with divisive normalization replicates the properties of the neural data. These results provide new insights into neural processing in prefrontal regions. |
David A. Tovar; Jacob A. Westerberg; Michele A. Cox; Kacie Dougherty; Thomas A. Carlson; Mark T. Wallace; Alexander Maier Stimulus feature-specific information flow along the columnar cortical microcircuit revealed by multivariate laminar spiking analysis Journal Article In: Frontiers in Systems Neuroscience, vol. 14, pp. 600601, 2020. @article{Tovar2020,Most of the mammalian neocortex is comprised of a highly similar anatomical structure, consisting of a granular cell layer between superficial and deep layers. Even so, different cortical areas process different information. Taken together, this suggests that cortex features a canonical functional microcircuit that supports region-specific information processing. For example, the primate primary visual cortex (V1) combines the two eyes' signals, extracts stimulus orientation, and integrates contextual information such as visual stimulation history. These processes co-occur during the same laminar stimulation sequence that is triggered by the onset of visual stimuli. Yet, we still know little regarding the laminar processing differences that are specific to each of these types of stimulus information. Univariate analysis techniques have provided great insight by examining one electrode at a time or by studying average responses across multiple electrodes. Here we focus on multivariate statistics to examine response patterns across electrodes instead. Specifically, we applied multivariate pattern analysis (MVPA) to linear multielectrode array recordings of laminar spiking responses to decode information regarding the eye-of-origin, stimulus orientation, and stimulus repetition. MVPA differs from conventional univariate approaches in that it examines patterns of neural activity across simultaneously recorded electrode sites. We were curious whether this added dimensionality could reveal neural processes on the population level that are challenging to detect when measuring brain activity without the context of neighboring recording sites. We found that eye-of-origin information was decodable for the entire duration of stimulus presentation, but diminished in the deepest layers of V1. Conversely, orientation information was transient and equally pronounced along all layers. More importantly, using time-resolved MVPA, we were able to evaluate laminar response properties beyond those yielded by univariate analyses. Specifically, we performed a time generalization analysis by training a classifier at one point of the neural response and testing its performance throughout the remaining period of stimulation. Using this technique, we demonstrate repeating (reverberating) patterns of neural activity that have not previously been observed using standard univariate approaches. |
Pedro G. Vieira; Matthew R. Krause; Christopher C. Pack tACS entrains neural activity while somatosensory input is blocked Journal Article In: PLoS Biology, vol. 18, no. 10, pp. 1–14, 2020. @article{Vieira2020,Transcranial alternating current stimulation (tACS) modulates brain activity by passing electrical current through electrodes that are attached to the scalp. Because it is safe and noninvasive, tACS holds great promise as a tool for basic research and clinical treatment. However, little is known about how tACS ultimately influences neural activity. One hypothesis is that tACS affects neural responses directly, by producing electrical fields that interact with the brain's endogenous electrical activity. By controlling the shape and location of these electric fields, one could target brain regions associated with particular behaviors or symptoms. However, an alternative hypothesis is that tACS affects neural activity indirectly, via peripheral sensory afferents. In particular, it has often been hypothesized that tACS acts on sensory fibers in the skin, which in turn provide rhythmic input to central neurons. In this case, there would be little possibility of targeted brain stimulation, as the regions modulated by tACS would depend entirely on the somatosensory pathways originating in the skin around the stimulating electrodes. Here, we directly test these competing hypotheses by recording single-unit activity in the hippocampus and visual cortex of alert monkeys receiving tACS. We find that tACS entrains neuronal activity in both regions, so that cells fire synchronously with the stimulation. Blocking somatosensory input with a topical anesthetic does not significantly alter these neural entrainment effects. These data are therefore consistent with the direct stimulation hypothesis and suggest that peripheral somatosensory stimulation is not required for tACS to entrain neurons. |
Benjamin Voloh; Mariann Oemisch; Thilo Womelsdorf Phase of firing coding of learning variables across the fronto-striatal network during feature-based learning Journal Article In: Nature Communications, vol. 11, pp. 4669, 2020. @article{Voloh2020,The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that populations of neurons encoding choice outcomes, outcome prediction errors, and outcome history in their firing rates also carry significant information in their phase-of-firing at a 10–25 Hz band-limited beta frequency at which they synchronize across lateral prefrontal cortex, anterior cingulate cortex and anterior striatum when outcomes were processed. The phase-of-firing code exceeds information that can be obtained from firing rates alone and is evident for inter-areal connections between anterior cingulate cortex, lateral prefrontal cortex and anterior striatum. For the majority of connections, the phase-of-firing information gain is maximal at phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document enhanced information of three important learning variables at specific phases of firing in the beta cycle at an inter-areally shared beta oscillation frequency during goal-directed behavior. |
2019 |
Maria C. Romero; Marco Davare; Marcelo Armendariz; Peter Janssen Neural effects of transcranial magnetic stimulation at the single-cell level Journal Article In: Nature Communications, vol. 10, pp. 2642, 2019. @article{Romero2019,Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS. |
Ariana R. Andrei; Sorin A. Pojoga; Roger Janz; Valentin Dragoi Integration of cortical population signals for visual perception Journal Article In: Nature Communications, vol. 10, pp. 3832, 2019. @article{Andrei2019,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. |
Seth W. Egger; Evan D. Remington; Chia-Jung Chang; Mehrdad Jazayeri Internal models of sensorimotor integration regulate cortical dynamics Journal Article In: Nature Neuroscience, vol. 22, pp. 1871–1882, 2019. @article{Egger2019,Sensorimotor control during overt movements is characterized in terms of three building blocks: a controller, a simulator and a state estimator. We asked whether the same framework could explain the control of internal states in the absence of movements. Recently, it was shown that the brain controls the timing of future movements by adjusting an internal speed command. We trained monkeys in a novel task in which the speed command had to be dynamically controlled based on the timing of a sequence of flashes. Recordings from the frontal cortex provided evidence that the brain updates the internal speed command after each flash based on the error between the timing of the flash and the anticipated timing of the flash derived from a simulated motor plan. These findings suggest that cognitive control of internal states may be understood in terms of the same computational principles as motor control. Control of movements can be understood in terms of the interplay between a controller, a simulator and an estimator. Egger et. al. show that cortical neurons establish the same building blocks to control cognitive states in the absence of movement. |
Kun Guo; Zhihan Li; Yin Yan; Wu Li Viewing heterospecific facial expressions: an eye-tracking study of human and monkey viewers Journal Article In: Experimental Brain Research, vol. 237, no. 8, pp. 2045–2059, 2019. @article{Guo2019,Common facial expressions of emotion have distinctive patterns of facial muscle movements that are culturally similar among humans, and perceiving these expressions is associated with stereotypical gaze allocation at local facial regions that are characteristic for each expression, such as eyes in angry faces. It is, however, unclear to what extent this ‘universality' view can be extended to process heterospecific facial expressions, and how ‘social learning' process contributes to heterospecific expression perception. In this eye-tracking study, we examined face-viewing gaze allocation of human (including dog owners and non-dog owners) and monkey observers while exploring expressive human, chimpanzee, monkey and dog faces (positive, neutral and negative expressions in human and dog faces; neutral and negative expressions in chimpanzee and monkey faces). Human observers showed species- and experience-dependent expression categorization accuracy. Furthermore, both human and monkey observers demonstrated different face-viewing gaze distributions which were also species dependent. Specifically, humans predominately attended at human eyes but animal mouth when judging facial expressions. Monkeys' gaze distributions in exploring human and monkey faces were qualitatively different from exploring chimpanzee and dog faces. Interestingly, the gaze behaviour of both human and monkey observers were further affected by their prior experience of the viewed species. It seems that facial expression processing is species dependent, and social learning may play a significant role in discriminating even rudimentary types of heterospecific expressions. |
Ramina Adam; Kevin D. Johnston; Stefan Everling In: Journal of Neurophysiology, vol. 122, no. 2, pp. 672–690, 2019. @article{Adam2019,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. |
Florian Sandhaeger; Constantin Nicolai; Earl K. Miller; Markus Siegel Monkey EEG links neuronal color and motion information across species and scales Journal Article In: eLife, vol. 8, pp. 1–21, 2019. @article{Sandhaeger2019,It remains challenging to relate EEG and MEG to underlying circuit processes and comparable experiments on both spatial scales are rare. To close this gap between invasive and non-invasive electrophysiology we developed and recorded human-comparable EEG in macaque monkeys during visual stimulation with colored dynamic random dot patterns. Furthermore, we performed simultaneous microelectrode recordings from 6 areas of macaque cortex and human MEG. Motion direction and color information were accessible in all signals. Tuning of the non- invasive signals was similar to V4 and IT, but not to dorsal and frontal areas. Thus, MEG and EEG were dominated by early visual and ventral stream sources. Source level analysis revealed corresponding information and latency gradients across cortex. We show how information-based methods and monkey EEG can identify analogous properties of visual processing in signals spanning spatial scales from single units to MEG – a valuable framework for relating human and animal studies. |
Romain Quentin; Jean Rémi King; Etienne Sallard; Nathan Fishman; Ryan Thompson; Ethan R. Buch; Leonardo G. Cohen Differential brain mechanisms of selection and maintenance of information during working memory Journal Article In: Journal of Neuroscience, vol. 39, no. 19, pp. 3728–3740, 2019. @article{Quentin2019,Working memory is our ability to select and temporarily hold information as needed for complex cognitive operations. The temporal dynamics of sustained and transient neural activity supporting the selection and holding of memory content is not known. To address this problem, we recorded magnetoencephalography in healthy participants performing a retro-cue working memory task in which the selection rule and the memory content varied independently. Multivariate decoding and source analyses showed that selecting the memory content relies on prefrontal and parieto-occipital persistent oscillatory neural activity. By contrast, the memory content was reactivated in a distributed occipitotemporal posterior network, preceding the working memory decision and in a different format than during the visual encoding. These results identify a neural signature of content selection and characterize differentiated spatiotemporal constraints for subprocesses of working memory. |
Rishi Rajalingham; James J. DiCarlo Reversible inactivation of different millimeter-scale regions of primate IT results in rifferent patterns of core object recognition deficits Journal Article In: Neuron, vol. 102, no. 2, pp. 493–505.e5, 2019. @article{Rajalingham2019,Rajalingham and DiCarlo show that inactivating millimeter-scale IT subregions results in selective object recognition deficits, providing direct evidence for a causal role of IT in this behavior. Inactivating different subregions resulted in different deficit patterns, revealing an underlying topographical organization. |
Douglas A. Ruff; Marlene R. Cohen Simultaneous multi-area recordings suggest that attention improves performance by reshaping stimulus representations Journal Article In: Nature Neuroscience, vol. 22, pp. 1669–1676, 2019. @article{Ruff2019,Visual attention dramatically improves individuals' ability to see and modulates the responses of neurons in every known visual and oculomotor area, but whether such modulations can account for perceptual improvements is unclear. We measured the relationship between populations of visual neurons, oculomotor neurons and behavior during detection and discrimination tasks. We found that neither of the two prominent hypothesized neuronal mechanisms underlying attention (which concern changes in information coding and the way sensory information is read out) provide a satisfying account of the observed behavioral improvements. Instead, our results are more consistent with the hypothesis that attention reshapes the representation of attended stimuli to more effectively influence behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas. |
Amirsaman Sajad; David C. Godlove; Jeffrey D. Schall Cortical microcircuitry of performance monitoring Journal Article In: Nature Neuroscience, vol. 22, pp. 265–274, 2019. @article{Sajad2019,The medial frontal cortex enables performance monitoring, indexed by the error-related negativity (ERN) and manifested by performance adaptations. We recorded electroencephalogram over and neural spiking across all layers of the supplementary eye field, an agranular cortical area, in monkeys performing a saccade-countermanding (stop signal) task. Neurons signaling error production, feedback predicting reward gain or loss, and delivery of fluid reward had different spike widths and were concentrated differently across layers. Neurons signaling error or loss of reward were more common in layers 2 and 3 (L2/3), whereas neurons signaling gain of reward were more common in layers 5 and 6 (L5/6). Variation of error– and reinforcement-related spike rates in L2/3 but not L5/6 predicted response time adaptation. Variation in error-related spike rate in L2/3 but not L5/6 predicted ERN magnitude. These findings reveal novel features of cortical microcircuitry supporting performance monitoring and confirm one cortical source of the ERN. |
Jason M. Samonds; Veronica Choi; Nicholas J. Priebe Mice discriminate stereoscopic surfaces without fixating in depth Journal Article In: Journal of Neuroscience, vol. 39, no. 41, pp. 8024–8037, 2019. @article{Samonds2019,Stereopsis is aubiquitous feature ofprimatemammalianvision, but little is knownabout ifandhowrodentssuchasmiceuse stereoscopic vision. We used random dot stereograms to test for stereopsis in male and female mice, and they were able to discriminate near from far surfaces over a range of disparities, with diminishing performance for small and large binocular disparities. Based on two-photon measurements of disparity tuning, the range of disparities represented in the visual cortex aligns with the behavior and covers a broad range ofdisparities. Whenwe examined their binocular eye movements, we found that, unlike primates, mice did not systematically vary relative eye positions or use vergence eye movements when presented with different disparities. Nonetheless, the representation of disparity tuning was wide enough to capture stereoscopic information over a range of potential vergence angles. Although mice share fundamental characteristics of stereoscopic vision with primates and carnivores, their lack ofdisparity-dependent vergence eye move- ments and wide neuronal representation suggests that they may use a distinct strategy for stereopsis. |
Morteza Sarafyazd; Mehrdad Jazayeri Hierarchical reasoning by neural circuits in the frontal cortex Journal Article In: Science, vol. 364, pp. 1–11, 2019. @article{Sarafyazd2019,Humans process information hierarchically. In the presence of hierarchies, sources of failures are ambiguous. Humans resolve this ambiguity by assessing their confidence after one or more attempts. To understand the neural basis of this reasoning strategy, we recorded from dorsomedial frontal cortex (DMFC) and anterior cingulate cortex (ACC) of monkeys in a task in which negative outcomes were caused either by misjudging the stimulus or by a covert switch between two stimulus-response contingency rules. We found that both areas harbored a representation of evidence supporting a rule switch. Additional perturbation experiments revealed that ACC functioned downstream of DMFC and was directly and specifically involved in inferring covert rule switches. These results reveal the computational principles of hierarchical reasoning, as implemented by cortical circuits. |
Veronica E. Scerra; M. Gabriela Costello; Emilio Salinas; Terrence R. Stanford All-or-none context dependence delineates limits of FEF visual target selection Journal Article In: Current Biology, vol. 29, no. 2, pp. 294–305, 2019. @article{Scerra2019,Choices of where to look are informed by perceptual judgments, which locate objects of current value or interest within the visual scene. This perceptual-motor transform is partly implemented in the frontal eye field (FEF), where visually responsive neurons appear to select behaviorally relevant visual targets and, subsequently, saccade-related neurons select the movements required to look at them. Here, we use urgent decision-making tasks to show (1) that FEF motor activity can direct accurate, visually informed choices in the complete absence of prior target-distracter discrimination by FEF visual responses and (2) that such discrimination by FEF visual cells shows an all-or-none reliance on the presence of stimulus attributes strongly associated with saliency-driven attentional allocation. The present findings suggest that FEF visual target selection is specific to visual judgments made on the basis of saliency and may not play a significant role in guiding saccadic choices informed solely by feature content. |
Ehsan Sedaghat-Nejad; David J. Herzfeld; Paul Hage; Kaveh Karbasi; Tara Palin; Xiaoqin Wang; Reza Shadmehr Behavioral training of marmosets and electrophysiological recording from the cerebellum Book 2019. @book{SedaghatNejad2019,The common marmoset (Callithrix jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. However, the number of trials per session has been relatively small, thus limiting the utility of marmosets as a model for behavioral and neurophysiological studies. In this article, we report the results of a series of new behavioral training and neurophysiological protocols aimed at increasing the number of trials per session while recording from the cerebellum. To improve the training efficacy, we designed a precisely calibrated food regulation regime that motivates the subjects to perform saccade tasks, resulting in $sim$1,000 reward-driven trials on a daily basis. We then developed a multichannel recording system that uses imaging to target a desired region of the cerebellum, allowing for simultaneous isolation of multiple Purkinje cells in the vermis. In this report, we describe 1) the design and surgical implantation of a computer tomography (CT)guided, subject-specific head post, 2) the design of a CT- and MRI-guided alignment tool for trajectory guidance of electrodes mounted on an absolute encoder microdrive, 3) development of a protocol for behavioral training of subjects, and 4) simultaneous recordings from pairs of Purkinje cells during a saccade task. |
Janahan Selvanayagam; Kevin D. Johnston; David J. Schaeffer; Lauren K. Hayrynen; Stefan Everling Functional localization of the frontal eye fields in the common marmoset using microstimulation Journal Article In: Journal of Neuroscience, vol. 39, no. 46, pp. 9197–9206, 2019. @article{Selvanayagam2019,The frontal eye field (FEF) is a critical region for the deployment of overt and covert spatial attention. Although investigations in the macaque continue to provide insight into the neural underpinnings of the FEF, due to its location within a sulcus, the macaque FEF is virtually inaccessible to electrophysiological techniques such as high-density and laminar recordings. With a largely lissencephalic cortex, the common marmoset (Callithrix jacchus) is a promising alternative primate model for studying FEF microcircuitry. Putative homologies have been established with the macaque FEF on the basis of cytoarchitecture and connectivity; however, physiological investigation in awake, behaving marmosets is necessary to physiologically locate this area. Here, we addressed this gap using intracortical microstimulation in a broad range of frontal cortical areas in three adult marmosets (two males, one female). We implanted marmosets with 96-channel Utah arrays and applied microstimulation trains while they freely viewed video clips. We evoked short-latency fixed vector saccades at low currents (<50 $mu$A) in areas 45, 8aV, 8C, and 6DR. We observed a topography of saccade direction and amplitude consistent with findings in macaques and humans: small saccades in ventrolateral FEF and large saccades combined with contralateral neck and shoulder movements encoded in dorsomedial FEF. Our data provide compelling evidence supporting homology between marmoset and macaque FEF and suggest that the marmoset is a useful primate model for investigating FEF microcircuitry and its contributions to oculomotor and cognitive functions.SIGNIFICANCE STATEMENT The frontal eye field (FEF) is a critical cortical region for overt and covert spatial attention. The microcircuitry of this area remains poorly understood because in the macaque, the most commonly used model, it is embedded within a sulcus and is inaccessible to modern electrophysiological and imaging techniques. The common marmoset is a promising alternative primate model due to its lissencephalic cortex and potential for genetic manipulation. However, evidence for homologous cortical areas in this model remains limited and unclear. Here, we applied microstimulation in frontal cortical areas in marmosets to physiologically identify FEF. Our results provide compelling evidence for an FEF in the marmoset and suggest that the marmoset is a useful model for investigating FEF microcircuitry. |
Neda Shahidi; Ariana R. Andrei; Ming Hu; Valentin Dragoi High-order coordination of cortical spiking activity modulates perceptual accuracy Journal Article In: Nature Neuroscience, vol. 22, pp. 1148–1158, 2019. @article{Shahidi2019,The accurate relay of electrical signals within cortical networks is key to perception and cognitive function. Theoretically, it has long been proposed that temporal coordination of neuronal spiking activity controls signal transmission and behavior. However, whether and how temporally precise neuronal coordination in population activity influences perception are unknown. Here, we recorded populations of neurons in early and mid-level visual cortex (areas V1 and V4) simultaneously to discover that the precise temporal coordination between the spiking activity of three or more cells carries information about visual perception in the absence of firing rate modulation. The accuracy of perceptual responses correlated with high-order spiking coordination within V4, but not V1, and with feedforward coordination between V1 and V4. These results indicate that while visual stimuli are encoded in the discharge rates of neurons, perceptual accuracy is related to temporally precise spiking coordination within and between cortical networks. |
Hansem Sohn; Devika Narain; Nicolas Meirhaeghe; Mehrdad Jazayeri Bayesian computation through cortical latent dynamics Journal Article In: Neuron, vol. 103, no. 5, pp. 934–947.e5, 2019. @article{Sohn2019,Statistical regularities in the environment create prior beliefs that we rely on to optimize our behavior when sensory information is uncertain. Bayesian theory formalizes how prior beliefs can be leveraged and has had a major impact on models of perception, sensorimotor function, and cognition. However, it is not known how recurrent interactions among neurons mediate Bayesian integration. By using a time-interval reproduction task in monkeys, we found that prior statistics warp neural representations in the frontal cortex, allowing the mapping of sensory inputs to motor outputs to incorporate prior statistics in accordance with Bayesian inference. Analysis of recurrent neural network models performing the task revealed that this warping was enabled by a low-dimensional curved manifold and allowed us to further probe the potential causal underpinnings of this computational strategy. These results uncover a simple and general principle whereby prior beliefs exert their influence on behavior by sculpting cortical latent dynamics. Sohn et al. found that prior beliefs warp neural representations in the frontal cortex. This warping provides a substrate for the optimal integration of prior beliefs with sensory evidence during sensorimotor behavior. |
Sébastien Tremblay; Florian Pieper; Adam Sachs; Ridha Joober; Julio Martinez-Trujillo The effects of methylphenidate (Ritalin) on the neurophysiology of the monkey caudal prefrontal cortex Journal Article In: eNeuro, vol. 6, no. 1, pp. 1–17, 2019. @article{Tremblay2019,Methylphenidate (MPH), commonly known as Ritalin, is the most widely prescribed drug worldwide to treat patients with attention deficit disorders. Although MPH is thought to modulate catecholamine neurotransmission in the brain, it remains unclear how these neurochemical effects influence neuronal activity and lead to attentional enhancements. Studies in rodents overwhelmingly point to the lateral prefrontal cortex (LPFC) as a main site of action of MPH. To understand the mechanism of action of MPH in a primate brain, we recorded the responses of neuronal populations using chronic multielectrode arrays implanted in the caudal LPFC of two macaque monkeys while the animals performed an attention task (N 2811 neuronal recordings). Over different recording sessions (N 55), we orally administered either various doses of MPH or a placebo to the animals. Behavioral analyses revealed positive effects of MPH on task performance at specific doses. However, analyses of individual neurons activity, noise correlations, and neuronal ensemble activity using machine learning algorithms revealed no effects of MPH. Our results suggest that the positive behavioral effects of MPH observed in primates (including humans) may not be mediated by changes in the activity of caudal LPFC neurons. MPH may enhance cognitive performance by modulating neuronal activity in other regions of the attentional network in the primate brain. |
Kasper Vinken; Rufin Vogels A behavioral face preference deficit in a monkey with an incomplete face patch system Journal Article In: NeuroImage, vol. 189, pp. 415–424, 2019. @article{Vinken2019,Primates are experts in face perception and naturally show a preference for faces under free-viewing conditions. The primate ventral stream is characterized by a network of face patches that selectively responds to faces, but it remains uncertain how important such parcellation is for face perception. Here we investigated free-viewing behavior in a female monkey who naturally lacks fMRI-defined posterior and middle lateral face patches. We presented a series of content-rich images of scenes that included faces or other objects to that monkey during a free-viewing task and tested a group of 10 control monkeys on the same task for comparison. We found that, compared to controls, the monkey with missing face patches showed a marked reduction of face viewing preference that was most pronounced for the first few fixations. In addition, her gaze fixation patterns were substantially distinct from those of controls, especially for pictures with a face. These data demonstrate an association between the clustering of neurons in face selective patches and a behavioral bias for faces in natural images. |
Sébastien Ballesta; Camillo Padoa-Schioppa Economic decisions through circuit inhibition Journal Article In: Current Biology, vol. 29, no. 22, pp. 3814–3824, 2019. @article{Ballesta2019,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. |
Annamaria Barczak; Saskia Haegens; Deborah A. Ross; Tammy McGinnis; Peter Lakatos; Charles E. Schroeder Dynamic modulation of cortical excitability during visual active sensing Journal Article In: Cell Reports, vol. 27, no. 12, pp. 3447–3459, 2019. @article{Barczak2019,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. |
Marie E. Bellet; Joachim Bellet; Hendrikje Nienborg; Ziad M. Hafed; Philipp Berens Human-level saccade detection performance using deep neural networks Journal Article In: Journal of Neurophysiology, vol. 121, no. 2, pp. 646–661, 2019. @article{Bellet2019,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. |
Narcisse P. Bichot; Rui Xu; Azriel Ghadooshahy; Michael L. Williams; Robert Desimone The role of prefrontal cortex in the control of feature attention in area V4 Journal Article In: Nature Communications, vol. 10, pp. 5727, 2019. @article{Bichot2019,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. Hurley; Rick L. Jenison; Luis C. Populin Changes in endogenous dopamine induced by methylphenidate predict functional connectivity in nonhuman primates Journal Article In: Journal of Neuroscience, vol. 39, no. 8, pp. 1436–1444, 2019. @article{Birn2019,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. |
Amarender R. Bogadhi; Anil Bollimunta; David A. Leopold; Richard J. Krauzlis Spatial attention deficits are causally linked to an area in macaque temporal cortex Journal Article In: Current Biology, vol. 29, no. 5, pp. 726–736, 2019. @article{Bogadhi2019,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. |
Xinying Cai; Camillo Padoa-Schioppa Neuronal evidence for good-based economic decisions under variable action costs Journal Article In: Nature Communications, vol. 10, pp. 393, 2019. @article{Cai2019,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. |
Chih Yang Chen; Klaus Peter Hoffmann; Claudia Distler; Ziad M. Hafed The foveal visual representation of the primate superior colliculus Journal Article In: Current Biology, vol. 29, no. 13, pp. 2109–2119, 2019. @article{Chen2019h,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. |
Katherine E. Conen; X. Camillo Padoa-Schioppa Partial adaptation to the value range in the macaque orbitofrontal cortex Journal Article In: Journal of Neuroscience, vol. 39, no. 18, pp. 3498 –3513, 2019. @article{Conen2019,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. |
Michele A. Cox; Kacie Dougherty; Geoffrey K. Adams; Eric A. Reavis; Jacob A. Westerberg; Brandon S. Moore; David A. Leopold; Alexander Maier Spiking suppression precedes cued attentional enhancement of neural responses in primary visual cortex Journal Article In: Cerebral Cortex, vol. 29, no. 1, pp. 77–90, 2019. @article{Cox2019a,Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naive subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses. |
Michele A. Cox; Kacie Dougherty; Jacob A. Westerberg; Michelle S. Schall; Alexander Maier Temporal dynamics of binocular integration in primary visual cortex Journal Article In: Journal of Vision, vol. 19, no. 12, pp. 1–21, 2019. @article{Cox2019,Whenever we open our eyes, our brain quickly integrates the two eyes' perspectives into a combined view. This process of binocular integration happens so rapidly that even incompatible stimuli are briefly fused before one eye's view is suppressed in favor of the other (binocular rivalry). The neuronal basis for this brief period of fusion during incompatible binocular stimulation is unclear. Neuroanatomically, the eyes provide two largely separate streams of information that are integrated into a binocular response by the primary visual cortex (V1). However, the temporal dynamics underlying the formation of this binocular response are largely unknown. To address this question, we examined the temporal profile of binocular responses in V1 of fixating monkeys. We found that V1 processes binocular stimuli in a dynamic sequence that comprises at least two distinct temporal phases. An initial transient phase is characterized by enhanced spiking responses for both compatible and incompatible binocular stimuli compared to monocular stimulation. This transient is followed by a sustained response that differed markedly between congruent and incongruent binocular stimulation. Specifically, incompatible binocular stimulation resulted in overall response reduction relative to monocular stimulation (binocular suppression). In contrast, responses to compatible stimuli were either suppressed or enhanced (binocular facilitation) depending on the neurons' ocularity (selectivity for one eye over the other) and laminar location. These results suggest that binocular integration in V1 occurs in at least two sequential steps that comprise initial additive combination of the two eyes' signals followed by widespread differentiation between binocular concordance and discordance. |
Alexandre Dizeux; Marc Gesnik; Harry Ahnine; Kevin Blaize; Fabrice Arcizet; Serge Picaud; José Alain Sahel; Thomas Deffieux; Pierre Pouget; Mickael Tanter Functional ultrasound imaging of the brain reveals propagation of task-related brain activity in behaving primates Journal Article In: Nature Communications, vol. 10, pp. 1400, 2019. @article{Dizeux2019,Neuroimaging modalities such as MRI and EEG are able to record from the whole brain, but this comes at the price of either limited spatiotemporal resolution or limited sensitivity. Here, we show that functional ultrasound imaging (fUS) of the brain is able to assess local changes in cerebral blood volume during cognitive tasks, with sufficient temporal resolution to measure the directional propagation of signals. In two macaques, we observed an abrupt transient change in supplementary eye field (SEF) activity when animals were required to modify their behaviour associated with a change of saccade tasks. SEF activation could be observed in a single trial, without averaging. Simultaneous imaging of anterior cingulate cortex and SEF revealed a time delay in the directional functional connectivity of 0.27 ± 0.07 s and 0.9 ± 0.2 s for both animals. Cerebral hemodynamics of large brain areas can be measured at high spatiotemporal resolution using fUS. |
Kacie Dougherty; Michele A. Cox; Jacob A. Westerberg; Alexander Maier Binocular modulation of monocular V1 neurons Journal Article In: Current Biology, vol. 29, no. 3, pp. 381–391, 2019. @article{Dougherty2019,In humans and other primates, sensory signals from each eye remain separated until they arrive in the primary visual cortex (V1), but their exact meeting point is unknown. In V1, some neurons respond to stimulation of only one eye (monocular neurons), while most neurons respond to stimulation of either eye (binocular neurons). The main input layers of V1 contain most of the monocular neurons while binocular neurons dominate the layers above and below. This observation has given rise to the idea that the two eyes' signals remain separate until they converge outside V1's input layers. Here, we show that, despite responding to only one eye, monocular neurons in all layers, including the input layers, of V1 discriminate between stimulation of their driving eye alone and stimulation of both eyes. Some monocular V1 neurons' responses were significantly enhanced, or facilitated, when both eyes were stimulated. Binocular facilitation within V1's input layers tended to occur at the onset of the visual response, which could be explained by converging thalamocortical inputs. However, most V1 monocular neurons were significantly reduced, or suppressed, to binocular stimulation. In contrast to facilitation, binocular suppression occurred several milliseconds following the onset of the visual response, suggesting that the bulk of binocular modulation involves cortical inhibition. These findings, combined, suggest that binocular signals arise at an earlier processing stage than previously appreciated, as even so-called monocular neurons in V1's input layers encode what is shown to both eyes. |
Satwant Kumar; Ivo D. Popivanov; Rufin Vogels Transformation of visual representations across ventral stream body-selective patches Journal Article In: Cerebral Cortex, vol. 29, no. 1, pp. 215–229, 2019. @article{Kumar2019a,Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex. |
Satwant Kumar; Rufin Vogels Body patches in inferior temporal cortex encode categories with different temporal dynamics Journal Article In: Journal of Cognitive Neuroscience, vol. 31, no. 11, pp. 1699–1709, 2019. @article{Kumar2019,An unresolved question in cognitive neuroscience is how representations of object categories at different levels (basic and superordinate) develop during the course of the neural response within an area. To address this, we decoded categories of different levels from the spiking responses of populations of neurons recorded in two fMRI-defined body patches in the macaque STS. Recordings of the two patches were made in thesameanimals with thesamestimuli. Support vector machine classifiers were trained at brief response epochs and tested at the same or different epochs, thus assessing whether category representations change during the course of the response. In agreement with hierarchical processing within the body patch network, the posterior body patch mid STS body (MSB) showed an earlier onset of categorization compared with the anterior body patch anterior STS body (ASB), irrespective of the categorization level. Decoding of the superordinate body versus nonbody categories was less dynamic in MSB than in ASB, with ASB showing a biphasic temporal pattern. Decoding of the ordinate-level category human versus monkey bodies showed similar temporal patterns in both patches. The decoding onset of superordinate categorizations involving bodies was as early as for basic-level categorization, suggesting that previously reported differences between the onset of basic and superordinate categorizations may depend on the area. The qualitative difference between areas in their dynamics of category representation may hinder the interpretation of decoding dynamics based on EEG or MEG, methods that may mix signals of different areas. |
Noga Larry; Merav Yarkoni; Adi Lixenberg; Mati Joshua Cerebellar climbing fibers encode expected reward size Journal Article In: eLife, vol. 8, pp. 1–16, 2019. @article{Larry2019,Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activity increased when the monkeys were presented with a cue indicating a large reward size. Reward size did not modulate activity at reward delivery or during eye movements. Comparison between climbing fiber and simple spike activity indicated different interactions for coding of movement and reward. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction. |
Yin S. Li; Matthew R. Nassar; Joseph W. Kable; Joshua I. Gold Individual neurons in the cingulate cortex encode action monitoring, not selection, during adaptive decision-making Journal Article In: Journal of Neuroscience, vol. 39, no. 34, pp. 6668–6683, 2019. @article{Li2019g,The cingulate cortex contributes to complex, adaptive behaviors, but the exact nature of its contributions remains unresolved. Proposals from previous studies, including evaluating past actions or selecting future ones, have been difficult to distinguish in part because of an incomplete understanding of the task-relevant variables that are encoded by individual cingulate neurons. In this study, we recorded from individual neurons in parts ofboth the anterior cingulate cortex (ACC) and posterior cingulate cortex (PCC) in 2 male rhesus monkeys performing a saccadic reward task. The task required them to use adaptive, feedback-driven strategies to infer the spatial location ofa rewarded saccade target in the presence ofdifferent forms ofuncertainty. We found that task-relevant, spatially selective feedback signals were encoded by the activity of individual neurons in both brain regions, with stronger selectivity for spatial choice and reward-target signals in PCC and stronger selectivity for feedback in ACC. Moreover, neurons in both regions were sensitive to sequential effects of feedback that partly reflected sequential behavioral patterns. However, neither brain region exhibited systematic modulations by the blockwise conditions that governed the reliability of the trial-by-trial feedback and drove adaptive behavioral patterns. There was also little evidence that single-neuron responses in either brain region directly predicted the extent to which feedback and contextual information were used to inform choices on the subsequent trial. Thus, certain cingulate neurons encode diverse, evaluative signals needed for adaptive, feedback-driven decision-making, but those signals may be integrated elsewhere in the brain to guide actions. |
Zhihan Li; An Yan; Kun Guo; Wu Li Fear-related signals in the primary visual cortex Journal Article In: Current Biology, vol. 29, no. 23, pp. 4078–4083, 2019. @article{Li2019h,Neuronal responses in the primary visual cortex (V1) are driven by simple stimuli, but these stimulus- evoked responses can be markedly modulated by non-sensory factors, such as attention and reward [1], and shaped by perceptual training [2]. In real-life situations, neutral visual stimuli can become emotionally tagged by experience, resulting in altered perceptual abilities to detect and discriminate these stimuli [3–5]. Human imaging [4] and electroencephalography (EEG) studies [6–9] have shown that visual fear learning (the acquisition of aversive emotion associated with a visual stimulus) affects the activities in visual cortical areas as early as in V1. However, it remains elusive as to whether the fear-related activities seen in the early visual cortex have to do with feedback influences from other cortical areas; it is also unclear whether and how the response properties of V1 cells are modified during the fear learning. In the current study, we addressed these issues by recording from V1 of awake monkeys implanted with an array of microelectrodes. We found that responses of V1 neurons were rapidly modified when a given orientation of grating stimulus was repeatedly associated with an aversive stimulus. The output visual signals from V1 cells conveyed, from their response outset, fear-related signals that were specific to the fear-associated grating orientation and visual-field location. The specific fear signals were independent of neurons' orientation preferences and were present even though the fear-associated stimuli were rendered invisible. Our findings suggest a bottom-up mechanism that allows for proactive labeling of visual inputs that are predictive of imminent danger. |
Junxiang Luo; Keyan He; Ian Max Andolina; Xiaohong Li; Jiapeng Yin; Zheyuan Chen; Yong Gu; Wei Wang Going with the flow: The neural mechanisms underlying illusions of complex-flow motion Journal Article In: Journal of Neuroscience, vol. 39, no. 14, pp. 2664 –2685, 2019. @article{Luo2019,Studying the mismatch between perception and reality helps us better understand the constructive nature of the visual brain. The Pinna-Brelstaff motion illusion is a compelling example illustrating how a complex moving pattern can generate an illusory motion perception. When an observer moves toward (expansion) or away (contraction) from the Pinna-Brelstaff figure, the figure appears to rotate. The neural mechanisms underlying the illusory complex-flow motion of rotation, expansion, and contraction remain unknown. We studied this question at both perceptual and neuronal levels in behaving male macaques by using carefully parametrized Pinna-Brelstaff figures that induce the above motion illusions. We first demonstrate that macaques perceive illusory motion in a manner similar to that of human observers. Neurophysiological recordings were subsequently performed in the middle temporal area (MT) and the dorsal portion of the medial superior temporal area (MSTd). We find that subgroups of MSTd neurons encoding a particular global pattern of real complex-flow motion (rotation, expansion, contraction) also represent illusory motion patterns of the same class. They require an extra 15 ms to reliably discriminate the illusion. In contrast, MT neurons encode both real and illusory local motions with similar temporal delays. These findings reveal that illusory complex-flow motion is first represented in MSTd by the same neurons that normally encode real complex-flow motion. However, the extraction of global illusory motion in MSTd from other classes of real complex-flow motion requires extra processing time. Our study illustrates a cascaded integration mechanism from MT to MSTd underlying the transformation from external physical to internal nonveridical flow-motion perception. |
Liya Ma; Jason L. Chan; Kevin D. Johnston; Stephen G. Lomber; Stefan Everling Macaque anterior cingulate cortex deactivation impairs performance and alters lateral prefrontal oscillatory activities in a rule-switching task Journal Article In: PLoS Biology, vol. 17, no. 7, pp. e3000045, 2019. @article{Ma2019b,In primates, both the dorsal anterior cingulate cortex (dACC) and the dorsolateral prefrontal cortex (dlPFC) are key regions of the frontoparietal cognitive control network. To study the role of the dACC and its communication with the dlPFC in cognitive control, we recorded local field potentials (LFPs) from the dlPFC before and during the reversible deactivation of the dACC, in macaque monkeys engaging in uncued switches between 2 stimulus-response rules, namely prosaccade and antisaccade. Cryogenic dACC deactivation impaired response accuracy during maintenance of—but not the initial switching to—the cognitively demanding antisaccade rule, which coincided with a reduction in task-related theta activity and the correct-error (C-E) difference in dlPFC beta-band power. During both rule switching and maintenance, dACC deactivation prolonged the animals' reaction time and reduced task-related alpha power in the dlPFC. Our findings support a role of the dACC in prefrontal oscillatory activities that are involved the maintenance of a new, challenging task rule. |
Corentin Massot; Uday K Jagadisan; Neeraj J. Gandhi In: Communications Biology, vol. 2, pp. 1–14, 2019. @article{Massot2019,The superior colliculus (SC) is an excellent substrate to study sensorimotor transformations. To date, the spatial and temporal properties of population activity along its dorsoventral axis have been inferred from single electrode studies. Here, we recorded SC population activity in non-human primates using a linear multi-contact array during delayed saccade tasks. We show that during the visual epoch, information appeared first in dorsal layers and systematically later in ventral layers. During the delay period, the laminar organization of low-spiking rate activity matched that of the visual epoch. During the pre-saccadic epoch, spiking activity emerged first in a more ventral layer, $sim$ 100 ms before saccade onset. This buildup of activity appeared later on nearby neurons situated both dorsally and ventrally, culminating in a synchronous burst across the dorsoventral axis, $sim$ 28 ms before saccade onset. Collectively, these results reveal a principled spatiotemporal organization of SC population activity underlying sensorimotor transformation for the control of gaze. |
Vincent B. McGinty Overt attention toward appetitive cues enhances their subjective value, independent of orbitofrontal cortex activity Journal Article In: eNeuro, vol. 6, no. 6, pp. 1–19, 2019. @article{McGinty2019,Neural representations of value underlie many behaviors that are crucial for survival. Previously, we found that value representations in primate orbitofrontal cortex (OFC) are modulated by attention, specifically, by overt shifts of gaze toward or away from reward-associated visual cues (McGinty et al., 2016). Here, we investigate the influence of overt attention on behavior by asking how gaze shifts correlate with reward anticipatory responses and whether activity in OFC mediates this correlation. Macaque monkeys viewed pavlovian conditioned appetitive cues on a visual display, while the fraction of time they spent looking toward or away from the cues was measured using an eye tracker. Also measured during cue presentation were the reward anticipation, indicated by conditioned licking responses (CRs), and single-neuron activity in OFC. In general, gaze allocation predicted subsequent licking responses: the longer the monkeys spent looking at a cue at a given time point in a trial, the more likely they were to produce an anticipatory CR later in that trial, as if the subjective value of the cue were increased. To address neural mechanisms, mediation analysis measured the extent to which the gaze–CR correlation could be statistically explained by the concurrently recorded firing of OFC neurons. The resulting mediation effects were indistinguishable from chance. Therefore, while overt attention may increase the subjective value of reward-associated cues (as revealed by anticipatory behaviors), the underlying mechanism remains unknown, as does the functional significance of gaze-driven modulation of OFC value signals. |
Priyanka S. Mehta; Jiaxin Cindy Tu; Giuliana A. LoConte; Meghan C. Pesce; Benjamin Y. Hayden Ventromedial prefrontal cortex tracks multiple environmental variables during search Journal Article In: Journal of Neuroscience, vol. 39, no. 27, pp. 5336–5350, 2019. @article{Mehta2019,To make efficient foraging decisions, we must combine information about the values of available options with nonvalue information. Some accounts of ventromedial PFC (vmPFC) suggest that it has a narrow role limited to evaluating immediately available options. We examined responses of neurons in area 14 (a putative macaque homolog of human vmPFC) as 2 male macaques performed a novel foraging search task. Although many neurons encoded the values of immediately available offers, they also independently encoded several other variables that influence choice, but that are conceptually distinct from offer value. These variables include average reward rate, number of offers viewed per trial, previous offer values, previous outcome sizes, and the locations of the currently attended offer.We conclude that, rather than serving as specialized economic value center, vmPFC plays a broad role in integrating relevant environmental information to drive foraging decisions. |
Adam P. Morris; Bart Krekelberg A stable visual world in primate primary visual cortex Journal Article In: Current Biology, vol. 29, no. 9, pp. 1471–1480, 2019. @article{Morris2019,Humans and other primates rely on eye movements to explore visual scenes and to track moving objects. As a result, the image that is projected onto the retina—and propagated throughout the visual cortical hierarchy—is almost constantly changing and makes little sense without taking into account the momentary direction of gaze. How is this achieved in the visual system? Here, we show that in primary visual cortex (V1), the earliest stage of cortical vision, neural representations carry an embedded “eye tracker” that signals the direction of gaze associated with each image. Using chronically implanted multi-electrode arrays, we recorded the activity of neurons in area V1 of macaque monkeys during tasks requiring fast (exploratory) and slow (pursuit) eye movements. Neurons were stimulated with flickering, full-field luminance noise at all times. As in previous studies, we observed neurons that were sensitive to gaze direction during fixation, despite comparable stimulation of their receptive fields. We trained a decoder to translate neural activity into metric estimates of gaze direction. This decoded signal tracked the eye accurately not only during fixation but also during fast and slow eye movements. After a fast eye movement, the eye-position signal arrived in V1 at approximately the same time at which the new visual information arrived from the retina. Using simulations, we show that this V1 eye-position signal could be used to take into account the sensory consequences of eye movements and map the fleeting positions of objects on the retina onto their stable position in the world. Visual input arrives as a series of snapshots, each taken from a different line of sight, due to eye movements from one part of a scene to another. How do we nevertheless see a stable visual world? Morris and Krekelberg show that in primary visual cortex, the neural representation of each snapshot includes “metadata” that tracks gaze direction. |
Aidan P. Murphy; David A. Leopold A parameterized digital 3D model of the Rhesus macaque face for investigating the visual processing of social cues Journal Article In: Journal of Neuroscience Methods, vol. 324, pp. 1–14, 2019. @article{Murphy2019,Background: Rhesus macaques are the most popular model species for studying the neural basis of visual face processing and social interaction using intracranial methods. However, the challenge of creating realistic, dynamic, and parametric macaque face stimuli has limited the experimental control and ethological validity of existing approaches. New method: We performed statistical analyses of in vivo computed tomography data to generate an anatomically accurate, three-dimensional representation of Rhesus macaque cranio-facial morphology. The surface structures were further edited, rigged and textured by a professional digital artist with careful reference to photographs of macaque facial expression, colouration and pelage. Results: The model offers precise, continuous, parametric control of craniofacial shape, emotional expression, head orientation, eye gaze direction, and many other parameters that can be adjusted to render either static or dynamic high-resolution faces. Example single-unit responses to such stimuli in macaque inferotemporal cortex demonstrate the value of parametric control over facial appearance and behaviours. Comparison with existing method(s): The generation of such a high-dimensionality and systematically controlled stimulus set of conspecific faces, with accurate craniofacial modelling and professional finalization of facial details, is currently not achievable using existing methods. Conclusions: The results herald a new set of possibilities in adaptive sampling of a high-dimensional and socially meaningful feature space, thus opening the door to systematic testing of hypotheses about the abundant neural specialization for faces found in the primate. |
Sunny Nigam; Sorin Pojoga; Valentin Dragoi Synergistic coding of visual information in columnar networks Journal Article In: Neuron, vol. 104, no. 2, pp. 402–411.e4, 2019. @article{Nigam2019,Incoming stimuli are encoded collectively by populations of cortical neurons, which transmit information by using a neural code thought to be predominantly redundant. Redundant coding is widely believed to reflect a design choice whereby neurons with overlapping receptive fields sample environmental stimuli to convey similar information. Here, we performed multi-electrode laminar recordings in awake monkey V1 to report significant synergistic interactions between nearby neurons within a cortical column. These interactions are clustered non-randomly across cortical layers to form synergy and redundancy hubs. Homogeneous sub-populations comprising synergy hubs decode stimulus information significantly better compared to redundancy hubs or heterogeneous sub-populations. Mechanistically, synergistic interactions emerge from the stimulus dependence of correlated activity between neurons. Our findings suggest a refinement of the prevailing ideas regarding coding schemes in sensory cortex: columnar populations can efficiently encode information due to synergistic interactions even when receptive fields overlap and shared noise between cells is high. |
Kaiser Niknam; Amir Akbarian; Kelsey Clark; Yasin Zamani; Behrad Noudoost; Neda Nategh 2019. @book{Niknam2019,In many brain areas, sensory responses are heavily modulated by factors including attentional state, context, reward history, motor preparation, learned associations, and other cognitive variables. Modelling the effect of these modulatory factors on sensory responses has proven challenging, mostly due to the time-varying and nonlinear nature of the underlying computations. Here we present a computational model capable of capturing and dissociating multiple time-varying modulatory effects on neuronal responses on the order of milliseconds. The model's performance is tested on extrastriate perisaccadic visual responses in nonhuman primates. Visual neurons respond to stimuli presented around the time of saccades differently than during fixation. These perisaccadic changes include sensitivity to the stimuli presented at locations outside the neuron's receptive field, which suggests a contribution of multiple sources to perisaccadic response generation. Current computational approaches cannot quantitatively characterize the contribution of each modulatory source in response generation, mainly due to the very short timescale on which the saccade takes place. In this study, we use a high spatiotemporal resolution experimental paradigm along with a novel extension of the generalized linear model framework (GLM), termed the sparse-variable GLM, to allow for time-varying model parameters representing the temporal evolution of the system with a resolution on the order of milliseconds. We used this model framework to precisely map the temporal evolution of the spatiotemporal receptive field of visual neurons in the middle temporal area during the execution of a saccade. Moreover, an extended model based on a factorization of the sparse-variable GLM allowed us to disassociate and quantify the contribution of individual sources to the perisaccadic response. Our results show that our novel framework can precisely capture the changes in sensitivity of neurons around the time of saccades, and provide a general framework to quantitatively track the role of multiple modulatory sources over time. |
Mariann Oemisch; Stephanie Westendorff; Marzyeh Azimi; Seyed Alireza Hassani; Salva Ardid; Paul Tiesinga; Thilo Womelsdorf Feature-specific prediction errors and surprise across macaque fronto-striatal circuits Journal Article In: Nature Communications, vol. 10, pp. 176, 2019. @article{Oemisch2019,To adjust expectations efficiently, prediction errors need to be associated with the precise features that gave rise to the unexpected outcome, but this credit assignment may be problematic if stimuli differ on multiple dimensions and it is ambiguous which feature dimension caused the outcome. Here, we report a potential solution: neurons in four recorded areas of the anterior fronto-striatal networks encode prediction errors that are specific to feature values of different dimensions of attended multidimensional stimuli. The most ubiquitous prediction error occurred for the reward-relevant dimension. Feature-specific prediction error signals a) emerge on average shortly after non-specific prediction error signals, b) arise earliest in the anterior cingulate cortex and later in dorsolateral prefrontal cortex, caudate and ventral striatum, and c) contribute to feature-based stimulus selection after learning. Thus, a widely-distributed feature-specific eligibility trace may be used to update synaptic weights for improved feature-based attention. |
Davide Paoletti; Christoph Braun; Elisabeth Julie Vargo; Wieske Zoest Spontaneous pre-stimulus oscillatory activity shapes the way we look: A concurrent imaging and eye-movement study Journal Article In: European Journal of Neuroscience, vol. 49, pp. 137–149, 2019. @article{Paoletti2019,Previous behavioural studies have accrued evidence that response time plays a critical role in determining whether selection is influenced by stimulus saliency or target template. In the present work, we investigated to what extent the variations in timing and consequent oculomotor controls are influenced by spontaneous variations in pre-stimulus alpha oscillations. We recorded simultaneously brain activity using magnetoencephalography (MEG) and eye movements while participants performed a visual search task. Our results show that slower saccadic reaction times were predicted by an overall stronger alpha power in the 500 ms time window preceding the stimulus onset, while weaker alpha power was a signature of faster responses. When looking separately at performance for fast and slow responses, we found evidence for two specific sources of alpha activity predicting correct versus incorrect responses. When saccades were quickly elicited, errors were predicted by stronger alpha activity in posterior areas, comprising the angular gyrus in the temporal-parietal junction (TPJ) and possibly the lateral intraparietal area (LIP). Instead, when participants were slower in responding, an increase of alpha power in frontal eye fields (FEF), supplementary eye fields (SEF) and dorsolateral pre-frontal cortex (DLPFC) predicted erroneous saccades. In other words, oculomotor accuracy in fast responses was predicted by alpha power differences in more posterior areas, while the accuracy in slow responses was predicted by alpha power differences in frontal areas, in line with the idea that these areas may be differentially related to stimulus-driven and goal-driven control of selection. |
Michael A. Paradiso; Seth Akers-Campbell; Octavio Ruiz; James E. Niemeyer; Stuart Geman; Jackson Loper Transsacadic information and corollary discharge in local field potentials of macaque V1 Journal Article In: Frontiers in Integrative Neuroscience, vol. 12, pp. 63, 2019. @article{Paradiso2019,Approximately three times per second, human visual perception is interrupted by a saccadic eye movement. In addition to taking the eyes to a new location, several lines of evidence suggest that the saccades play multiple roles in visual perception. Indeed, it may be crucial that visual processing is informed about movements of the eyes in order to analyze visual input distinctly and efficiently on each fixation and preserve stable visual perception of the world across saccades. A variety of studies has demonstrated that activity in multiple brain areas is modulated by saccades. The hypothesis tested here is that these signals carry significant information that could be used in visual processing. To test this hypothesis, local field potentials (LFPs) were simultaneously recorded from multiple electrodes in macaque primary visual cortex (V1); support vector machines (SVMs) were used to classify the peri-saccadic LFPs. We find that LFPs in area V1 carry information that can be used to distinguish neural activity associated with fixations from saccades, precisely estimate the onset time of fixations, and reliably infer the directions of saccades. This information may be used by the brain in processes including visual stability, saccadic suppression, receptive field (RF) remapping, fixation amplification, and trans-saccadic visual perception. |
Aishwarya Parthasarathy; Cheng Tang; Roger Herikstad; Loong Fah Cheong; Shih Cheng Yen; Camilo Libedinsky Time-invariant working memory representations in the presence of code-morphing in the lateral prefrontal cortex Journal Article In: Nature Communications, vol. 10, pp. 4995, 2019. @article{Parthasarathy2019,Maintenance of working memory is thought to involve the activity of prefrontal neuronal populations with strong recurrent connections. However, it was recently shown that distractors evoke a morphing of the prefrontal population code, even when memories are maintained throughout the delay. How can a morphing code maintain time-invariant memory information? We hypothesized that dynamic prefrontal activity contains time-invariant memory information within a subspace of neural activity. Using an optimization algorithm, we found a low-dimensional subspace that contains time-invariant memory information. This information was reduced in trials where the animals made errors in the task, and was also found in periods of the trial not used to find the subspace. A bump attractor model replicated these properties, and provided predictions that were confirmed in the neural data. Our results suggest that the high-dimensional responses of prefrontal cortex contain subspaces where different types of information can be simultaneously encoded with minimal interference. |
Alina Peter; Cem Uran; Johanna Klon-Lipok; Rasmus Roese; Sylvia Van Stijn; William Barnes; Jarrod R. Dowdall; Wolf Singer; Pascal Fries; Martin Vinck Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations Journal Article In: eLife, vol. 8, pp. 1–38, 2019. @article{Peter2019,The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30–80 Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context. |
Dina V. Popovkina; Wyeth Bair; Anitha Pasupathy Modeling diverse responses to filled and outline shapes in macaque V4 Journal Article In: Journal of Neurophysiology, vol. 121, no. 3, pp. 1059–1077, 2019. @article{Popovkina2019,Visual area V4 is an important midlevel cortical processing stage that subserves object recognition in primates. Studies investigating shape coding in V4 have largely probed neuronal responses with filled shapes, i.e., shapes defined by both a boundary and an interior fill. As a result, we do not know whether form-selective V4 responses are dictated by boundary features alone or if interior fill is also important. We studied 43 V4 neurons in two male macaque monkeys ( Macaca mulatta) with a set of 362 filled shapes and their corresponding outlines to determine how interior fill modulates neuronal responses in shape-selective neurons. Only a minority of neurons exhibited similar response strength and shape preferences for filled and outline stimuli. A majority responded preferentially to one stimulus category (either filled or outline shapes) and poorly to the other. Our findings are inconsistent with predictions of the hierarchical-max (HMax) V4 model that builds form selectivity from oriented boundary features and takes little account of attributes related to object surface, such as the phase of the boundary edge. We modified the V4 HMax model to include sensitivity to interior fill by either removing phase-pooling or introducing unoriented units at the V1 level; both modifications better explained our data without increasing the number of free parameters. Overall, our results suggest that boundary orientation and interior surface information are both maintained until at least the midlevel visual representation, consistent with the idea that object fill is important for recognition and perception in natural vision. |
Pascal Wallisch; J. Anthony Movshon Responses of neurons in macaque MT to unikinetic plaids Journal Article In: Journal of Neurophysiology, vol. 122, no. 5, pp. 1937–1945, 2019. @article{Wallisch2019,Response properties of MT neurons are often studied with “bikinetic” plaid stimuli, which consist of two superimposed sine wave gratings moving in different directions. Oculomotor studies using “unikinetic plaids” in which only one of the two superimposed gratings moves suggest that the eyes first move reflexively in the direction of the moving grating and only later converge on the perceived direction of the moving pattern. MT has been implicated as the source of visual signals that drives these responses. We wanted to know whether stationary gratings, which have little effect on MT cells when presented alone, would influence MT responses when paired with a moving grating. We recorded extracellularly from neurons in area MT and measured responses to stationary and moving gratings, and to their sums: bikinetic and unikinetic plaids. As expected, stationary gratings presented alone had a very modest influence on the activity of MT neurons. Responses to moving gratings and bikinetic plaids were similar to those previously reported and revealed cells selective for the motion of plaid patterns and of their components (pattern and component cells). When these neurons were probed with unikinetic plaids, pattern cells shifted their direction preferences in a way that revealed the influence of the static grating. Component cell preferences shifted little or not at all. These results support the notion that pattern-selective neurons in area MT integrate component motions that differ widely in speed, and that they do so in a way that is consistent with an intersection-of-constraints model. |
Ting Yan; Hui Hui Zhou Synchronization between frontal eye field and area V4 during free-gaze visual search Journal Article In: Zoological research, vol. 40, no. 5, pp. 394–403, 2019. @article{Yan2019d,Information flow between the prefrontal and visual cortices is critical for visual behaviors such as visual search. To investigate its mechanisms, we simultaneously recorded spike and local field potential (LFP) signals in the frontal eye field (FEF) and area V4 while monkeys performed a free-gaze visual search task. During free-gaze search, spike-LFP coherence between FEF and V4 was enhanced in the theta rhythm (4-8 Hz) but suppressed in the alpha rhythm (8-13 Hz). Cross-frequency couplings during the Cue period before the search phase were related to monkey performance, with higher FEF theta-V4 gamma coupling and lower FEF alpha-V4 gamma coupling associated with faster search. Finally, feature-based attention during search enhanced spike-LFP coherence between FEF and V4 in the gamma and beta rhythms, whereas overt spatial attention reduced coherence at frequencies up to 30 Hz. These results suggest that oscillatory coupling may play an important role in mediating interactions between the prefrontal and visual cortices during visual search. |
Man Yi Yim; Xinying Cai; Xiao Jing Wang Transforming the choice outcome to an action plan in monkey lateral prefrontal cortex: A neural circuit model Journal Article In: Neuron, vol. 103, no. 3, pp. 520–532.e5, 2019. @article{Yim2019,In economic decisions, we make a good-based choice first, then we transform the outcome into an action to obtain the good. To elucidate the network mechanisms for such transformation, we constructed a neural circuit model consisting of modules representing choice, integration of choice with target locations, and the final action plan. We examined three scenarios regarding how the final action plan could emerge in the neural circuit and compared their implications with experimental data. Our model with heterogeneous connectivity predicts the coexistence of three types of neurons with distinct functions, confirmed by analyzing the neural activity in the lateral prefrontal cortex (LPFC) of behaving monkeys. We obtained a much more distinct classification of functional neuron types in the ventral than the dorsal region of LPFC, suggesting that the action plan is initially generated in ventral LPFC. Our model offers a biologically plausible neural circuit architecture that implements good-to-action transformation during economic choice. Yim et al. propose a circuit model that implements good-to-action transformation during economic choice. Heterogeneity in circuit synaptic connections is crucial for the coexistence of distinct functional neuron types, which is confirmed by cluster analysis of neuronal activity in LPFC. |
Konstantin F. Willeke; Xiaoguang Tian; Antimo Buonocore; Joachim Bellet; Araceli Ramirez-Cardenas; Ziad M. Hafed Memory-guided microsaccades Journal Article In: Nature Communications, vol. 10, pp. 3710, 2019. @article{Willeke2019,Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior. |
J. Kael White; Ethan S. Bromberg-Martin; Sarah R. Heilbronner; Kaining Zhang; Julia Pai; Suzanne N. Haber; Ilya E. Monosov A neural network for information seeking Journal Article In: Nature Communications, vol. 10, pp. 5168, 2019. @article{White2019a,Humans and other animals often show a strong desire to know the uncertain rewards their future has in store, even when they cannot use this information to influence the outcome. However, it is unknown how the brain predicts opportunities to gain information and motivates this information-seeking behavior. Here we show that neurons in a network of interconnected subregions of primate anterior cingulate cortex and basal ganglia predict the moment of gaining information about uncertain rewards. Spontaneous increases in their information prediction signals are followed by gaze shifts toward objects associated with resolving uncertainty, and pharmacologically disrupting this network reduces the motivation to seek information. These findings demonstrate a cortico-basal ganglia mechanism responsible for motivating actions to resolve uncertainty by seeking knowledge about the future. |
Brian J. White; Laurent Itti; Douglas P. Munoz Superior colliculus encodes visual saliency during smooth pursuit eye movements Journal Article In: European Journal of Neuroscience, pp. 1–11, 2019. @article{White2019,The saliency map has played a long-standing role in models and theories of visual attention, and it is now supported by neurobiological evidence from several cortical and subcortical brain areas. While visual saliency is computed during moments of active fixation, it is not known whether the same is true while engaged in smooth pursuit of a moving stimulus, which is very common in real-world vision. Here, we examined extrafoveal saliency coding in the superior colliculus, a midbrain area associated with attention and gaze, during smooth pursuit eye movements. We found that SC neurons from the superficial visual layers showed a robust representation of peripheral saliency evoked by a conspicuous stimulus embedded in a wide-field array of goal-irrelevant stimuli. In contrast, visuomotor neurons from the intermediate saccade-related layers showed a poor saliency representation, even though most of these neurons were visually responsive during smooth pursuit. These results confirm and extend previous findings that place the SCs in a unique role as a saliency map that monitors peripheral vision during foveation of stationary and now moving objects. |
Jacob A. Westerberg; Michele A. Cox; Kacie Dougherty; Alexander Maier V1 microcircuit dynamics: Altered signal propagation suggests intracortical origins for adaptation in response to visual repetition Journal Article In: Journal of Neurophysiology, vol. 121, no. 5, pp. 1938–1952, 2019. @article{Westerberg2019,Repetitive visual stimulation profoundly changes sensory processing in the primary visual cortex (V1). We show how the associated adaptive changes are linked to an altered flow of synaptic activation across the V1 laminar microcircuit. Using repeated visual stimulation, we recorded layer-specific responses in V1 of two fixating monkeys. We found that repetition-related spiking suppression was most pronounced outside granular V1 layers that receive the main retinogeniculate input. This repetition-related response suppression was robust to alternating stimuli between the eyes, in line with the notion that repetition-related adaptation is predominantly of cortical origin. Most importantly, current source density (CSD) analysis, which provides an estimate of local net depolarization, revealed that synaptic processing during repeated stimulation was most profoundly affected within supragranular layers, which harbor the bulk of corticocortical connections. Direct comparison of the temporal evolution of laminar CSD and spiking activity showed that stimulus repetition first affected supragranular synaptic currents, which translated into a reduction of stimulus-evoked spiking across layers. Together, these results suggest that repetition induces an altered state of intracortical processing that underpins visual adaptation. |
Andrew D. Zaharia; Robbe L. T. Goris; J. Anthony Movshon; Eero P. Simoncelli Compound stimuli reveal the structure of visual motion selectivity in macaque MT neurons Journal Article In: eNeuro, vol. 6, no. 6, pp. 1–19, 2019. @article{Zaharia2019,Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (“frequency-separable”). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (“velocity-separable”). This construction explains “pattern direction-selective” MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. We designed a set of experiments to distinguish frequency-separable and velocity-separable models and executed them with single-unit recordings in macaque V1 and MT. Surprisingly, when tested with single drifting gratings, most MT neurons' responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions. |
Kaining Zhang; Charles D. Chen; Ilya E. Monosov Novelty, salience, and surprise timing are signaled by neurons in the basal forebrain Journal Article In: Current Biology, vol. 29, no. 1, pp. 134–142, 2019. @article{Zhang2019g,The basal forebrain (BF) is a principal source of modulation of the neocortex [1–6] and is thought to regulate cognitive functions such as attention, motivation, and learning by broadcasting information about salience [2, 3, 5, 7–19]. However, events can be salient for multiple reasons—such as novelty, surprise, or reward prediction errors [20–24]—and to date, precisely which salience-related information the BF broadcasts isunclear.Here, wereport that theprimate BF contains at least two types of neurons that often process salient events in distinct manners: one with phasic burst responses to cues predicting salient events and one with ramping activity anticipating such events. Bursting neurons respond to cues that convey predictions about the magnitude, probability, and timing of primary reinforcements. They also burst to the reinforcement itself, particularly when it is unexpected. However, they do not have a selective response to reinforcement omission (the unexpected absence of an event). Thus, bursting neurons do not convey value-prediction errors but do signal surprise associated with external events. Indeed, they are not limited to processing primary reinforcement: they discriminate fully expected novel visual objects from familiar objects and respond to object-sequence violations. In contrast, ramping neurons predict the timing of many salient, novel, and surprising events. Their ramping activity is highly sensitive to the subjects' confidence in event timing and on average encodes the subjects' surprise after unexpected events occur. These data suggest that the primate BF contains mechanisms to anticipate the timing of a diverse set of important external events (via ramping activity) and to rapidly deploy cognitive resources when these events occur (via short latency bursting). |
Maya Zhe Wang; Benjamin Y. Hayden Monkeys are curious about counterfactual outcomes Journal Article In: Cognition, vol. 189, pp. 1–10, 2019. @article{Wang2019g,Many non-human animals show exploratory behaviors. It remains unclear whether any possess human-like curiosity. We previously proposed three criteria for applying the term curiosity to animal behavior: (1) the subject is willing to sacrifice reward to obtain information, (2) the information provides no immediate instrumental or strategic benefit, and (3) the amount the subject is willing to pay depends systematically on the amount of information available. In previous work on information-seeking in animals, information generally predicts upcoming rewards, and animals' decisions may therefore be a byproduct of reinforcement processes. Here we get around this potential confound by taking advantage of macaques' ability to reason counterfactually (that is, about outcomes that could have occurred had the subject chosen differently). Specifically, macaques sacrificed fluid reward to obtain information about counterfactual outcomes. Moreover, their willingness to pay scaled with the information (Shannon entropy) offered by the counterfactual option. These results demonstrate the existence of human-like curiosity in non-human primates according to our criteria, which circumvent several confounds associated with less stringent criteria. |
Lyndon Duong; Matthew Leavitt; Florian Pieper; Adam Sachs; Julio Martinez-Trujillo A normalization circuit underlying coding of spatial attention in primate lateral prefrontal cortex Journal Article In: eNeuro, vol. 6, no. 2, pp. 1–23, 2019. @article{Duong2019,Lateral prefrontal cortex (LPFC) neurons signal the allocation of voluntary attention; however, the neural computations underlying this function remain unknown. To investigate this, we recorded from neuronal ensembles in the LPFC of two Macaca fascicularis performing a visuospatial attention task. LPFC neural responses to a single stimulus were normalized when additional stimuli/distracters appeared across the visual field and were wellcharacterized by an averaging computation. Deploying attention toward an individual stimulus surrounded by distracters shifted neural activity from an averaging regime toward a regime similar to that when the attended stimulus was presented in isolation (winner-take-all; WTA). However, attentional modulation is both qualitatively and quantitatively dependent on a neuron's visuospatial tuning. Our results show that during attentive vision, LPFC neuronal ensemble activity can be robustly read out by downstream areas to generate motor commands, and/or fed back into sensory areas to filter out distracter signals in favor of target signals. |