EyeLink非人类灵长类出版物
All EyeLink non-human primate research publications up until 2024 (with some early 2025s) 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!
2025 |
Timo Kerkoerle; Louise Pape; Milad Ekramnia; Xiaoxia Feng; Jordy Tasserie; Morgan Dupont; Xiaolian Li; Bechir Jarraya; Wim Vanduffel; Stanislas Dehaene; Ghislaine Dehaene-Lambertz Brain mechanisms of reversible symbolic reference: A potential singularity of the human brain Journal Article In: eLife, vol. 12, pp. 1–28, 2025. @article{Kerkoerle2025, The emergence of symbolic thinking has been proposed as a dominant cognitive criterion to distinguish humans from other primates during hominization. Although the proper definition of a symbol has been the subject of much debate, one of its simplest features is bidirectional attachment: the content is accessible from the symbol, and vice versa. Behavioral observations scattered over the past four decades suggest that this criterion might not be met in non-human primates, as they fail to generalize an association learned in one temporal order (A to B) to the reverse order (B to A). Here, we designed an implicit fMRI test to investigate the neural mechanisms of arbitrary audio-visual and visual-visual pairing in monkeys and humans and probe their spontaneous reversibility. After learning a unidirectional association, humans showed surprise signals when this learned association was violated. Crucially, this effect occurred spontaneously in both learned and reversed directions, within an extended network of high-level brain areas, including, but also going beyond the language network. In monkeys, by contrast, violations of association effects occurred solely in the learned direction and were largely confined to sensory areas. We propose that a human-specific brain network may have evolved the capacity for reversible symbolic reference. ### Competing Interest Statement The authors have declared no competing interest. |
Elle Minh Ngoc Le Nguyen; Meaghan J. Clough; Joanne Fielding; Owen B. White A video-oculography study of fixation instability in myasthenia gravis Journal Article In: Frontiers in Neurology, vol. 16, pp. 1–9, 2025. @article{Nguyen2025, Introduction: Myasthenia gravis (MG) is an autoimmune disease that causes extraocular muscle weakness in up to 70–85% of patients, which can impact quality of life. Current diagnostic measures are not very sensitive for ocular MG. This study aimed to compare fixation instability (inability to maintain gaze on a target) in patients with MG with control participants using video-oculography. Methods: A prospective study of 20 age-and sex-matched MG and control participants was performed using a novel protocol with the EyeLink 1000 plus ©. Bivariate contour ellipse area (BCEA) analysis, number of fixations on a target, and percentage of dwell time of fixations in the target interest area (IA) were calculated. Inter-eye (right vs. left) comparisons were performed using paired t-tests, and inter-group (MG vs. control) comparisons were performed using independent samples t-tests. Results: There were no inter-eye differences in the BCEAs between control eyes and MG eyes. However, the BCEAs were larger in both the right (RE) and left (LE) eyes of MG patients in the right (RE p = 0.029, LE p = 0.033), left (RE p = 0.006, LE p = 0.004), upward (RE p = 0.009, LE p = 0.018), and downward (RE p = 0.006, LE p = 0.006) gaze holds of the controls. The total mean sum of gaze hold fixations in all directions was greater in MG patients than in control participants (354 ± 139 vs. 249 ± 135 |
Pierre Pouget; Pierre Daye; Martin Paré Cognitive and kinematic markers of ketamine effects in behaving non-human primates Journal Article In: European Journal of Pharmacology, vol. 987, pp. 1–7, 2025. @article{Pouget2025, Ketamine is widely used to probe cognitive functions relying on the properties of methyl-D-aspartate receptor (NMDAR) synaptic transmission. Numerous works have proved that cognitive performance and adjustments in the decision or perceptual domains are affected after ketamine injection in general circulation of primates. Here, we take advantage of that in the brain stem; horizontal saccade deceleration is controlled by glycine-NMDAR-gated current, while gamma-aminobutyric acid (GABA) current controls vertical deceleration to demonstrate that despite general circulation level manipulation of NMDAR synaptic transmission, the kinematic of the saccade appeared to be in the motor brainstem generator circuit differentially maintained. The results show that the deacceleration of the saccade elicited toward a horizontal target was substantially decreased, while the deacceleration of a vertical saccade remained largely unaffected. These results provide functional distinct markers for estimating cognitive and kinematic NMDAR-gated specificity acting in the pre-frontal cortex while maintaining specificity among the GABA circuit of drugs in general circulation. |
Meizhen Qian; Jianbao Wang; Yang Gao; Ming Chen; Yin Liu; Dengfeng Zhou; Haidong D Lu; Xiaotong Zhang; Jia Ming Hu; Anna Wang Roe Multiple loci for foveolar vision in macaque monkey visual cortex Journal Article In: Nature Neuroscience, vol. 28, no. 1, pp. 137–149, 2025. @article{Qian2025, In humans and nonhuman primates, the central 1° of vision is processed by the foveola, a retinal structure that comprises a high density of photoreceptors and is crucial for primate-specific high-acuity vision, color vision and gaze-directed visual attention. Here, we developed high-spatial-resolution ultrahigh-field 7T functional magnetic resonance imaging methods for functional mapping of the foveolar visual cortex in awake monkeys. In the ventral pathway (visual areas V1–V4 and the posterior inferior temporal cortex), viewing of a small foveolar spot elicits a ring of multiple (eight) foveolar representations per hemisphere. This ring surrounds an area called the ‘foveolar core', which is populated by millimeter-scale functional domains sensitive to fine stimuli and high spatial frequencies, consistent with foveolar visual acuity, color and achromatic information and motion. Thus, this elaborate rerepresentation of central vision coupled with a previously unknown foveolar core area signifies a cortical specialization for primate foveation behaviors. |
Rishi Rajalingham; Hansem Sohn; Mehrdad Jazayeri Dynamic tracking of objects in the macaque dorsomedial frontal cortex Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–16, 2025. @article{Rajalingham2025, A central tenet of cognitive neuroscience is that humans build an internal model of the external world and use mental simulation of the model to perform physical inferences. Decades of human experiments have shown that behaviors in many physical reasoning tasks are consistent with predictions fromthemental simulation theory. However, evidence for the defining feature ofmental simulation – that neural population dynamics reflect simulations of physical states in the environment – is limited. We test the mental simulation hypothesis by combining a naturalistic ball-interception task, large-scale electrophysiology in non-human primates, and recurrent neural network modeling. We find that neurons in the monkeys' dorsomedial frontal cortex (DMFC) represent task-relevant information about the ball position in a mul- tiplexed fashion. At a population level, the activity pattern in DMFC comprises a low-dimensional neural embedding that tracks the ball both when it is visible and invisible, serving as a neural substrate for mental simulation. A systematic comparison of different classes of task-optimized RNN models with the DMFC data provides further evidence supporting the mental simulation hypothesis. Our findings provide evidence that neural dynamics in the frontal cortex are consistent with internal simulation of external states in the environment. |
Mohamad Abbass; Benjamin Corrigan; Renée Johnston; Roberto Gulli; Adam Sachs; Jonathan C. Lau; Julio Martinez-Trujillo Prefrontal cortex neuronal ensembles dynamically encode task features during associative memory and virtual navigation Journal Article In: Cell Reports, vol. 44, no. 1, pp. 1–23, 2025. @article{Abbass2025, Neuronal populations expand their information-encoding capacity using mixed selective neurons. This is particularly prominent in association areas such as the lateral prefrontal cortex (LPFC), which integrate information from multiple sensory systems. However, during conditions that approximate natural behaviors, it is unclear how LPFC neuronal ensembles process space- and time-varying information about task features. Here, we show that, during a virtual reality task with naturalistic elements that requires associative memory, individual neurons and neuronal ensembles in the primate LPFC dynamically mix unconstrained features of the task, such as eye movements, with task-related visual features. Neurons in dorsal regions show more selectivity for space and eye movements, while ventral regions show more selectivity for visual features, representing them in a separate subspace. In summary, LPFC neurons exhibit dynamic and mixed selectivity for unconstrained and constrained task elements, and neural ensembles can separate task features in different subspaces. |
He Chen; Jun Kunimatsu; Tomomichi Oya; Yuri Imaizumi; Yukiko Hori; Masayuki Matsumoto; Yasuhiro Tsubo; Okihide Hikosaka; Takafumi Minamimoto; Yuji Naya; Hiroshi Yamada Formation of brain-wide neural geometry during visual item recognition in monkeys Journal Article In: iScience, vol. 28, no. 3, pp. 1–17, 2025. @article{Chen2025, Neural dynamics are thought to reflect computations that relay and transform information in the brain. Previous studies have identified the neural population dynamics in many individual brain regions as a trajectory geometry, preserving a common computational motif. However, whether these populations share particular geometric patterns across brain-wide neural populations remains unclear. Here, by mapping neural dynamics widely across temporal/frontal/limbic regions in the cortical and subcortical structures of monkeys, we show that 10 neural populations, including 2,500 neurons, propagate visual item information in a stochastic manner. We found that visual inputs predominantly evoked rotational dynamics in the higher-order visual area, TE, and its downstream striatum tail, while curvy/straight dynamics appeared frequently downstream in the orbitofrontal/hippocampal network. These geometric changes were not deterministic but rather stochastic according to their respective emergence rates. Our meta-analysis results indicate that visual information propagates as a heterogeneous mixture of stochastic neural population signals in the brain. |
Leor N. Katz; Martin O. Bohlen; Gongchen Yu; Carlos Mejias-Aponte; Marc A. Sommer; Richard J. Krauzlis Optogenetic manipulation of covert attention in the nonhuman primate Journal Article In: Journal of Cognitive Neuroscience, vol. 37, no. 2, pp. 266–285, 2025. @article{Katz2025, Optogenetics affords new opportunities to interrogate neuronal circuits that control behavior. In primates, the usefulness of optogenetics in studying cognitive functions remains a challenge. The technique has been successfully wielded, but behavioral effects have been demonstrated primarily for sensorimotor processes. Here, we tested whether brief optogenetic suppression of primate superior colliculus can change performance in a covert attention task, in addition to previously reported optogenetic effects on saccadic eye movements. We used an attention task that required the monkey to detect and report a stimulus change at a cued location via joystick release, while ignoring changes at an uncued location. When the cued location was positioned in the response fields of transduced neurons in the superior colliculus, transient light delivery coincident with the stimulus change disrupted the monkey's detection performance, significantly lowering hit rates. When the cued location was elsewhere, hit rates were unaltered, indicating that the effect was spatially specific and not a motor deficit. Hit rates for trials with only one stimulus were also unaltered, indicating that the effect depended on selection among distractors rather than a low-level visual impairment. Psychophysical analysis revealed that optogenetic suppression increased perceptual threshold, but only for locations matching the transduced site. These data show that optogenetic manipulations can cause brief and spatially specific deficits in covert attention, independent of sensorimotor functions. This dissociation of effect, and the temporal precision provided by the technique, demonstrates the utility of optogenetics in interrogating neuronal circuits that mediate cognitive functions in the primate. |
Xinhe Liu; Zhiting Zhang; Lu Gan; Panke Yu; Ji Dai Medium spiny neurons mediate timing perception in coordination with prefrontal neurons in primates Journal Article In: Advanced Science, pp. 1–15, 2025. @article{Liu2025, Timing perception is a fundamental cognitive function that allows organisms to navigate their environment effectively, encompassing both prospective and retrospective timing. Despite significant advancements in understanding how the brain processes temporal information, the neural mechanisms underlying these two forms of timing remain largely unexplored. In this study, it aims to bridge this knowledge gap by elucidating the functional roles of various neuronal populations in the striatum and prefrontal cortex (PFC) in shaping subjective experiences of time. Utilizing a large-scale electrode array, it recorded responses from over 3000 neurons in the striatum and PFC of macaque monkeys during timing tasks. The analysis classified neurons into distinct groups and revealed that retrospective and prospective timings are governed by separate neural processes. Specifically, this study demonstrates that medium spiny neurons (MSNs) in the striatum play a crucial role in facilitating these timing processes. Through cell-type-specific manipulation, it identified D2-MSNs as the primary contributors to both forms of timing. Additionally, the findings indicate that effective processing of timing requires coordination between the PFC and the striatum. In summary, this study advances the understanding of the neural foundations of timing perception and highlights its behavioral implications. |
Stella Mayer; Pankhuri Saxena; Max Arwed Crayen; Stefan Treue In: Journal of Neuroscience Methods, vol. 415, pp. 1–11, 2025. @article{Mayer2025, Background: Neuronal activity is modulated by behavior and cognitive processes. The combination of several neurotransmitter systems, acting directly or indirectly on specific populations of neurons, underlie such modulations. Most studies with non-human primates (NHPs) fail to capture this complexity, partly due to the lack of adequate methods for reliably and simultaneously measuring a broad spectrum of neurotransmitters while the animal engages in behavioral tasks. New Method: To address this gap, we introduce a novel implementation of brain microdialysis (MD), employing semi-chronically implanted guides and probes in awake, behaving NHPs facilitated by removable insets within a standard recording chamber over extrastriate visual cortex (here, the visual middle temporal area (MT)). This approach allows flexible access to diverse brain regions, including areas deep within the sulcus. Results: Reliable concentration measurements of GABA, glutamate, norepinephrine, epinephrine, dopamine, serotonin, and choline were achieved from small sample volumes (<20 µl) using ultra-performance liquid chromatography with electrospray ionization-mass spectrometry (UPLC-ESI-MS). Comparing two behavioral states – ‘active' and ‘inactive', we observe subtle concentration variations between the two behavioral states and a greater variability of concentrations in the active state. Additionally, we find positively and negatively correlated concentration changes for neurotransmitter pairs between the behavioral states. Conclusions: Therefore, this MD setup allows insights into the neurochemical dynamics in awake primates, facilitating comprehensive investigations into the roles and the complex interplay of neurotransmitters in cognitive and behavioral functions. |
Ramanujan Srinath; Amy M. Ni; Claire Marucci; Marlene R. Cohen; David H. Brainard Orthogonal neural representations support perceptual judgements of natural stimuli Journal Article In: Scientific Reports, vol. 15, pp. 1–17, 2025. @article{Srinath2025, In natural behavior, observers must separate relevant information from a barrage of irrelevant information. Many studies have investigated the neural underpinnings of this ability using artificial stimuli presented on simple backgrounds. Natural viewing, however, carries a set of challenges that are inaccessible using artificial stimuli, including neural responses to background objects that are task-irrelevant. An emerging body of evidence suggests that the visual abilities of humans and animals can be modeled through the linear decoding of task-relevant information from visual cortex. This idea suggests the hypothesis that irrelevant features of a natural scene should impair performance on a visual task only if their neural representations intrude on the linear readout of the task relevant feature, as would occur if the representations of task-relevant and irrelevant features are not orthogonal in the underlying neural population. We tested this hypothesis using human psychophysics and monkey neurophysiology, in response to parametrically variable naturalistic stimuli. We demonstrate that 1) the neural representation of one feature (the position of a central object) in visual area V4 is orthogonal to those of several background features, 2) the ability of human observers to precisely judge object position was largely unaffected by task-irrelevant variation in those background features, and 3) many features of the object and the background are orthogonally represented by V4 neural responses. Our observations are consistent with the hypothesis that orthogonal neural representations support stable perception of objects and features despite the tremendous richness of natural visual scenes. |
Ekin Tünçok; Lynne Kiorpes; Marisa Carrasco Opposite asymmetry in visual perception of humans and macaques Journal Article In: Current Biology, vol. 35, pp. 681–687, 2025. @article{Tuencok2025, In human adults, visual perception varies throughout the visual field. Performance decreases with eccentricity1,2 and varies around polar angle. At isoeccentric locations, performance is typically higher along the horizontal than vertical meridian (horizontal-vertical asymmetry [HVA]) and along the lower than the upper vertical meridian (vertical meridian asymmetry [VMA]). It is unknown whether the macaque visual system, the leading animal model for understanding human vision also exhibits these performance asymmetries. Here, we investigated whether and how visual field asymmetries differ between these two groups. Human adults and adult macaque monkeys (Macaca nemestrina) performed a two-alternative forced choice (2AFC) motion direction discrimination task for a target presented among distractors at isoeccentric locations. Both groups showed heterogeneous visual sensitivity around the visual field, but there were striking differences between them. Human observers showed a large VMA—their sensitivity was poorest at the upper vertical meridian—a weak horizontal-vertical asymmetry, and lower sensitivity at intercardinal locations. Macaque performance revealed an inverted VMA—their sensitivity was poorest in the lower vertical meridian. The opposite pattern of VMA in macaques and humans revealed in this study may reflect adaptive behavior by increasing discriminability at locations with greater relevance for visuomotor integration. This study reveals that performance also varies as a function of polar angle for monkeys, but in a different manner than in humans, and highlights the need to investigate species-specific similarities and differences in brain and behavior to constrain models of vision and brain function. |
Joshua O. Eayrs; Haya Serena Tobing; S. Tabitha Steendam; Nicoleta Prutean; Wim Notebaert; Jan R. Wiersema; Ruth M. Krebs; C. Nico Boehler Reward and efficacy modulate the rate of anticipatory pupil dilation Journal Article In: Psychophysiology, vol. 62, no. 1, pp. 1–12, 2025. @article{Eayrs2025, Pupil size is a well-established marker of cognitive effort, with greater efforts leading to larger pupils. This is particularly true for pupil size during task performance, whereas findings on anticipatory effort triggered by a cue stimulus are less consistent. For example, a recent report by Frömer et al. found that in a cued-Stroop task, behavioral performance and electrophysiological markers of preparatory effort allocation were modulated by cued reward and ‘efficacy' (the degree to which rewards depended on good performance), but pupil size did not show a comparable pattern. Here, we conceptually replicated this study, employing an alternative approach to the pupillometry analyses. In line with previous findings, we found no modulation of absolute pupil size in the cue-to-target interval. Instead, we observed a significant difference in the rate of pupil dilation in anticipation of the target: pupils dilated more rapidly for high-reward trials in which rewards depended on good performance. This was followed by a significant difference in absolute pupil size within the first hundreds of milliseconds following Stroop stimulus onset, likely reflecting a lagging effect of anticipatory effort allocation. Finally, the slope of pupil dilation was significantly correlated with behavioral response times, and this association was strongest for the high-reward, high-efficacy trials, further supporting that the rate of anticipatory pupil dilation reflects anticipatory effort. We conclude that pupil size is modulated by anticipatory effort, but in a highly temporally-specific manner, which is best reflected by the rate of dilation in the moments just prior to stimulus onset. |
Nico A. Flierman; Sue Ann Koay; Willem S. Hoogstraten; Tom J. H. Ruigrok; Pieter Roelfsema; Aleksandra Badura; Chris I. De Zeeuw Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques Journal Article In: eLife, vol. 13, pp. 1–23, 2025. @article{Flierman2025, The role of cerebellum in controlling eye movements is well established, but its contribution to more complex forms of visual behavior has remained elusive. To study cerebellar activity during visual attention we recorded extracellular activity of dentate nucleus (DN) neurons in two non-human primates (NHPs). NHPs were trained to read the direction indicated by a peripheral visual stimulus while maintaining fixation at the center, and report the direction of the cue by performing a saccadic eye movement into the same direction following a delay. We found that single-unit DN neurons modulated spiking activity over the entire time course of the task, and that their activity often bridged temporally separated intra-trial events, yet in a heterogeneous manner. To better understand the heterogeneous relationship between task structure, behavioral performance, and neural dynamics, we constructed a behavioral, an encoding, and a decoding model. Both NHPs showed different behavioral strategies, which influenced the performance. Activity of the DN neurons reflected the unique strategies, with the direction of the visual stimulus frequently being encoded long before an upcoming saccade. Moreover, the latency of the ramping activity of DN neurons following presentation of the visual stimulus was shorter in the better performing NHP. Labeling with the retrograde tracer Cholera Toxin B in the recording location in the DN indicated that these neurons predominantly receive inputs from Purkinje cells in the D1 and D2 zones of the lateral cerebellum as well as neurons of the principal olive and medial pons, all regions known to connect with neurons in the prefrontal cortex contributing to planning of saccades. Together, our results highlight that DN neurons can dynamically modulate their activity during a visual attention task, comprising not only sensorimotor but also cognitive attentional components. |
Jessica Heeman; Brian J. White; Stefan Van der Stigchel; Jan Theeuwes; Laurent Itti; Douglas P. Munoz Saliency response in superior colliculus at the future saccade goal predicts fixation duration during free viewing of dynamic scenes Journal Article In: The Journal of Neuroscience, vol. 45, no. 3, pp. 1–10, 2025. @article{Heeman2025, Eye movements in daily life occur in rapid succession and often without a predefined goal. Using a free viewing task, we examined how fixation duration prior to a saccade correlates to visual saliency and neuronal activity in the superior colliculus (SC) at the saccade goal. Rhesus monkeys (three male) watched videos of natural, dynamic, scenes while eye movements were tracked and, simultaneously, neurons were recorded in the superficial and intermediate layers of the superior colliculus (SCs and SCi, respectively), a midbrain structure closely associated with gaze, attention, and saliency coding. Saccades that were directed into the neuron's receptive field (RF) were extrapolated from the data. To interpret the complex visual input, saliency at the RF location was computed during the pre-saccadic fixation period using a computational saliency model. We analyzed if visual saliency and neural activity at the saccade goal predicted pre-saccadic fixation duration. We report three major findings: (1) Saliency at the saccade goal inversely correlated with fixation duration, with motion and edge information being the strongest predictors. (2) SC visual saliency responses in both SCs and SCi were inversely related to fixation duration. (3) SCs neurons, and not SCi neurons, showed higher activation for two consecutive short fixations, suggestive of concurrent saccade processing during free viewing. These results reveal a close correspondence between visual saliency, SC processing, and the timing of saccade initiation during free viewing and are discussed in relation to their implication for understanding saccade initiation during real-world gaze behavior. |
2024 |
Max Arwed Crayen; Igor Kagan; Moein Esghaei; Dirk Hoehl; Uwe Thomas; Robert Prückl; Stefan Schaffelhofer; Stefan Treue Using camera-guided electrode microdrive navigation for precise 3D targeting of macaque brain sites Journal Article In: PLoS ONE, vol. 19, no. 5, pp. 1–22, 2024. @article{Crayen2024, Spatial accuracy in electrophysiological investigations is paramount, as precise localization and reliable access to specific brain regions help the advancement of our understanding of the brain's complex neural activity. Here, we introduce a novel, multi camera-based, frameless neuronavigation technique for precise, 3-dimensional electrode positioning in awake monkeys. The investigation of neural functions in awake primates often requires stable access to the brain with thin and delicate recording electrodes. This is usually realized by implanting a chronic recording chamber onto the skull of the animal that allows direct access to the dura. Most recording and positioning techniques utilize this implanted recording chamber as a holder of the microdrive or to hold a grid. This in turn reduces the degrees of freedom in positioning. To solve this problem, we require innovative, flexible, but precise tools for neuronal recordings. We instead mount the electrode microdrive above the animal on an arch, equipped with a series of translational and rotational micromanipulators, allowing movements in all axes. Here, the positioning is controlled by infrared cameras tracking the location of the microdrive and the monkey, allowing precise and flexible trajectories. To verify the accuracy of this technique, we created iron deposits in the tissue that could be detected by MRI. Our results demonstrate a remarkable precision with the confirmed physical location of these deposits averaging less than 0.5 mm from their planned position. Pilot electrophysiological recordings additionally demonstrate the accuracy and flexibility of this method. Our innovative approach could significantly enhance the accuracy and flexibility of neural recordings, potentially catalyzing further advancements in neuroscientific research. |
Sofie De Schrijver; Thomas Decramer; Peter Janssen Simple visual stimuli are sufficient to drive responses in action observation and execution neurons in macaque ventral premotor cortex Journal Article In: PLoS Biology, vol. 22, pp. 1–21, 2024. @article{DeSchrijver2024, Neurons responding during action execution and action observation were discovered in the ventral premotor cortex 3 decades ago. However, the visual features that drive the responses of action observation/execution neurons (AOENs) have not been revealed at present. We investigated the neural responses of AOENs in ventral premotor area F5c of 4 macaques during the observation of action videos and crucial control stimuli. The large majority of AOENs showed highly phasic responses during the action videos, with a preference for the moment that the hand made contact with the object. They also responded to an abstract shape moving towards but not interacting with an object, even when the shape moved on a scrambled background, implying that most AOENs in F5c do not require the perception of causality or a meaningful action. Additionally, the majority of AOENs responded to static frames of the videos. Our findings show that very elementary stimuli, even without a grasping context, are sufficient to drive responses in F5c AOENs. |
Siqi Fan; Olga Dal Monte; Amrita R. Nair; Nicholas A. Fagan; Steve W. C. Chang Closed-loop microstimulations of the orbitofrontal cortex during real-life gaze interaction enhance dynamic social attention Journal Article In: Neuron, vol. 112, no. 15, pp. 2631–2644, 2024. @article{Fan2024, Neurons from multiple prefrontal areas encode several key variables of social gaze interaction. To explore the causal roles of the primate prefrontal cortex in real-life gaze interaction, we applied weak closed-loop microstimulations that were precisely triggered by specific social gaze events. Microstimulations of the orbitofrontal cortex, but not the dorsomedial prefrontal cortex or the anterior cingulate cortex, enhanced momentary dynamic social attention in the spatial dimension by decreasing the distance of fixations relative to a partner's eyes and in the temporal dimension by reducing the inter-looking interval and the latency to reciprocate the other's directed gaze. By contrast, on a longer timescale, microstimulations of the dorsomedial prefrontal cortex modulated inter-individual gaze dynamics relative to one's own gaze positions. These findings demonstrate that multiple regions in the primate prefrontal cortex may serve as functionally accessible nodes in controlling different aspects of dynamic social attention and suggest their potential for a therapeutic brain interface. |
Mathilda Froesel; Maëva Gacoin; Simon Clavagnier; Marc Hauser; Quentin Goudard; Suliann Ben Hamed In: European Journal of Neuroscience, vol. 59, no. 12, pp. 3203–3223, 2024. @article{Froesel2024, Social communication draws on several cognitive functions such as perception, emotion recognition and attention. The association of audio-visual information is essential to the processing of species-specific communication signals. In this study, we use functional magnetic resonance imaging in order to identify the subcortical areas involved in the cross-modal association of visual and auditory information based on their common social meaning. We identified three subcortical regions involved in audio-visual processing of species-specific communicative signals: the dorsolateral amygdala, the claustrum and the pulvinar. These regions responded to visual, auditory congruent and audio-visual stimulations. However, none of them was significantly activated when the auditory stimuli were semantically incongruent with the visual context, thus showing an influence of visual context on auditory processing. For example, positive vocalization (coos) activated the three subcortical regions when presented in the context of positive facial expression (lipsmacks) but not when presented in the context of negative facial expression (aggressive faces). In addition, the medial pulvinar and the amygdala presented multisensory integration such that audiovisual stimuli resulted in activations that were significantly higher than those observed for the highest unimodal response. Last, the pulvinar responded in a task-dependent manner, along a specific spatial sensory gradient. We propose that the dorsolateral amygdala, the claustrum and the pulvinar belong to a multisensory network that modulates the perception of visual socioemotional information and vocalizations as a function of the relevance of the stimuli in the social context. Significance statement: Understanding and correctly associating socioemotional information across sensory modalities, such that happy faces predict laughter and escape scenes predict screams, is essential when living in complex social groups. With the use of functional magnetic imaging in the awake macaque, we identify three subcortical structures—dorsolateral amygdala, claustrum and pulvinar—that only respond to auditory information that matches the ongoing visual socioemotional context, such as hearing positively valenced coo calls and seeing positively valenced mutual grooming monkeys. We additionally describe task-dependent activations in the pulvinar, organizing along a specific spatial sensory gradient, supporting its role as a network regulator. |
Supriya Ghosh; John H. R. Maunsell Locus coeruleus norepinephrine contributes to visual-spatial attention by selectively enhancing perceptual sensitivity Journal Article In: Neuron, vol. 112, no. 13, pp. 2231–2240, 2024. @article{Ghosh2024, Selectively focusing on a behaviorally relevant stimulus while ignoring irrelevant stimuli improves perception. Enhanced neuronal response gain is thought to support attention-related improvements in detection and discrimination. However, understanding of the neuronal pathways regulating perceptual sensitivity remains limited. Here, we report that responses of norepinephrine (NE) neurons in the locus coeruleus (LC) of non-human primates to behaviorally relevant sensory stimuli promote visual discrimination in a spatially selective way. LC-NE neurons spike in response to a visual stimulus appearing in the contralateral hemifield only when that stimulus is attended. This spiking is associated with enhanced behavioral sensitivity, is independent of motor control, and is absent on error trials. Furthermore, optogenetically activating LC-NE neurons selectively improves monkeys' contralateral stimulus detection without affecting motor criteria, supporting NE's causal role in granular cognitive control of selective attention at a cellular level, beyond its known diffuse and non-selective functions. |
Camille Giacometti; Delphine Autran-Clavagnier; Audrey Dureux; Laura Viñales; Franck Lamberton; Emmanuel Procyk; Charles R. E. Wilson; Céline Amiez; Fadila Hadj-Bouziane Differential functional organization of amygdala-medial prefrontal cortex networks in macaque and human Journal Article In: Communications Biology, vol. 7, pp. 1–10, 2024. @article{Giacometti2024, Over the course of evolution, the amygdala (AMG) and medial frontal cortex (mPFC) network, involved in behavioral adaptation, underwent structural changes in the old-world monkey and human lineages. Yet, whether and how the functional organization of this network differs remains poorly understood. Using resting-state functional magnetic resonance imagery, we show that the functional connectivity (FC) between AMG nuclei and mPFC regions differs between humans and awake macaques. In humans, the AMG-mPFC FC displays U-shaped pattern along the corpus callosum: a positive FC with the ventromedial prefrontal (vmPFC) and anterior cingulate cortex (ACC), a negative FC with the anterior mid-cingulate cortex (MCC), and a positive FC with the posterior MCC. Conversely, in macaques, the negative FC shifted more ventrally at the junction between the vmPFC and the ACC. The functional organization divergence of AMG-mPFC network between humans and macaques might help understanding behavioral adaptation abilities differences in their respective socio-ecological niches. |
Vishwa Goudar; Jeong-Woo Kim; Yue Liu; Adam J. O. Dede; Michael J. Jutras; Ivan Skelin; Michael Ruvalcaba; William Chang; Bhargavi Ram; Adrienne L. Fairhall; Jack J. Lin; Robert T. Knight; Elizabeth A. Buffalo; Xiao-Jing Wang A comparison of rapid rule-learning strategies in humans and monkeys Journal Article In: Journal of Neuroscience, vol. 44, no. 28, pp. 1–17, 2024. @article{Goudar2024, Interspecies comparisons are key to deriving an understanding of the behavioral and neural correlates of human cognition from animal models. We perform a detailed comparison of the strategies of female macaque monkeys to male and female humans on a variant of the Wisconsin Card Sorting Test (WCST), a widely studied and applied task that provides a multiattribute measure of cognitive function and depends on the frontal lobe. WCST performance requires the inference of a rule change given ambiguous feedback. We found that well-trained monkeys infer new rules three times more slowly than minimally instructed humans. Input-dependent hidden Markov model–generalized linear models were fit to their choices, revealing hidden states akin to feature-based attention in both species. Decision processes resembled a win–stay, lose–shift strategy with interspecies similarities as well as key differences. Monkeys and humans both test multiple rule hypotheses over a series of rule-search trials and perform inference-like computations to exclude candidate choice options. We quantitatively show that perseveration, random exploration, and poor sensitivity to negative feedback account for the slower task-switching performance in monkeys. |
Seyed A. Hassani; Paul Tiesinga; Thilo Womelsdorf In: Nature Communications, vol. 15, no. 1, pp. 1–15, 2024. @article{Hassani2024, The noradrenergic system is believed to support behavioral flexibility. A possible source mediating improved flexibility are α2A adrenoceptors (α2AR) in prefrontal cortex (PFC) or the anterior cingulate cortex (ACC). We tested this hypothesis by stimulating α2ARs using Guanfacine during attentional set shifting in male nonhuman primates. We found that α2AR stimulation improved learning from errors and updating attention sets. Neural recordings in the ACC, dorsolateral PFC, and the striatum showed that α2AR stimulation selectively enhanced neural signaling of prediction errors in neurons of the ACC and the striatum, but not in dlPFC. This modulation was accompanied by enhanced encoding of attended target features and particularly apparent in putative fast-spiking interneurons, pointing to an interneuron mediated mechanism of α2AR action. These results reveal that α2A receptors are part of the causal chain of flexibly updating attention sets through an enhancement of outcomes and prediction error signaling in ACC and striatum. |
Janina Hüer; Pankhuri Saxena; Stefan Treue Pathwa-selective optogenetics reveals the functional anatomy of top-down attentional modulation in the macaque visual cortex Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 3, pp. 1–9, 2024. @article{Hueer2024, Spatial attention represents a powerful top–down influence on sensory responses in primate visual cortical areas. The frontal eye field (FEF) has emerged as a key candidate area for the source of this modulation. However, it is unclear whether the FEF exerts its effects via its direct axonal projections to visual areas or indirectly through other brain areas and whether the FEF affects both the enhancement of attended and the suppression of unattended sensory responses. We used pathway-selective optogenetics in rhesus macaques performing a spatial attention task to inhibit the direct input from the FEF to area MT, an area along the dorsal visual pathway specialized for the processing of visual motion information. Our results show that the optogenetic inhibition of the FEF input specifically reduces attentional modulation in MT by about a third without affecting the neurons' sensory response component. We find that the direct FEF-to-MT pathway contributes to both the enhanced processing of target stimuli and the suppression of distractors. The FEF, thus, selectively modulates firing rates in visual area MT, and it does so via its direct axonal projections. |
Janina Hüer; Pankhuri Saxena; Stefan Treuea Pathway-selective optogenetics reveals the functional anatomy of top–down attentional modulation in the macaque visual cortex Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 3, pp. 1–9, 2024. @article{Hueer2024a, Spatial attention represents a powerful top–down influence on sensory responses in primate visual cortical areas. The frontal eye field (FEF) has emerged as a key candidate area for the source of this modulation. However, it is unclear whether the FEF exerts its effects via its direct axonal projections to visual areas or indirectly through other brain areas and whether the FEF affects both the enhancement of attended and the suppression of unattended sensory responses. We used pathway- selective optogenetics in rhesus macaques performing a spatial attention task to inhibit the direct input from the FEF to area MT, an area along the dorsal visual pathway specialized for the processing of visual motion information. Our results show that the optogenetic inhibition of the FEF input specifically reduces attentional modulation in MT by about a third without affecting the neurons' sensory response component. We find that the direct FEF- to- MT pathway contributes to both the enhanced processing of target stimuli and the suppression of distractors. The FEF, thus, selectively modulates firing rates in visual area MT, and it does so via its direct axonal projections. |
Matteo Alleman; Matthew Panichello; Timothy J. Buschman; W. Jeffrey Johnston The neural basis of swap errors in working memory Journal Article In: Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 33, pp. 1–11, 2024. @article{Alleman2024, When making decisions in a cluttered world, humans and other animals often have to hold multiple items in memory at once—such as the different items on a shopping list. Psychophysical experiments in humans and other animals have shown remembered stimuli can sometimes become confused, with participants reporting chimeric stimuli composed of features from different stimuli. In particular, subjects will often make “swap errors” where they misattribute a feature from one object as belonging to another object. While swap errors have been described behaviorally and theoretical explanations have been proposed, their neural mechanisms are unknown. Here, we elucidate these neural mechanisms by analyzing neural population recordings from monkeys performing two multistimulus working memory tasks. In these tasks, monkeys were cued to report the color of an item that either was previously shown at a corresponding location or will be shown at the corresponding location. Animals made swap errors in both tasks. In the neural data, we find evidence that the neural correlates of swap errors emerged when correctly remembered information is selected from working memory. This led to a representation of the distractor color as if it were the target color, underlying the eventual swap error. We did not find consistent evidence that swap errors arose from misinterpretation of the cue or errors during encoding or storage in working memory. These results provide evidence that swap errors emerge during selection of correctly remembered information from working memory, and highlight this selection as a crucial—yet surprisingly brittle—neural process. |
Satoko Amemori; Ann M. Graybiel; Ken-ichi Amemori Cingulate microstimulation induces negative decision-making via reduced top-down influence on primate fronto-cingulo-striatal network Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–17, 2024. @article{Amemori2024, The dorsolateral prefrontal cortex (dlPFC) is crucial for regulation of emotion that is known to aid prevention of depression. The broader fronto-cingulo-striatal (FCS) network, including cognitive dlPFC and limbic cingulo-striatal regions, has been associated with a negative evaluation bias often seen in depression. The mechanism by which dlPFC regulates the limbic system remains largely unclear. Here we have successfully induced a negative bias in decision-making in female primates performing a conflict decision-making task, by directly microstimulating the subgenual cingulate cortex while simultaneously recording FCS local field potentials (LFPs). The artificially induced negative bias in decision-making was associated with a significant decrease in functional connectivity from cognitive to limbic FCS regions, represented by a reduction in Granger causality in beta-range LFPs from the dlPFC to the other regions. The loss of top-down directional influence from cognitive to limbic regions, we suggest, could underlie negative biases in decision-making as observed in depressive states. |
Wajd Amly; Chih-Yang Chen; Tadashi Isa Modeling saccade reaction time in marmosets: The contribution of earlier visual response and variable inhibition Journal Article In: Frontiers in Systems Neuroscience, vol. 18, pp. 1–12, 2024. @article{Amly2024, Marmosets are expected to serve as a valuable model for studying the primate visuomotor system due to their similar oculomotor behaviors to humans and macaques. Despite these similarities, differences exist; challenges in training marmosets on tasks requiring suppression of unwanted saccades, having consistently shorter, yet more variable saccade reaction times (SRT) compared to humans and macaques. This study investigates whether the short and variable SRT in marmosets is related to differences in visual signal transduction and variability in inhibitory control. We refined a computational SRT model, adjusting parameters to better capture the marmoset SRT distribution in a gap saccade task. Our findings indicate that visual information processing is faster in marmosets, and that saccadic inhibition is more variable compared to other species. |
Shashank A. Anand; Fatih Sogukpinar; Ilya E. Monosov Arousal effects on oscillatory dynamics in the non-human primate brain Journal Article In: Cerebral Cortex, vol. 34, no. 12, pp. 1–13, 2024. @article{Anand2024, Arousal states are thought to influence many aspects of cognition and behavior by broadly modulating neural activity. Many studies have observed arousal-related modulations of alpha (~8 to 15 Hz) and gamma (~30 to 50 Hz) power and coherence in local field potentials across relatively small groups of brain regions. However, the global pattern of arousal-related oscillatory modulation in local field potentials is yet to be fully elucidated. We simultaneously recorded local field potentials in numerous cortical and subcortical regions in the primate brain and assessed oscillatory activity and inter-regional coherence associated with arousal state. In high arousal states, we found a uniquely strong and coherent gamma oscillation between the amygdala and basal forebrain. In low arousal rest-like states, a relative increase in coherence at alpha frequencies was present across sampled brain regions, with the notable exception of the medial temporal lobe. We consider how these patterns of activity may index arousal-related brain states that support the processing of incoming sensory stimuli during high arousal states and memory-related functions during rest. |
Reza Azadi; Emily Lopez; Jessica Taubert; Amanda Patterson; Arash Afraz Inactivation of face-selective neurons alters eye movements when free viewing faces Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 3, pp. 1–10, 2024. @article{Azadi2024a, During free viewing, faces attract gaze and induce specific fixation patterns corresponding to the facial features. This suggests that neurons encoding the facial features are in the causal chain that steers the eyes. However, there is no physiological evidence to support a mechanistic link between face- encoding neurons in high- level visual areas and the oculo- motor system. In this study, we targeted the middle face patches of the inferior temporal (IT) cortex in two macaque monkeys using an functional magnetic resonance imaging (fMRI) localizer. We then utilized muscimol microinjection to unilaterally suppress IT neural activity inside and outside the face patches and recorded eye movements while the animals free viewing natural scenes. Inactivation of the face- selective neurons altered the pattern of eye movements on faces: The monkeys found faces in the scene but neglected the eye contralateral to the inactivation hemisphere. These findings reveal the causal contribution of the high- level visual cortex in eye movements. |
Alexandra Busch; Megan Roussy; Rogelio Luna; Matthew L. Leavitt; Maryam H. Mofrad; Roberto A. Gulli; Benjamin Corrigan; Ján Mináč; Adam J. Sachs; Lena Palaniyappan; Lyle Muller; Julio C. Martinez-Trujillo Neuronal activation sequences in lateral prefrontal cortex encode visuospatial working memory during virtual navigation Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–15, 2024. @article{Busch2024, Working memory (WM) is the ability to maintain and manipulate information ‘in mind'. The neural codes underlying WM have been a matter of debate. We simultaneously recorded the activity of hundreds of neurons in the lateral prefrontal cortex of male macaque monkeys during a visuospatial WM task that required navigation in a virtual 3D environment. Here, we demonstrate distinct neuronal activation sequences (NASs) that encode remembered target locations in the virtual environment. This NAS code outperformed the persistent firing code for remembered locations during the virtual reality task, but not during a classical WM task using stationary stimuli and constraining eye movements. Finally, blocking NMDA receptors using low doses of ketamine deteriorated the NAS code and behavioral performance selectively during the WM task. These results reveal the versatility and adaptability of neural codes supporting working memory function in the primate lateral prefrontal cortex. |
Nancy D Carney; Aarit Ahuja; Nadira Yusif Rodriguez; Alekh Karkada Ashok; Thomas Serre; Theresa Desrochers; David Sheinberg Monkeys engage in visual simulation to solve complex problems Journal Article In: Current Biology, vol. 34, pp. 5635–5645, 2024. @article{Carney2024, Visual simulation — i.e., using internal reconstructions of the world to experience potential future versions of events that are not currently happening — is among the most sophisticated capacities of the human mind. But is this ability in fact uniquely human? To answer this question, we tested monkeys on a series of experiments involving the ‘Planko' game, which we have previously used to evoke visual simulation in human participants. We found that monkeys were able to successfully play the game using a simulation strategy, predicting the trajectory of a ball through a field of planks while demonstrating a level of accuracy and behavioral signatures comparable to humans. Computational analyses further revealed that the monkeys' strategy while playing Planko aligned with a recurrent neural network (RNN) that approached the task using a spontaneously learned simulation strategy. Finally, we carried out awake functional magnetic resonance imaging while monkeys played Planko. We found activity in motion-sensitive regions of the monkey brain during hypothesized simulation periods, even without any perceived visual motion cues. This neural result closely mirrors previous findings from human research, suggesting a shared mechanism of visual simulation across species. In all, these findings challenge traditional views of animal cognition, proposing that nonhuman primates possess a complex cognitive landscape, capable of invoking imaginative and predictive mental experiences to solve complex everyday problems. |
Adithya Narayan Chandrasekaran; Ayesha Vermani; Priyanka Gupta; Nicholas Steinmetz; Tirin Moore; Devarajan Sridharan Dissociable components of attention exhibit distinct neuronal signatures in primate visual cortex Journal Article In: Science Advances, vol. 10, no. 5, pp. 1–15, 2024. @article{Chandrasekaran2024, Attention can be deployed in multiple forms and facilitates behavior by influencing perceptual sensitivity and choice bias. Attention is also associated with a myriad of changes in sensory neural activity. Yet, the relationship between the behavioral components of attention and the accompanying changes in neural activity remains largely unresolved. We examined this relationship by quantifying sensitivity and bias in monkeys performing a task that dissociated eye movement responses from the focus of covert attention. Unexpectedly, bias, not sensitivity, increased at the focus of covert attention, whereas sensitivity increased at the location of planned eye movements. Furthermore, neuronal activity within visual area V4 varied robustly with bias, but not sensitivity, at the focus of covert attention. In contrast, correlated variability between neuronal pairs was lowest at the location of planned eye movements, and varied with sensitivity, but not bias. Thus, dissociable behavioral components of attention exhibit distinct neuronal signatures within the visual cortex. |
Julie A. Charlton; Robbe L. T. Goris Abstract deliberation by visuomotor neurons in prefrontal cortex Journal Article In: Nature Neuroscience, vol. 27, no. 6, pp. 1167–1175, 2024. @article{Charlton2024, During visually guided behavior, the prefrontal cortex plays a pivotal role in mapping sensory inputs onto appropriate motor plans. When the sensory input is ambiguous, this involves deliberation. It is not known whether the deliberation is implemented as a competition between possible stimulus interpretations or between possible motor plans. Here we study neural population activity in the prefrontal cortex of macaque monkeys trained to flexibly report perceptual judgments of ambiguous visual stimuli. We find that the population activity initially represents the formation of a perceptual choice before transitioning into the representation of the motor plan. Stimulus strength and prior expectations both bear on the formation of the perceptual choice, but not on the formation of the action plan. These results suggest that prefrontal circuits involved in action selection are also used for the deliberation of abstract propositions divorced from a specific motor plan, thus providing a crucial mechanism for abstract reasoning. |
Jingwen Chen; Cong Zhang; Peiyao Hu; Bin Min; Liping Wang Flexible control of sequence working memory in the macaque frontal cortex Journal Article In: Neuron, vol. 112, no. 20, pp. 3502–3514, 2024. @article{Chen2024a, To memorize a sequence, one must serially bind each item to its rank order. How the brain controls a given input to bind its associated order in sequence working memory (SWM) remains unexplored. Here, we investigated the neural representations underlying SWM control using electrophysiological recordings in the frontal cortex of macaque monkeys performing forward and backward SWM tasks. Separate and generalizable low-dimensional subspaces for sensory and memory information were found within the same frontal circuitry, and SWM control was reflected in these neural subspaces' organized dynamics. Each item at each rank was sequentially entered into a common sensory subspace and, depending on forward or backward task requirement, flexibly and timely sent into rank-selective SWM subspaces. Neural activity in these SWM subspaces faithfully predicted the recalled item and order information in single error trials. Thus, compositional neural population codes with well-orchestrated dynamics in frontal cortex support the flexible control of SWM. |
Spencer Chin Yu Chen; Yuzhi Chen; Wilson S. Geisler; Eyal Seidemann Neural correlates of perceptual similarity masking in primate V1 Journal Article In: eLife, vol. 12, pp. 1–25, 2024. @article{Chen2024h, Visual detection is a fundamental natural task. Detection becomes more challenging as the similarity between the target and the background in which it is embedded increases, a phenomenon termed ‘similarity masking'. To test the hypothesis that V1 contributes to similarity masking, we used voltage sensitive dye imaging (VSDI) to measure V1 population responses while macaque monkeys performed a detection task under varying levels of target-background similarity. Paradoxically, we find that during an initial transient phase, V1 responses to the target are enhanced, rather than suppressed, by target-background similarity. This effect reverses in the second phase of the response, so that in this phase V1 signals are positively correlated with the behavioral effect of similarity. Finally, we show that a simple model with delayed divisive normalization can qualitatively account for our findings. Overall, our results support the hypothesis that a nonlinear gain control mechanism in V1 contributes to perceptual similarity masking. |
Christopher Conroy; Rakesh Nanjappa; Robert M. McPeek Inhibitory tagging both speeds and strengthens saccade target selection in the superior colliculus during visual search Journal Article In: Journal of Neurophysiology, vol. 131, no. 3, pp. 548–555, 2024. @article{Conroy2024, It has been suggested that, during difficult visual search tasks involving time pressure and multiple saccades, inhibitory tagging helps to facilitate efficient saccade target selection by reducing responses to objects in the scene once they have been searched and rejected. The superior colliculus (SC) is a midbrain structure involved in target selection, and recent findings suggest an influence of inhibitory tagging on SC activity. Precisely how, and by how much, inhibitory tagging influences target selection by SC neurons, however, is unclear. The purpose of this study, therefore, was to characterize and quantify the influence of inhibitory tagging on target selection in the SC. Rhesus monkeys performed a visual search task involving time pressure and multiple saccades. Early in the fixation period between saccades in the context of this task, a subset of SC neurons reliably discriminated the stimulus selected as the next saccade goal, consistent with a role in target selection. Discrimination occurred earlier and was more robust, however, when unselected stimuli in the search array had been previously fixated on the same trial. This indicates that inhibitory tagging both speeds and strengthens saccade target selection in the SC during multisaccade search. The results provide constraints on models of target selection based on SC activity. |
Shanna H. Coop; Jacob L. Yates; Jude F. Mitchell Pre-saccadic neural enhancements in marmoset area MT Journal Article In: The Journal of Neuroscience, vol. 44, no. 4, pp. 1–16, 2024. @article{Coop2024, Each time we make an eye movement, attention moves before the eyes, resulting in a perceptual enhancement at the target. Recent psychophysical studies suggest that this pre-saccadic attention enhances the visual features at the saccade target, whereas covert attention causes only spatially selective enhancements. While previous nonhuman primate studies have found that pre-saccadic attention does enhance neural responses spatially, no studies have tested whether changes in neural tuning reflect an automatic feature enhancement. Here we examined pre-saccadic attention using a saccade foraging task developed for marmoset monkeys (one male and one female). We recorded from neurons in the middle temporal area with peripheral receptive fields that contained a motion stimulus, which would either be the target of a saccade or a distracter as a saccade was made to another location. We established that marmosets, like macaques, show enhanced pre-saccadic neural responses for saccades toward the receptive field, including increases in firing rate and motion information. We then examined if the specific changes in neural tuning might support feature enhancements for the target. Neurons exhibited diverse changes in tuning but predominantly showed additive and multiplicative increases that were uniformly applied across motion directions. These findings confirm that marmoset monkeys, like macaques, exhibit pre-saccadic neural enhancements during saccade foraging tasks with minimal training requirements. However, at the level of individual neurons, the lack of feature-tuned enhancements is similar to neural effects reported during covert spatial attention. |
Pedro G. Vieira; Matthew R. Krause; Christopher C. Pack Temporal interference stimulation disrupts spike timing in the primate brain Journal Article In: Nature Communications, vol. 15, no. 1, pp. 11–17, 2024. @article{Vieira2024a, Electrical stimulation can regulate brain activity, producing clear clinical benefits, but focal and effective neuromodulation often requires surgically implanted electrodes. Recent studies argue that temporal interference (TI) stimulation may provide similar outcomes non-invasively. During TI, scalp electrodes generate multiple electrical fields in the brain, modulating neural activity only at their intersection. Despite considerable enthusiasm for this approach, little empirical evidence demonstrates its effectiveness, especially under conditions suitable for human use. Here, using single-neuron recordings in non-human primates, we establish that TI reliably alters the timing, but not the rate, of spiking activity. However, we show that TI requires strategies—high carrier frequencies, multiple electrodes, and amplitude-modulated waveforms—that also limit its effectiveness. Combined, these factors make TI 80 % weaker than other forms of non-invasive brain stimulation. Although unlikely to cause widespread neuronal entrainment, TI may be ideal for disrupting pathological oscillatory activity, a hallmark of many neurological disorders. |
Lei Wang; Xufeng Zhou; Jie Yang; Fu Zeng; Shuzhen Zuo; Makoto Kusunoki; Huimin Wang; Yong-di Zhou; Aihua Chen; Sze Chai Kwok Mixed coding of content-temporal detail by dorsomedial posterior parietal neurons Journal Article In: Journal of Neuroscience, vol. 44, no. 3, pp. 1–16, 2024. @article{Wang2024, The dorsomedial posterior parietal cortex (dmPPC) is part of a higher-cognition network implicated in elaborate processes under- pinning memory formation, recollection, episode reconstruction, and temporal information processing. Neural coding for complex episodic processing is however under-documented. Here, we recorded extracellular neural activities from three male rhesus macaques (Macaca mulatta) and revealed a set of neural codes of “neuroethogram” in the primate parietal cortex. Analyzing neural responses in macaque dmPPC to naturalistic videos, we discovered several groups of neurons that are sensitive to different categories of ethogram items, low-level sensory features, and saccadic eye movement. We also discovered that the processing of category and feature information by these neurons is sustained by the accumulation of temporal information over a long timescale of up to 30 s, corroborating its reported long temporal receptive windows. We performed an additional behavioral experiment with additional two male rhesus macaques and found that saccade-related activities could not account for the mixed neuronal responses elicited by the video stimuli. We further observed monkeys' scan paths and gaze consistency are modulated by video content. Taken altogether, these neural findings explain how dmPPC weaves fabrics of ongoing experiences together in real time. The high dimensionality of neural representations should motivate us to shift the focus of attention from pure selectivity neurons to mixed selectivity neurons, especially in increasingly complex naturalistic task designs. |
Raymond Ka Wong; Janahan Selvanayagam; Kevin Johnston; Stefan Everling Functional specialization and distributed processing across marmoset lateral prefrontal subregions Journal Article In: Cerebral Cortex, vol. 34, no. 10, pp. 1–15, 2024. @article{Wong2024, A prominent aspect of primate lateral prefrontal cortex organization is its division into several cytoarchitecturally distinct subregions. Neurophysiological investigations in macaques have provided evidence for the functional specialization of these subregions, but an understanding of the relative representational topography of sensory, social, and cognitive processes within them remains elusive. One explanatory factor is that evidence for functional specialization has been compiled largely from a patchwork of findings across studies, in many animals, and with considerable variation in stimulus sets and tasks. Here, we addressed this by leveraging the common marmoset (Callithrix jacchus) to carry out large-scale neurophysiological mapping of the lateral prefrontal cortex using high-density microelectrode arrays, and a diverse suite of test stimuli including faces, marmoset calls, and spatial working memory task. Task-modulated units and units responsive to visual and auditory stimuli were distributed throughout the lateral prefrontal cortex, while those with saccade-related activity or face-selective responses were restricted to 8aV, 8aD, 10, 46 V, and 47. Neurons with contralateral visual receptive fields were limited to areas 8aV and 8aD. These data reveal a mixed pattern of functional specialization in the lateral prefrontal cortex, in which responses to some stimuli and tasks are distributed broadly across lateral prefrontal cortex subregions, while others are more limited in their representation. |
Jimin Wu; Yuzhi Chen; Ashok Veeraraghavan; Eyal Seidemann; Jacob T. Robinson Mesoscopic calcium imaging in a head-unrestrained male non-human primate using a lensless microscope Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–14, 2024. @article{Wu2024b, Mesoscopic calcium imaging enables studies of cell-type specific neural activity over large areas. A growing body of literature suggests that neural activity can be different when animals are free to move compared to when they are restrained. Unfortunately, existing systems for imaging calcium dynamics over large areas in non-human primates (NHPs) are table-top devices that require restraint of the animal's head. Here, we demonstrate an imaging device capable of imaging mesoscale calcium activity in a head-unrestrained male non-human primate. We successfully miniaturize our system by replacing lenses with an optical mask and computational algorithms. The resulting lensless microscope can fit comfortably on an NHP, allowing its head to move freely while imaging. We are able to measure orientation columns maps over a 20 mm2 field-of-view in a head-unrestrained macaque. Our work establishes mesoscopic imaging using a lensless microscope as a powerful approach for studying neural activity under more naturalistic conditions. |
Will Xiao; Saloni Sharma; Gabriel Kreiman; Margaret S. Livingstone Feature-selective responses in macaque visual cortex follow eye movements during natural vision Journal Article In: Nature Neuroscience, vol. 27, no. 6, pp. 1157–1166, 2024. @article{Xiao2024a, In natural vision, primates actively move their eyes several times per second via saccades. It remains unclear whether, during this active looking, visual neurons exhibit classical retinotopic properties, anticipate gaze shifts or mirror the stable quality of perception, especially in complex natural scenes. Here, we let 13 monkeys freely view thousands of natural images across 4.6 million fixations, recorded 883 h of neuronal responses in six areas spanning primary visual to anterior inferior temporal cortex and analyzed spatial, temporal and featural selectivity in these responses. Face neurons tracked their receptive field contents, indicated by category-selective responses. Self-consistency analysis showed that general feature-selective responses also followed eye movements and remained gaze-dependent over seconds of viewing the same image. Computational models of feature-selective responses located retinotopic receptive fields during free viewing. We found limited evidence for feature-selective predictive remapping and no viewing-history integration. Thus, ventral visual neurons represent the world in a predominantly eye-centered reference frame during natural vision. |
Ruyi Yang; Peng Zhao; Liyang Wang; Chenli Feng; Chen Peng; Zhexuan Wang; Yingying Zhang; Minqian Shen; Kaiwen Shi; Shijun Weng; Chunqiong Dong; Fu Zeng; Tianyun Zhang; Xingdong Chen; Shuiyuan Wang; Yiheng Wang; Yuanyuan Luo; Qingyuan Chen; Yuqing Chen; Chunhui Chengyong Jiang; Shanshan Jia; Zhaofei Yu; Jian Liu; Fei Wang; Su Jiang; Wendong Xu; Liang Li; Gang Wang; Xiaofen Mo; Gengfeng Zheng; Aihua Chen; Xingtao Zhou; Chunhui Chengyong Jiang; Yuanzhi Yuan; Biao Yan; Jiayi Zhang Assessment of visual function in blind mice and monkeys with subretinally implanted nanowire arrays as artificial photoreceptors Journal Article In: Nature Biomedical Engineering, vol. 8, no. 8, pp. 1018–1039, 2024. @article{Yang2024e, Retinal prostheses could restore image-forming vision in conditions of photoreceptor degeneration. However, contrast sensitivity and visual acuity are often insufficient. Here we report the performance, in mice and monkeys with induced photoreceptor degeneration, of subretinally implanted gold-nanoparticle-coated titania nanowire arrays providing a spatial resolution of 77.5 μm and a temporal resolution of 3.92 Hz in ex vivo retinas (as determined by patch-clamp recording of retinal ganglion cells). In blind mice, the arrays allowed for the detection of drifting gratings and flashing objects at light-intensity thresholds of 15.70–18.09 μW mm–2, and offered visual acuities of 0.3–0.4 cycles per degree, as determined by recordings of visually evoked potentials and optomotor-response tests. In monkeys, the arrays were stable for 54 weeks, allowed for the detection of a 10-μW mm–2 beam of light (0.5° in beam angle) in visually guided saccade experiments, and induced plastic changes in the primary visual cortex, as indicated by long-term in vivo calcium imaging. Nanomaterials as artificial photoreceptors may ameliorate visual deficits in patients with photoreceptor degeneration. |
Yang Yiling; Johanna Klon-Lipok; Wolf Singer Joint encoding of stimulus and decision in monkey primary visual cortex Journal Article In: Cerebral Cortex, vol. 34, no. 1, pp. 1–6, 2024. @article{Yiling2024a, We investigated whether neurons in monkey primary visual cortex (V1) exhibit mixed selectivity for sensory input and behavioral choice. Parallel multisite spiking activity was recorded from area V1 of awake monkeys performing a delayed match-to-sample task. The monkeys had to make a forced choice decision of whether the test stimulus matched the preceding sample stimulus. The population responses evoked by the test stimulus contained information about both the identity of the stimulus and with some delay but before the onset of the motor response the forthcoming choice. The results of subspace identification analysis indicate that stimulus-specific and decision-related information coexists in separate subspaces of the high-dimensional population activity, and latency considerations suggest that the decision-related information is conveyed by top-down projections. |
Yang Yiling; Johanna Klon Lipok; Katharine Shapcott; Andreea Lazar; Wolf Singer Dynamic fading memory and expectancy effects in the monkey primary visual cortex Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 8, pp. 2024, 2024. @article{Yiling2024, In order to investigate the involvement of the primary visual cortex (V1) in working memory (WM), parallel, multisite recordings of multi-unit activity were obtained from monkey V1 while the animals performed a delayed match-to-sample (DMS) task. During the delay period, V1 population firing rate vectors maintained a lingering trace of the sample stimulus that could be reactivated by intervening impulse stimuli that enhanced neuronal firing. This fading trace of the sample did not require active engagement of the monkeys in the DMS task and likely reflects the intrinsic dynamics of recurrent cortical networks in lower visual areas. This renders an active, attention-dependent involvement of V1 in the maintenance of WM contents unlikely. By contrast, population responses to the test stimulus depended on the probabilistic contingencies between sample and test stimuli. Responses to tests that matched expectations were reduced which agrees with concepts of predictive coding. |
Atsushi Yoshida; Okihide Hikosaka Involvement of neurons in the nonhuman primate anterior striatum in proactive inhibition Journal Article In: The Journal of Neuroscience, vol. 44, no. 49, pp. 1–20, 2024. @article{Yoshida2024, Behaving as desired requires selecting the appropriate behavior and inhibiting the selection of inappropriate behavior. This inhibitory function involves multiple processes, such as reactive and proactive inhibition, instead of a single process. In this study, two male macaque monkeys were required to perform a task in which they had to sequentially select (accept) or refuse (reject) a choice. Neural activity was recorded from the anterior striatum, which is considered to be involved in behavioral inhibition, focusing on the distinction between proactive and reactive inhibitions. We identified neurons with significant activity changes during the rejection of bad objects. Cluster analysis revealed three distinct groups, of which only one showed increased activity during object rejection, suggesting its involvement in proactive inhibition. This activity pattern was consistent irrespective of the rejection method, indicating a role beyond saccadic suppression. Furthermore, minimal activity changes during the fixation task indicated that these neurons were not primarily involved in reactive inhibition. In conclusion, these findings suggest that the anterior striatum plays a crucial role in cognitive control and orchestrates goal-directed behavior through proactive inhibition, which may be critical in understanding the mechanisms of behavioral inhibition dysfunction that occur in patients with basal ganglia disease. |
Gongchen Yu; Leor N. Katz; Christian Quaia; Adam Messinger; Richard J. Krauzlis Short-latency preference for faces in primate superior colliculus depends on visual cortex Journal Article In: Neuron, vol. 112, no. 16, pp. 2814–2822, 2024. @article{Yu2024, Face processing is fundamental to primates and has been extensively studied in higher-order visual cortex. Here, we report that visual neurons in the midbrain superior colliculus (SC) of macaque monkeys display a preference for images of faces. This preference emerges within 40 ms of stimulus onset—well before “face patches” in visual cortex—and, at the population level, can be used to distinguish faces from other visual objects with accuracies of ∼80%. This short-latency face preference in SC depends on signals routed through early visual cortex because inactivating the lateral geniculate nucleus, the key relay from retina to cortex, virtually eliminates visual responses in SC, including face-related activity. These results reveal an unexpected circuit in the primate visual system for rapidly detecting faces in the periphery, complementing the higher-order areas needed for recognizing individual faces. |
Nadira Yusif Rodriguez; Aarit Ahuja; Debaleena Basu; Theresa H. McKim; Theresa M. Desrochers Different subregions of monkey lateral prefrontal cortex respond to abstract sequences and their components Journal Article In: The Journal of Neuroscience, vol. 44, no. 47, pp. 1–13, 2024. @article{YusifRodriguez2024, Sequential information permeates daily activities, such as when watching for the correct series of buildings to determine when to get off the bus or train. These sequences include periodicity (the spacing of the buildings), the identity of the stimuli (the kind of house), and higher-order more abstract rules that may not depend on the exact stimulus (e.g., house, house, house, business). Previously, we found that the posterior fundus of area 46 in the monkey lateral prefrontal cortex (LPFC) responds to rule changes in such abstract visual sequences. However, it is unknown if this region responds to other components of the sequence, i.e., image periodicity and identity, in isolation. Further, it is unknown if this region dissociates from other, more ventral LPFC subregions that have been associated with sequences and their components. To address these questions, we used awake functional magnetic resonance imaging in three male macaque monkeys during two no-report visual tasks. One task contained abstract visual sequences, and the other contained no visual sequences but maintained the same image periodicity and identities. We found the fundus of area 46 responded only to abstract sequence rule violations. In contrast, the ventral bank of area 46 responded to changes in image periodicity and identity, but not changes in the abstract sequence. These results suggest a functional specialization within anatomical substructures of LPFC to signal different kinds of stimulus regularities. This specialization may provide key scaffolding to identify abstract patterns and construct complex models of the world for daily living. |
Yordanka Zafirova; Anna Bognár; Rufin Vogels Configuration-sensitive face-body interactions in primate visual cortex Journal Article In: Progress in Neurobiology, vol. 232, pp. 1–16, 2024. @article{Zafirova2024, Traditionally, the neural processing of faces and bodies is studied separately, although they are encountered together, as parts of an agent. Despite its social importance, it is poorly understood how faces and bodies interact, particularly at the single-neuron level. Here, we examined the interaction between faces and bodies in the macaque inferior temporal (IT) cortex, targeting an fMRI-defined patch. We recorded responses of neurons to monkey images in which the face was in its natural location (natural face-body configuration), or in which the face was mislocated with respect to the upper body (unnatural face-body configuration). On average, the neurons did not respond stronger to the natural face-body configurations compared to the summed responses to their faces and bodies, presented in isolation. However, the neurons responded stronger to the natural compared to the unnatural face-body configurations. This configuration effect was present for face- and monkey-centered images, did not depend on local feature differences between configurations, and was present when the face was replaced by a small object. The face-body interaction rules differed between natural and unnatural configurations. In sum, we show for the first time that single IT neurons process faces and bodies in a configuration-specific manner, preferring natural face-body configurations. |
Sheng Hui Zhang; Shi Ming Tang; Cong Yu Testing Hubel and Wiesel's "ice-cube" model of functional maps at cellular resolution in macaque V1 Journal Article In: Cerebral Cortex, vol. 34, no. 12, pp. 1–11, 2024. @article{Zhang2024h, Hubel and Wiesel's ice-cube model proposed that V1 orientation and ocular dominance functional maps intersect orthogonally to optimize wiring efficiency. Here, we revisited this model and additional arrangements at both cellular and pixel levels in awake macaques using two-photon calcium imaging. The recorded response fields of view were similar in size to hypercolumns, each containing up to 2,000 identified neurons and representing full periods of orientation preferences and ocular dominance. We estimated each neuron/pixel's orientation, ocular dominance, and spatial frequency preferences, constructed respective functional maps, computed geometric gradients of feature preferences, and calculated intersection angles among these gradients. At the cellular level, the intersection angles among functional maps were nearly evenly distributed. Nonetheless, pixel-based maps after Gaussian smoothing displayed orientation-ocular dominance and orientation-spatial frequency orthogonality, as well as ocular dominance-spatial frequency parallelism, in alignment with previous results, even though the trends were weak and highly variable. However, these Gaussian smoothing effects were not observed in cellular maps, indicating that the pixel-based trends may not accurately represent the relationships among feature-tuning properties of V1 neurons. We suggest that the widely distributed intersections among cellular maps can ensure that multiple stimulus features are represented within a hypercolumn, and no pair of features is represented with the least economical wiring (e.g. parallel intersections). |
Sheng Hui Zhang; Xing Nan Zhao; Dan Qing Jiang; Shi Ming Tang; Cong Yu Ocular dominance-dependent binocular combination of monocular neuronal responses in macaque V1 Journal Article In: eLife, vol. 13, pp. 1–15, 2024. @article{Zhang2024i, Primates rely on two eyes to perceive depth, while maintaining stable vision when either one eye or both eyes are open. Although psychophysical and modeling studies have investigated how monocular signals are combined to form binocular vision, the underlying neuronal mechanisms, particularly in V1 where most neurons exhibit binocularity with varying eye preferences, remain poorly understood. Here, we used two-photon calcium imaging to compare the monocular and binocular responses of thousands of simultaneously recorded V1 superficial-layer neurons in three awake macaques. During monocular stimulation, neurons preferring the stimulated eye exhibited significantly stronger responses compared to those preferring both eyes. However, during binocular stimulation, the responses of neurons preferring either eye were suppressed on the average, while those preferring both eyes were enhanced, resulting in similar neuronal responses irrespective of their eye preferences, and an overall response level similar to that with monocular viewing. A neuronally realistic model of binocular combination, which incorporates ocular dominance-dependent divisive interocular inhibition and binocular summation, is proposed to account for these findings. |
Xing-Nan Zhao; Xing-Si Dong; Dan-Qing Jiang; Si Wu; Shi-Ming Tang; Cong Yu Population coding for figure-ground texture segregation in macaque V1 and V4 Journal Article In: Progress in Neurobiology, vol. 240, pp. 1–11, 2024. @article{Zhao2024d, Object recognition often involves the brain segregating objects from their surroundings. Neurophysiological studies of figure-ground texture segregation have yielded inconsistent results, particularly on whether V1 neurons can perform figure-ground texture segregation or just detect texture borders. To address this issue from a population perspective, we utilized two-photon calcium imaging to simultaneously record the responses of large samples of V1 and V4 neurons to figure-ground texture stimuli in awake, fixating macaques. The average response changes indicate that V1 neurons mainly detect texture borders, while V4 neurons are involved in figure-ground segregation. However, population analysis (SVM decoding of PCA-transformed neuronal responses) reveal that V1 neurons not only detect figure-ground borders, but also contribute to figure-ground texture segregation, although requiring substantially more principal components than V4 neurons to reach a 75 % decoding accuracy. Individually, V1/V4 neurons showing larger (negative/positive) figure-ground response differences contribute more to figure-ground segregation. But for V1 neurons, the contribution becomes significant only when many principal components are considered. We conclude that V1 neurons participate in figure-ground segregation primarily by defining the figure borders, and the poorly structured figure-ground information V1 neurons carry could be further utilized by V4 neurons to accomplish figure-ground segregation. |
Zikang Zhu; Byounghoon Kim; Raymond Doudlah; Ting Yu Chang; Ari Rosenberg Differential clustering of visual and choice- and saccade-related activity in macaque V3A and CIP Journal Article In: Journal of Neurophysiology, vol. 131, no. 4, pp. 709–722, 2024. @article{Zhu2024f, Neurons in sensory and motor cortices tend to aggregate in clusters with similar functional properties. Within the primate dorsal ("where") pathway, an important interface between three-dimensional (3-D) visual processing and motor-related functions consists of two hierarchically organized areas: V3A and the caudal intraparietal (CIP) area. In these areas, 3-D visual information, choice-related activity, and saccade-related activity converge, often at the single-neuron level. Characterizing the clustering of functional properties in areas with mixed selectivity, such as these, may help reveal organizational principles that support sensorimotor transformations. Here we quantified the clustering of visual feature selectivity, choice-related activity, and saccaderelated activity by performing correlational and parametric comparisons of the responses of well-isolated, simultaneously recorded neurons in macaque monkeys. Each functional domain showed statistically significant clustering in both areas. However, there were also domain-specific differences in the strength of clustering across the areas. Visual feature selectivity and saccade-related activity were more strongly clustered in V3A than in CIP. In contrast, choice-related activity was more strongly clustered in CIP than in V3A. These differences in clustering may reflect the areas' roles in sensorimotor processing. Stronger clustering of visual and saccade-related activity in V3A may reflect a greater role in within-domain processing, as opposed to cross-domain synthesis. In contrast, stronger clustering of choice-related activity in CIP may reflect a greater role in synthesizing information across functional domains to bridge perception and action. |
Corey M. Ziemba; Robbe L. T. Goris; Gabriel M. Stine; Richard K. Perez; Eero P. Simoncelli; J. Anthony Movshon Neuronal and behavioral responses to naturalistic texture images in macaque monkeys Journal Article In: The Journal of Neuroscience, vol. 44, no. 42, pp. 1–14, 2024. @article{Ziemba2024, The visual world is richly adorned with texture, which can serve to delineate important elements of natural scenes. In anesthetized macaque monkeys, selectivity for the statistical features of natural texture is weak in V1, but substantial in V2, suggesting that neuronal activity in V2 might directly support texture perception. To test this, we investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured behavioral judgments of texture. We generated stimuli along a continuum between naturalistic texture and phase-randomized noise and trained two macaque monkeys to judge whether a sample texture more closely resembled one or the other extreme. Analysis of responses revealed that individual V1 and V2 neurons carried much less information about texture naturalness than behavioral reports. However, the sensitivity of V2 neurons, especially those preferring naturalistic textures, was significantly closer to that of behavior compared with V1. The firing of both V1 and V2 neurons predicted perceptual choices in response to repeated presentations of the same ambiguous stimulus in one monkey, despite low individual neural sensitivity. However, neither population predicted choice in the second monkey. We conclude that neural responses supporting texture perception likely continue to develop downstream of V2. Further, combined with neural data recorded while the same two monkeys performed an orientation discrimination task, our results demonstrate that choice-correlated neural activity in early sensory cortex is unstable across observers and tasks, untethered from neuronal sensitivity, and thus unlikely to reflect a critical aspect of the formation of perceptual decisions. Significance statement As visual signals propagate along the cortical hierarchy, they encode increasingly complex aspects of the sensory environment and likely have a more direct relationship with perceptual experience. We replicate and extend previous results from anesthetized monkeys differentiating the selectivity of neurons along the first step in cortical vision from area V1 to V2. However, our results further complicate efforts to establish neural signatures that reveal the relationship between perception and the neuronal activity of sensory populations. We find that choice-correlated activity in V1 and V2 is unstable across different observers and tasks, and also untethered from neuronal sensitivity and other features of nonsensory response modulation. |
Diego Mendoza-Halliday; Alex James Major; Noah Lee; Maxwell J. Lichtenfeld; Brock Carlson; Blake Mitchell; Patrick D. Meng; Yihan Xiong; Jacob A. Westerberg; Xiaoxuan Jia; Kevin D. Johnston; Janahan Selvanayagam; Stefan Everling; Alexander Maier; Robert Desimone; Earl K. Miller; André M. Bastos A ubiquitous spectrolaminar motif of local field potential power across the primate cortex Book Springer US, 2024. @book{MendozaHalliday2024, The mammalian cerebral cortex is anatomically organized into a six-layer motif. It is currently unknown whether a corresponding laminar motif of neuronal activity patterns exists across the cortex. Here we report such a motif in the power of local field potentials (LFPs). Using laminar probes, we recorded LFPs from 14 cortical areas across the cortical hierarchy in five macaque monkeys. The laminar locations of recordings were histologically identified by electrolytic lesions. Across all areas, we found a ubiquitous spectrolaminar pattern characterized by an increasing deep-to-superficial layer gradient of high-frequency power peaking in layers 2/3 and an increasing superficial-to-deep gradient of alpha-beta power peaking in layers 5/6. Laminar recordings from additional species showed that the spectrolaminar pattern is highly preserved among primates—macaque, marmoset and human—but more dissimilar in mouse. Our results suggest the existence of a canonical layer-based and frequency-based mechanism for cortical computation. |
Diego Mendoza-Halliday; Haoran Xu; Frederico A. C. Azevedo; Robert Desimone Dissociable neuronal substrates of visual feature attention and working memory Journal Article In: Neuron, vol. 112, no. 5, pp. 850–863, 2024. @article{MendozaHalliday2024a, Attention and working memory (WM) are distinct cognitive functions, yet given their close interactions, it is often assumed that they share the same neuronal mechanisms. We show that in macaques performing a WM-guided feature attention task, the activity of most neurons in areas middle temporal (MT), medial superior temporal (MST), lateral intraparietal (LIP), and posterior lateral prefrontal cortex (LPFC-p) displays attentional modulation or WM coding and not both. One area thought to play a role in both functions is LPFC-p. To test this, we optogenetically inactivated LPFC-p bilaterally during different task periods. Attention period inactivation reduced attentional modulation in LPFC-p, MST, and LIP neurons and impaired task performance. In contrast, WM period inactivation did not affect attentional modulation or performance and minimally affected WM coding. Our results suggest that feature attention and WM have dissociable neuronal substrates and that LPFC-p plays a critical role in feature attention, but not in WM. |
Abdolvahed Narmashiri; Mojtaba Abbaszadeh; Mohammad Hossein Nadian; Ali Ghazizadeh Value-based search efficiency is encoded in the substantia nigra reticulata firing rate, spiking irregularity and local field potential Journal Article In: The Journal of Neuroscience, vol. 44, no. 6, pp. 1–12, 2024. @article{Narmashiri2024, Recent results show that valuable objects can pop out in visual search, yet its neural mechanisms remain unexplored. Given the role of substantia nigra reticulata (SNr) in object value memory and control of gaze, we recorded its single-unit activity while male macaque monkeys engaged in efficient or inefficient search for a valuable target object among low-value objects. The results showed that efficient search was concurrent with stronger inhibition and higher spiking irregularity in the target-present (TP) compared with the target-absent (TA) trials in SNr. Importantly, the firing rate differentiation of TP and TA trials happened within ∼100 ms of display onset, and its magnitude was significantly correlated with the search times and slopes (search efficiency). Time–frequency analyses of local field potential (LFP) after display onset revealed significant modulations of the gamma band power with search efficiency. The greater reduction of SNr firing in TP trials in efficient search can create a stronger disinhibition of downstream superior colliculus, which in turn can facilitate saccade to obtain valuable targets in competitive environments. |
Sujaya Neupane; Ila Fiete; Mehrdad Jazayeri Mental navigation in the primate entorhinal cortex Journal Article In: Nature, vol. 630, no. 8017, pp. 704–711, 2024. @article{Neupane2024, A cognitive map is a suitably structured representation that enables novel computations using previous experience; for example, planning a new route in a familiar space. Work in mammals has found direct evidence for such representations in the presence of exogenous sensory inputs in both spatial and non-spatial domains. Here we tested a foundational postulate of the original cognitive map theory: that cognitive maps support endogenous computations without external input. We recorded from the entorhinal cortex of monkeys in a mental navigation task that required the monkeys to use a joystick to produce one-dimensional vectors between pairs of visual landmarks without seeing the intermediate landmarks. The ability of the monkeys to perform the task and generalize to new pairs indicated that they relied on a structured representation of the landmarks. Task-modulated neurons exhibited periodicity and ramping that matched the temporal structure of the landmarks and showed signatures of continuous attractor networks. A continuous attractor network model of path integration14 augmented with a Hebbian-like learning mechanism provided an explanation of how the system could endogenously recall landmarks. The model also made an unexpected prediction that endogenous landmarks transiently slow path integration, reset the dynamics and thereby reduce variability. This prediction was borne out in a reanalysis of firing rate variability and behaviour. Our findings link the structured patterns of activity in the entorhinal cortex to the endogenous recruitment of a cognitive map during mental navigation. |
Tarana Nigam; Caspar M. Schwiedrzik Predictions enable top-down pattern separation in the macaque face-processing hierarchy Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–13, 2024. @article{Nigam2024, Distinguishing faces requires well distinguishable neural activity patterns. Contextual information may separate neural representations, leading to enhanced identity recognition. Here, we use functional magnetic resonance imaging to investigate how predictions derived from contextual information affect the separability of neural activity patterns in the macaque face-processing system, a 3-level processing hierarchy in ventral visual cortex. We find that in the presence of predictions, early stages of this hierarchy exhibit well separable and high-dimensional neural geometries resembling those at the top of the hierarchy. This is accompanied by a systematic shift of tuning properties from higher to lower areas, endowing lower areas with higher-order, invariant representations instead of their feedforward tuning properties. Thus, top-down signals dynamically transform neural representations of faces into separable and high-dimensional neural geometries. Our results provide evidence how predictive context transforms flexible representational spaces to optimally use the computational resources provided by cortical processing hierarchies for better and faster distinction of facial identities. |
Taihei Ninomiya; Masaki Isoda Dynamic spatial representation of self and others' actions in the macaque frontal cortex Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 31, pp. 1–10, 2024. @article{Ninomiya2024, Modulation of neuronal firing rates by the spatial locations of physical objects is a widespread phenomenon in the brain. However, little is known about how neuronal responses to the actions of biological entities are spatially tuned and whether such spatially tuned responses are affected by social contexts. These issues are of key importance for understanding the neural basis of embodied social cognition, such as imitation and perspectivetaking. Here, we show that spatial representation of actions can be dynamically changed depending on others' social relevance and agents of action. Monkeys performed a turn-taking choice task with a real monkey partner sitting face-to-face or a filmed partner in prerecorded videos. Three rectangular buttons (left, center, and right) were positioned in front of the subject and partner as their choice targets. We recorded from single neurons in two frontal nodes in the social brain, the ventral premotor cortex (PMv) and the medial prefrontal cortex (MPFC). When the partner was filmed rather than real, spatial preference for partner-actions was markedly diminished in MPFC, but not PMv, neurons. This social context-dependent modulation in the MPFC was also evident for self- actions. Strikingly, a subset of neurons in both areas switched their spatial preference between self-actions and partner-actions in a diametrically opposite manner. This observation suggests that these cortical areas are associated with coordinate transformation in ways consistent with an actor- centered perspective-taking coding scheme. The PMv may subserve such functions in context-independent manners, whereas the MPFC may do so primarily in social contexts. |
Jalaledin Noroozi; Ehsan Rezayat; Mohammad-Reza A. Dehaqan Frontotemporal network contribution to occluded face processing Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 48, pp. 1–12, 2024. @article{Noroozi2024, Primates are known for their exceptional ability to recognize faces. However, we still have much to learn about how their brains process faces when they are partially hidden. When we cover parts of a face, it affects how our brains respond, even though we still perceive the face as a whole. This suggests that complex brain networks are at work in understanding partially hidden faces. To explore this further, we studied two brain regions, the ventrolateral prefrontal cortex (vlPFC) and the inferior temporal cortex (ITC), while showing primate images of faces with parts occluded. We found that vlPFC neurons were more active when faces were partially covered, while ITC neurons preferred fully visible faces. Interestingly, the ITC seemed to process occluded faces in a separate phase after the vlPFC responded. Our research revealed a coordinated effort between these brain regions based on the level of facial obstruction. Specifically, the vlPFC seemed to play a crucial role, driving the representation of occluded faces in the later phase of ITC processing. Importantly, we also found that the brain processes occluded faces differently from those that are fully visible, suggesting specialized mechanisms for handling these situations. These findings high-light the importance of feedback from the vlPFC in understanding occluded faces in the ITC region of the brain. Understanding these neural processes not only enhances our understanding of how primates perceive faces but also provides insights into broader aspects of visual cognition. |
Matthew F. Panichello; Donatas Jonikaitis; Yu Jin Oh; Shude Zhu; Ethan B. Trepka; Tirin Moore Intermittent rate coding and cue-specific ensembles support working memory Journal Article In: Nature, vol. 636, pp. 1–26, 2024. @article{Panichello2024, Persistent, memorandum-specific neuronal spiking activity has long been hypothesized to underlie working memory1,2. However, emerging evidence suggests a potential role for ‘activity-silent' synaptic mechanisms3–5. This issue remains controversial because evidence for either view has largely relied either on datasets that fail to capture single-trial population dynamics or on indirect measures of neuronal spiking. We addressed this controversy by examining the dynamics of mnemonic information on single trials obtained from large, local populations of lateral prefrontal neurons recorded simultaneously in monkeys performing a working memory task. Here we show that mnemonic information does not persist in the spiking activity of neuronal populations during memory delays, but instead alternates between coordinated ‘On' and ‘Off' states. At the level of single neurons, Off states are driven by both a loss of selectivity for memoranda and a return of firing rates to spontaneous levels. Further exploiting the large-scale recordings used here, we show that mnemonic information is available in the patterns of functional connections among neuronal ensembles during Off states. Our results suggest that intermittent periods of memorandum-specific spiking coexist with synaptic mechanisms to support working memory. |
Jagruti J. Pattadkal; Carrie Barr; Nicholas J. Priebe Interactions between saccades and smooth pursuit eye movements in marmosets Journal Article In: eNeuro, vol. 11, no. 6, pp. 1–11, 2024. @article{Pattadkal2024, Animals use a combination of eye movements to track moving objects. These different eye movements need to be coordinated for successful tracking, requiring interactions between the systems involved. Here, we study the interaction between the saccadic and smooth pursuit eye movement systems in marmosets. Using a single-target pursuit task, we show that saccades cause an enhancement in pursuit following a saccade. Using a two-target pursuit task, we show that this enhancement in pursuit is selective toward the motion of the target selected by the saccade, irrespective of any biases in pursuit prior to the saccade. These experiments highlight the similarities in the functioning of saccadic and smooth pursuit eye movement systems across primates. |
Barbara Peysakhovich; Ou Zhu; Stephanie M. Tetrick; Vinay Shirhatti; Alessandra A. Silva; Sihai Li; Guilhem Ibos; Matthew C. Rosen; W. Jeffrey; David J. Freedman Primate superior colliculus is causally engaged in abstract higher-order cognition Journal Article In: Nature Neuroscience, vol. 27, pp. 1999–2008, 2024. @article{Peysakhovich2024, The superior colliculus is an evolutionarily conserved midbrain region that is thought to mediate spatial orienting, including saccadic eye movements and covert spatial attention. Here, we reveal a role for the superior colliculus in higher-order cognition, independent of its role in spatial orienting. We trained rhesus macaques to perform an abstract visual categorization task that involved neither instructed eye movements nor differences in covert attention. We compared neural activity in the superior colliculus and the posterior parietal cortex, a region previously shown to causally contribute to abstract category decisions. The superior colliculus exhibits robust encoding of learned visual categories, which is stronger than in the posterior parietal cortex and arises at a similar latency in the two areas. Moreover, inactivation of the superior colliculus markedly impaired animals' category decisions. These results demonstrate that the primate superior colliculus mediates abstract, higher-order cognitive processes that have traditionally been attributed to the neocortex. Categorization |
Jay S. Pi; Mohammad Amin Fakharian; Paul Hage; Ehsan Sedaghat-Nejad; Salomon Z. Muller; Reza Shadmehr The olivary input to the cerebellum dissociates sensory events from movement plans Journal Article In: Proceedings of the National Academy of Sciences, vol. 121, no. 17, pp. 2024, 2024. @article{Pi2024, Neurons in the inferior olive are thought to anatomically organize the Purkinje cells (P-cells) of the cerebellum into computational modules, but what is computed by each module? Here, we designed a saccade task in marmosets that dissociated sensory events from motor events and then recorded the complex and simple spikes of hundreds of P-cells. We found that when a visual target was presented at a random location, the olive reported the direction of that sensory event to one group of P- cells, but not to a seond group. However, just before movement onset, it reported the direction of the planned movement to both groups, even if that movement was not toward the target. At the end of the movement if the subject experienced an error but chose to withhold the corrective movement, only the first group received information about the sensory prediction error. We organized the P-cells based on the information content of their olivary input and found that in the group that received sensory information, the simple spikes were suppressed during fixation, then produced a burst before saccade onset in a direction consistent with assisting the movement. In the second group, the simple spikes were not suppressed during fixation but burst near saccade deceleration in a direction consistent with stopping the movement. Thus, the olive differentiated the P-cells based on whether they would receive sensory or motor information, and this defined their contributions to control of movements as well as holding still. |
Hamidreza Ramezanpour; Christopher Giverin; Kohitij Kar Low-cost, portable, easy-to-use kiosks to facilitate home-cage testing of nonhuman primates during vision-based behavioral tasks Journal Article In: Journal of Neurophysiology, vol. 132, no. 3, pp. 666–677, 2024. @article{Ramezanpour2024, Nonhuman primates (NHPs), especially rhesus macaques, have significantly contributed to our understanding of the neural computations underlying human vision. Besides the established homologies in the visual brain areas between these species and our ability to probe detailed neural mechanisms in monkeys at multiple scales, NHPs' ability to perform human-like visual behavior makes them an extremely appealing animal model of human vision. Traditionally, such behavioral studies have been conducted in controlled laboratory settings, offering experimenters tight control over variables like luminance, eye movements, and auditory interference. However, in-lab experiments have several constraints, including limited experimental time, the need for dedicated human experimenters, additional lab space requirements, invasive surgeries for headpost implants, and extra time and training for chairing and head restraints. To overcome these limitations, we propose adopting home-cage behavioral training and testing of NHPs, enabling the administration of many vision-based behavioral tasks simultaneously across multiple monkeys with reduced human personnel requirements, no NHP head restraint, and monkeys' unrestricted access to experiments. In this article, we present a portable, low-cost, easy-to-use kiosk system developed to conduct home-cage vision-based behavioral tasks in NHPs. We provide details of its operation and build to enable more open-source development of this technology. Furthermore, we present validation results using behavioral measurements performed in the lab and in NHP home cages, demonstrating the system's reliability and potential to enhance the efficiency and flexibility of NHP behavioral research. |
Samy Rima; Jennifer Greilsamer; Marcus Haag; Jaime Cadena-Valencia; Morgan Sansonnens; Andrea Francovich; Florian Lanz; Andrina Zbinden; Alessandra Bergadano; Michael Christopher Schmid A chinrest-based approach to measure eye movements and experimental task engagement in macaques with minimal restraint Journal Article In: Journal of Neuroscience Methods, vol. 408, pp. 1–8, 2024. @article{Rima2024, Background: The use of Rhesus macaques in vision research is crucial due to their visual system's similarity to humans. While invasive techniques have been the norm, there has been a shift towards non-invasive methods, such as facemasks and head molds, to enhance animal welfare and address ethical concerns. New Method: We present a non-invasive, 3D-printed chinrest with infrared sensors, adapted from canine research, allowing for accurate eye movement measurements and voluntary animal participation in experiments. Results: The chinrest method showed a 16% and 28% increase in average trial numbers for Monkey 1 and Monkey 2, respectively, compared to the traditional headpost method. The engagement was high, with monkeys performing over 500 trials per session and initiating a new trial after an average intertrial interval of approximately 1 second. The hit rate improved by about 10% for Monkey 1 in the chinrest condition, and the fixation precision, measured by the standard deviation of gaze positions, was significantly better in the chinrest condition, with Monkey 1 showing a reduction in fixation imprecision from 0.26° to 0.17° in the X-axis. Comparison with Existing Methods: The chinrest approach showed significant improvements in trial engagement and reduction in aborted trials due to fixation breaks, indicating less stress and potentially improved data quality compared to previous non-invasive methods. Conclusions: The chinrest method offers a significant advancement in primate cognitive testing by allowing for precise data collection while addressing animal welfare concerns, possibly leading to better scientific outcomes and a paradigm shift in primate research methodologies. |
C. L. Rodríguez Deliz; Gerick M. Lee; Brittany N. Bushnell; Najib J. Majaj; J. Anthony Movshon; Lynne Kiorpes Development of radial frequency pattern perception in macaque monkeys Journal Article In: Journal of Vision, vol. 24, no. 6, pp. 1–17, 2024. @article{RodriguezDeliz2024, Infant primates see poorly, and most perceptual functions mature steadily beyond early infancy. Behavioral studies on human and macaque infants show that global form perception, as measured by the ability to integrate contour information into a coherent percept, improves dramatically throughout the first several years after birth. However, it is unknown when sensitivity to curvature and shape emerges in early life or how it develops. We studied the development of shape sensitivity in 18 macaques, aged 2 months to 10 years. Using radial frequency stimuli, circular targets whose radii are modulated sinusoidally, we tested monkeys' ability to radial frequency stimuli from circles as a function of the depth and frequency of sinusoidal modulation. We implemented a new four-choice oddity task and compared the resulting data with that from a traditional two-alternative forced choice task. We found that radial frequency pattern perception was measurable at the youngest age tested (2 months). Behavioral performance at all radial frequencies improved with age. Performance was better for higher radial frequencies, suggesting the developing visual system prioritizes processing of fine visual details that are ecologically relevant. By using two complementary methods, we were able to capture a comprehensive developmental trajectory for shape perception. |
Majid Roshanaei; Zahra Bahmani; Kelsey Clark; Mohammad Reza Daliri; Behrad Noudoost Working memory expedites the processing of visual signals within the extrastriate cortex Journal Article In: iScience, vol. 27, no. 8, pp. 1–12, 2024. @article{Roshanaei2024, Working memory is the ability to maintain information in the absence of sensory input. In this study, we investigated how working memory benefits processing in visual areas. Using a measure of phase consistency to detect the arrival time of visual signals to the middle temporal (MT) area, we assessed the impact of working memory on the speed of sensory processing. We recorded from MT neurons in two monkeys during a spatial working memory task with visual probes. When the memorized location closely matches the receptive field center of the recording site, visual input arrives sooner, but if the memorized location does not match the receptive field center then the arrival of visual information is delayed. Thus, working memory expedites the arrival of visual input in MT. These results reveal that even in the absence of firing rate changes, working memory can still benefit the processing of information within sensory areas. |
Atena Sajedin; Sina Salehi; Hossein Esteky Information content and temporal structure of face selective local field potentials frequency bands in IT cortex Journal Article In: Cerebral Cortex, vol. 34, no. 1, pp. 1–12, 2024. @article{Sajedin2024, Sensory stimulation triggers synchronized bioelectrical activity in the brain across various frequencies. This study delves into network-level activities, specifically focusing on local field potentials as a neural signature of visual category representation. Specifically, we studied the role of different local field potential frequency oscillation bands in visual stimulus category representation by presenting images of faces and objects to three monkeys while recording local field potential from inferior temporal cortex. We found category selective local field potential responses mainly for animate, but not inanimate, objects. Notably, face-selective local field potential responses were evident across all tested frequency bands, manifesting in both enhanced (above mean baseline activity) and suppressed (below mean baseline activity) local field potential powers. We observed four different local field potential response profiles based on frequency bands and face selective excitatory and suppressive responses. Low-frequency local field potential bands (1–30 Hz) were more prodominstaly suppressed by face stimulation than the high-frequency (30–170 Hz) local field potential bands. Furthermore, the low-frequency local field potentials conveyed less face category informtion than the high-frequency local field potential in both enhansive and suppressive conditions. Furthermore, we observed a negative correlation between face/object d-prime values in all the tested local field potential frequency bands and the anterior–posterior position of the recording sites. In addition, the power of low-frequency local field potential systematically declined across inferior temporal anterior–posterior positions, whereas high-frequency local field potential did not exhibit such a pattern. In general, for most of the above-mentioned findings somewhat similar results were observed for body, but not, other stimulus categories. The observed findings suggest that a balance of face selective excitation and inhibition across time and cortical space shape face category selectivity in inferior temporal cortex. |
Jason M. Samonds; Martin Szinte; Carrie Barr; Anna Montagnini; Guillaume S. Masson; Nicholas J. Priebe Mammals achieve common neural coverage of visual scenes using distinct sampling behaviors Journal Article In: eNeuro, vol. 11, no. 2, pp. 1–13, 2024. @article{Samonds2024, Most vertebrates use head and eye movements to quickly change gaze orientation and sample different portions of the environment with periods of stable fixation. Visual information must be integrated across fixations to construct a complete perspective of the visual environment. In concert with this sampling strategy, neurons adapt to unchanging input to conserve energy and ensure that only novel information from each fixation is processed. We demonstrate how adaptation recovery times and saccade properties interact and thus shape spatiotemporal tradeoffs observed in the motor and visual systems of mice, cats, marmosets, macaques, and humans. These tradeoffs predict that in order to achieve similar visual coverage over time, animals with smaller receptive field sizes require faster saccade rates. Indeed, we find comparable sampling of the visual environment by neuronal populations across mammals when integrating measurements of saccadic behavior with receptive field sizes and V1 neuronal den-sity. We propose that these mammals share a common statistically driven strategy of maintaining coverage of their visual environment over time calibrated to their respective visual system characteristics. |
Janahan Selvanayagam; Kevin D. Johnston; Stefan Everling Laminar dynamics of target selection in the posterior parietal cortex of the common marmoset Journal Article In: The Journal of Neuroscience, vol. 44, no. 21, pp. 1–16, 2024. @article{Selvanayagam2024, The lateral intraparietal area (LIP) plays a crucial role in target selection and attention in primates, but the laminar microcircuitry of this region is largely unknown. To address this, we used ultra-high density laminar electrophysiology with Neuropixels probes to record neural activity in the posterior parietal cortex (PPC) of two adult marmosets while they performed a simple visual target selection task. Our results reveal neural correlates of visual target selection in the marmoset, similar to those observed in macaques and humans, with distinct timing and profiles of activity across cell types and cortical layers. Notably, a greater proportion of neurons exhibited stimulus-related activity in superficial layers whereas a greater proportion of infragranular neurons exhibited significant postsaccadic activity. Stimulus-related activity was first observed in granular layer putative interneurons, whereas target discrimination activity emerged first in supragranular layers putative pyramidal neurons, supporting a canonical laminar circuit underlying visual target selection in marmoset PPC. These findings provide novel insights into the neural basis of visual attention and target selection in primates. |
Elia Shahbazi; Timothy Ma; Martin Pernuš; Walter Scheirer; Arash Afraz Perceptography unveils the causal contribution of inferior temporal cortex to visual perception Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–11, 2024. @article{Shahbazi2024, Neurons in the inferotemporal (IT) cortex respond selectively to complex visual features, implying their role in object perception. However, perception is subjective and cannot be read out from neural responses; thus, bridging the causal gap between neural activity and perception demands independent characterization of perception. Historically, though, the complexity of the perceptual alterations induced by artificial stimulation of IT cortex has rendered them impossible to quantify. To address this old problem, we tasked male macaque monkeys to detect and report optical impulses delivered to their IT cortex. Combining machine learning with high-throughput behavioral optogenetics, we generated complex and highly specific images that were hard for the animal to distinguish from the state of being cortically stimulated. These images, named “perceptograms” for the first time, reveal and depict the contents of the complex hallucinatory percepts induced by local neural perturbation in IT cortex. Furthermore, we found that the nature and magnitude of these hallucinations highly depend on concurrent visual input, stimulation location, and intensity. Objective characterization of stimulation-induced perceptual events opens the door to developing a mechanistic theory of visual perception. Further, it enables us to make better visual prosthetic devices and gain a greater understanding of visual hallucinations in mental disorders. |
Patricia L. Stan; Matthew A. Smith Recent visual experience reshapes V4 neuronal activity and improves perceptual performance Journal Article In: The Journal of Neuroscience, vol. 44, no. 41, pp. 1–17, 2024. @article{Stan2024, Recent visual experience heavily influences our visual perception, but how this is mediated by the reshaping of neuronal activity to alter and improve perceptual discrimination remains unknown. We recorded from populations of neurons in visual cortical area V4 while two male rhesus macaque monkeys performed a natural image change detection task under different experience conditions. We found that maximizing the recent experience with a particular image led to an improvement in the ability to detect a change in that image. This improvement was associated with decreased neural responses to the image, consistent with neuronal changes previously seen in studies of adaptation and expectation. We found that the magnitude of behavioral improvement was correlated with the magnitude of response suppression. Furthermore, this suppression of activity led to an increase in signal separation, providing evidence that a reduction in activity can improve stimulus encoding. Within populations of neurons, greater recent experience was associated with decreased trial-to-trial shared variability, indicating that a reduction in variability is a key means by which experience influences perception. Taken together, the results of our study contribute to an understanding of how recent visual experience can shape our perception and behavior through modulating activity patterns in mid-level visual cortex. Significance Statement Our visual experience shapes our perception and behavior. This work identifies neural signatures of visual experience that directly link to behavioral performance, an area that has been elusive in past work. Our study represents a demonstration of how the activity of populations of neurons in the visual cortex, shaped by experience, can reflect an altered neural code that underlies behavior. |
Natalie A Steinemann; Gabriel M Stine; Eric M Trautmann; Ariel Zylberberg; Daniel M Wolpert; Michael N Shadlen Direct observation of the neural computations underlying a single decision Journal Article In: eLife, vol. 12, pp. 1–29, 2024. @article{Steinemann2024, Neurobiological investigations of perceptual decision-making have furnished the first glimpse of a flexible cognitive process at the level of single neurons (Shadlen & Newsome, 1996; Shadlen & Kiani 2013). Neurons in the parietal and prefrontal cortex (Kim & Shadlen, 1999; Romo, Hernandez & Zainos, 2004; Hernandez, Zainos & Romo, 2002; Ding & Gold, 2012) are thought to represent the accumulation of noisy evidence, acquired over time, leading to a decision. Neural recordings averaged over many decisions have provided support for the deterministic rise in activity to a termination bound (Roitman & Shadlen, 2002). Critically, it is the unobserved stochastic component that is thought to confer variability in both choice and decision time (Gold & Shadlen, 2007). Here, we elucidate this stochastic, diffusion-like signal on individual decisions by recording simultaneously from hundreds of neurons in the lateral intraparietal cortex (LIP). We show that a small subset of these neurons, previously studied singly, represent a combination of deterministic drift and stochastic diffusion—the integral of noisy evidence—during perceptual decision making, and we provide direct support for the hypothesis that this diffusion signal is the quantity responsible for the variability in choice and reaction times. Neuronal state space and decoding analyses, applied to the whole population, also identify the drift diffusion signal. However, we show that the signal relies on the subset of neurons with response fields that overlap the choice targets. This parsimonious observation would escape detection by these powerful methods, absent a clear hypothesis. ### Competing Interest Statement The authors have declared no competing interest. |
Reiji Tanaka; Kei Watanabe; Takafumi Suzuki; Kae Nakamura; Masaharu Yasuda; Hiroshi Ban; Ken Okada; Shigeru Kitazawa An easy-to-implement, non-invasive head restraint method for monkey fMRI Journal Article In: NeuroImage, vol. 285, pp. 1–12, 2024. @article{Tanaka2024, Functional magnetic resonance imaging (fMRI) in behaving monkeys has a strong potential to bridge the gap between human neuroimaging and primate neurophysiology. In monkey fMRI, to restrain head movements, researchers usually surgically implant a plastic head-post on the skull. Although time-proven to be effective, this technique could create burdens for animals, including a risk of infection and discomfort. Furthermore, the presence of extraneous objects on the skull, such as bone screws and dental cement, adversely affects signals near the cortical surface. These side effects are undesirable in terms of both the practical aspect of efficient data collection and the spirit of “refinement” from the 3R's. Here, we demonstrate that a completely non-invasive fMRI scan in awake monkeys is possible by using a plastic head mask made to fit the skull of individual animals. In all of the three monkeys tested, longitudinal, quantitative assessment of head movements showed that the plastic mask has effectively suppressed head movements, and we were able to obtain reliable retinotopic BOLD signals in a standard retinotopic mapping task. The present, easy-to-make plastic mask has a strong potential to simplify fMRI experiments in awake monkeys, while giving data that is as good as or even better quality than that obtained with the conventional head-post method. |
John M. Tauber; Scott L. Brincat; Emily P. Stephen; Jacob A. Donoghue; Leo Kozachkov; Emery N. Brown; Earl K. Miller Propofol-mediated unconsciousness disrupts progression of sensory signals through the cortical hierarchy Journal Article In: Journal of Cognitive Neuroscience, vol. 36, no. 2, pp. 394–413, 2024. @article{Tauber2024, A critical component of anesthesia is the loss of sensory perception. Propofol is the most widely used drug for general anesthesia, but the neural mechanisms of how and when it disrupts sensory processing are not fully understood. We analyzed local field potential and spiking recorded from Utah arrays in auditory cortex, associative cortex, and cognitive cortex of nonhuman primates before and during propofol-mediated unconsciousness. Sensory stimuli elicited robust and decodable stimulus responses and triggered periods of stimulus-related synchronization between brain areas in the local field potential of Awake animals. By contrast, propofol-mediated unconsciousness eliminated stimulus-related synchrony and drastically weakened stimulus responses and information in all brain areas except for auditory cortex, where responses and information persisted. However, we found stimuli occurring during spiking Up states triggered weaker spiking responses than in Awake animals in auditory cortex, and little or no spiking responses in higher order areas. These results suggest that propofol's effect on sensory processing is not just because of asynchronous Down states. Rather, both Down states and Up states reflect disrupted dynamics. |
Zhenghe Tian; Jingwen Chen; Cong Zhang; Bin Min; Bo Xu; Liping Wang Mental programming of spatial sequences in working memory in the macaque frontal cortex Journal Article In: Science, vol. 385, no. 1437, pp. 1–1, 2024. @article{Tian2024a, WM refers to our ability to temporarily maintain and manipulate information, which is foundational to the organization of goal-directed behavior. Although the nature of WM maintenance has been the focus of WM research in the past decades, WM manipulation or volitional control is more complex and has received less attention. The control process is what makes WM distinct and sets it apart from short-term memory. Previous human imaging studies have shown that the frontal cortex was highly involved inWM control. However, the neural dynamics and computational mechanisms supporting the control are not understood. We aimed to characterize these neural computations in the frontal cortex of nonhuman primates. |
Motoaki Uchimura; Hironori Kumano; Shigeru Kitazawa Neural transformation from retinotopic to background-centric coordinates in the macaque precuneus Journal Article In: The Journal of Neuroscience, vol. 44, no. 48, pp. 1–19, 2024. @article{Uchimura2024, Visual information is initially represented in retinotopic coordinates and later in craniotopic coordinates. Psychophysical evidence suggests that visual information is further represented in more general coordinates related to the external world; however, the neural basis of nonegocentric coordinates remains elusive. This study investigates the automatic transformation from egocentric to nonegocentric coordinates in the macaque precuneus (two males, one female), identified by a functional imaging study as a key area for nonegocentric representation. We found that 6.2% of neurons in the precuneus have receptive fields (RFs) anchored to the background rather than to the retina or the head, while 16% had traditional retinotopic RFs. Notably, these two types were not exclusive: many background-centric neurons initially encode a stimulus' position in retinotopic coordinates (up to ∼90 ms from the stimulus onset) but later shift to background coordinates, peaking at ∼150 ms. Regarding retinotopic information, the stimulus dominated the initial period, whereas the background dominated the later period. In the absence of a background, there is a dramatic surge in retinotopic information about the stimulus during the later phase, clearly delineating two distinct periods of retinotopic encoding: one focusing on the figure to be attended and another on the background. These findings suggest that the initial retinotopic information of the stimulus is combined with the background retinotopic information in a subsequent stage, yielding a more stable representation of the stimulus relative to the background through time-division multiplexing. |
Ahmad Jezzini; Camillo Padoa-Schioppa Neuronal activity in the gustatory cortex during economic choice Journal Article In: The Journal of Neuroscience, vol. 44, no. 33, pp. 1–16, 2024. @article{Jezzini2024, An economic choice entails computing and comparing the values of individual offers. Offer values are represented in the orbitofrontal cortex (OFC)—an area that participates in value comparison—but it is unknown where offer values are computed in the first place. One possibility is that this computation takes place in OFC. Alternatively, offer values might be computed upstream of OFC. For choices between edible goods, a primary candidate is the gustatory region of the anterior insula (gustatory cortex, GC). Here we recorded from the GC of male rhesus monkeys choosing between different juice types. As a population, neurons in GC represented the flavor, the quantity, and the subjective value of the juice chosen by the animal. These variables were represented by distinct groups of cells and with different time courses. Specifically, chosen value signals emerged shortly after offer presentation, while neurons encoding the chosen juice and the chosen quantity peaked after juice delivery. Surprisingly, neurons in GC did not represent individual offer values in a systematic way. In a computational sense, the variables encoded in GC follow the process of value comparison. Thus our results argue against the hypothesis that offer values are computed in GC. At the same time, signals representing the subjective value of the expected reward indicate that responses in GC are not purely sensory. Thus neuronal responses in GC appear consummatory in nature. |
W. Jeffrey Johnston; Justin M. Fine; Seng Bum Michael Yoo; R. Becket Ebitz; Benjamin Y. Hayden Semi-orthogonal subspaces for value mediate a tradeoff between binding and generalization Journal Article In: Nature Neuroscience, vol. 27, pp. 2218–2230, 2024. @article{Johnston2024, When choosing between options, we must associate their values with the actions needed to select them. We hypothesize that the brain solves this binding problem through neural population subspaces. Here, in macaques performing a choice task, we show that neural populations in five reward-sensitive regions encode the values of offers presented on the left and right in distinct subspaces. This encoding is sufficient to bind offer values to their locations while preserving abstract value information. After offer presentation, all areas encode the value of the first and second offers in orthogonal subspaces; this orthogonalization also affords binding. Our binding-by-subspace hypothesis makes two new predictions confirmed by the data. First, behavioral errors should correlate with spatial, but not temporal, neural misbinding. Second, behavioral errors should increase when offers have low or high values, compared to medium values, even when controlling for value difference. Together, these results support the idea that the brain uses semi-orthogonal subspaces to bind features. |
Katarzyna Jurewicz; Brianna J. Sleezer; Priyanka S. Mehta; Benjamin Y. Hayden; R. Becket Ebitz Irrational choices via a curvilinear representational geometry for value Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–15, 2024. @article{Jurewicz2024, We make decisions by comparing values, but it is not yet clear how value is represented in the brain. Many models assume, if only implicitly, that the representational geometry of value is linear. However, in part due to a historical focus on noisy single neurons, rather than neuronal populations, this hypothesis has not been rigorously tested. Here, we examine the representational geometry of value in the ventromedial prefrontal cortex (vmPFC), a part of the brain linked to economic decision-making, in two male rhesus macaques. We find that values are encoded along a curved manifold in vmPFC. This curvilinear geometry predicts a specific pattern of irrational decision-making: that decision-makers will make worse choices when an irrelevant, decoy option is worse in value, compared to when it is better. We observe this type of irrational choices in behavior. Together, these results not only suggest that the representational geometry of value is nonlinear, but that this nonlinearity could impose bounds on rational decision-making. |
Taekjun Kim; Anitha Pasupathy Neural correlates of crowding in macaque area V4 Journal Article In: The Journal of Neuroscience, vol. 44, no. 24, pp. 1—-16, 2024. @article{Kim2024f, Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Many psychophysical studies have investigated this phenomenon and proposed alternative models for the underlying mechanisms. One prominent hypothesis, albeit with mixed psychophysical support, posits that crowding arises from the loss of information due to pooled encoding of features from target and distractor stimuli in the early stages of cortical visual processing. However, neurophysiological studies have not rigorously tested this hypothesis. We studied the responses of single neurons in macaque (one male, one female) area V4, an intermediate stage of the object-processing pathway, to parametrically designed crowded displays and texture statistics-matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters—number, distance, and position of distractors—influence human psychophysical performance and V4 shape selectivity. Importantly, we also found that enhancing the salience of a target stimulus could alleviate crowding effects in highly cluttered scenes, and this could be temporally protracted reflecting a dynamical process. Thus, a pooled encoding of nearby stimuli cannot explain the observed responses, and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays. Overall, we conclude that the magnitude of crowding effects is determined not just by the number of distractors and target–distractor separation but also by the relative salience of targets versus distractors based on their feature attributes—the similarity of distractors and the contrast between target and distractor stimuli. |
Pooya Laamerad; Liu D. Liu; Christopher C. Pack Decision-related activity and movement selection in primate visual cortex Journal Article In: Science Advances, vol. 10, no. 22, pp. 1–12, 2024. @article{Laamerad2024, Fluctuations in the activity of sensory neurons often predict perceptual decisions. This connection can be quantified with a metric called choice probability (CP), and there is a longstanding debate about whether CP reflects a causal influence on decisions or an echo of decision-making activity elsewhere in the brain. Here, we show that CP can reflect a third variable, namely, the movement used to indicate the decision. In a standard visual motion discrimination task, neurons in the middle temporal (MT) area of primate cortex responded more strongly during trials that involved a saccade toward their receptive fields. This variability accounted for much of the CP observed across the neuronal population, and it arose through training. Moreover, pharmacological inactivation of MT biased behavioral responses away from the corresponding visual field locations. These results demonstrate that training on a task with fixed sensorimotor contingencies introduces movement-related activity in sensory brain regions and that this plasticity can shape the neural circuitry of perceptual decision-making. |
Noga Larry; Gil Zur; Mati Joshua Organization of reward and movement signals in the basal ganglia and cerebellum Journal Article In: Nature Communications, vol. 15, no. 1, pp. 1–13, 2024. @article{Larry2024, The basal ganglia and the cerebellum are major subcortical structures in the motor system. The basal ganglia have been cast as the reward center of the motor system, whereas the cerebellum is thought to be involved in adjusting sensorimotor parameters. Recent findings of reward signals in the cerebellum have challenged this dichotomous view. To compare the basal ganglia and the cerebellum directly, we recorded from oculomotor regions in both structures from the same monkeys. We partitioned the trial-by-trial variability of the neurons into reward and eye-movement signals to compare the coding across structures. Reward expectation and movement signals were the most pronounced in the output structure of the basal ganglia, intermediate in the cerebellum, and the smallest in the input structure of the basal ganglia. These findings suggest that reward and movement information is sharpened through the basal ganglia, resulting in a higher signal-to-noise ratio than in the cerebellum. |
Ye Liu; Bridget W. Mahony; Xiaochun Wang; Pierre M. Daye; Wei Wang; Patrick Cavanagh; Pierre Pouget; Ian Max Andolina Assessing perceptual chromatic equiluminance using a reflexive pupillary response Journal Article In: Scientific Reports, vol. 14, no. 1, pp. 1–12, 2024. @article{Liu2024i, Equiluminant stimuli help assess the integrity of colour perception and the relationship of colour to other visual features. As a result of individual variation, it is necessary to calibrate experimental visual stimuli to suit each individual's unique equiluminant ratio. Most traditional methods rely on training observers to report their subjective equiluminance point. Such paradigms cannot easily be implemented on pre-verbal or non-verbal observers. Here, we present a novel Pupil Frequency-Tagging Method (PFTM) for detecting a participant's unique equiluminance point without verbal instruction and with minimal training. PFTM analyses reflexive pupil oscillations induced by slow (< 2 Hz) temporal alternations between coloured stimuli. Two equiluminant stimuli will induce a similar pupil dilation response regardless of colour; therefore, an observer's equiluminant point can be identified as the luminance ratio between two colours for which the oscillatory amplitude of the pupil at the tagged frequency is minimal. We compared pupillometry-based equiluminance ratios to those obtained with two established techniques in humans: minimum flicker and minimum motion. In addition, we estimated the equiluminance point in non-human primates, demonstrating that this new technique can be successfully employed in non-verbal subjects. |
Liya Ma; Nupur Katyare; Kevin Johnston; Stefan Everling Effects of ketamine on frontoparietal interactions in a rule-based antisaccade task in macaque monkeys Journal Article In: Journal of Neuroscience, vol. 44, no. 50, pp. 1–19, 2024. @article{Ma2024c, Cognitive control is engaged by working memory processes and high-demand situations like antisaccade, where one must suppress a prepotent response. While it is known to be supported by the frontoparietal control network, how intra- and interareal dynamics contribute to cognitive control processes remains unclear. N-Methyl-D-aspartate glutamate receptors (NMDARs) play a key role in prefrontal dynamics that support cognitive control. NMDAR antagonists, such as ketamine, are known to alter task-related prefrontal activities and impair cognitive performance. However, the role of NMDAR in cognitive control-related frontoparietal dynamics remains underexplored. Here, we simultaneously recorded local field potentials and single-unit activities from the lateral prefrontal (lPFC) and posterior parietal cortices (PPC) in two male macaque monkeys during a rule-based antisaccade task, with both rule-visible (RV) and rule-memorized (RM) conditions. In addition to altering the E/I balance in both areas, ketamine had a negative impact on rule coding in true oscillatory activities. It also reduced frontoparietal coherence in a frequency- and rule-dependent manner. Granger prediction analysis revealed that ketamine induced an overall reduction in bidirectional connectivity. Among antisaccade trials, a greater reduction in lPFC–PPC connectivity during the delay period preceded a greater delay in saccadic onset under the RM condition and a greater deficit in performance under the RV condition. Lastly, ketamine compromised rule coding in lPFC neurons in both RV and RM conditions and in PPC neurons only in the RV condition. Our findings demonstrate the utility of acute NMDAR antagonists in understanding the mechanisms through which frontoparietal dynamics support cognitive control processes. |
2023 |
Patrick Jendritza; Frederike J. Klein; Pascal Fries Multi-area recordings and optogenetics in the awake, behaving marmoset Journal Article In: Nature Communications, vol. 14, no. 1, pp. 1–16, 2023. @article{Jendritza2023, The common marmoset has emerged as a key model in neuroscience. Marmosets are small in size, show great potential for genetic modification and exhibit complex behaviors. Thus, it is necessary to develop technology that enables monitoring and manipulation of the underlying neural circuits. Here, we describe a novel approach to record and optogenetically manipulate neural activity in awake, behaving marmosets. Our design utilizes a light-weight, 3D printed titanium chamber that can house several high-density silicon probes for semi-chronic recordings, while enabling simultaneous optogenetic stimulation. We demonstrate the application of our method in male marmosets by recording multi- and single-unit data from areas V1 and V6 with 192 channels simultaneously, and show that optogenetic activation of excitatory neurons in area V6 can influence behavior in a detection task. This method may enable future studies to investigate the neural basis of perception and behavior in the marmoset. |
Leor N. Katz; Gongchen Yu; James P. Herman; Richard J. Krauzlis Correlated variability in primate superior colliculus depends on functional class Journal Article In: Communications Biology, vol. 6, no. 1, pp. 1–13, 2023. @article{Katz2023, Correlated variability in neuronal activity (spike count correlations, rSC) can constrain how information is read out from populations of neurons. Traditionally, rSC is reported as a single value summarizing a brain area. However, single values, like summary statistics, stand to obscure underlying features of the constituent elements. We predict that in brain areas containing distinct neuronal subpopulations, different subpopulations will exhibit distinct levels of rSC that are not captured by the population rSC. We tested this idea in macaque superior colliculus (SC), a structure containing several functional classes (i.e., subpopulations) of neurons. We found that during saccade tasks, different functional classes exhibited differing degrees of rSC. “Delay class” neurons displayed the highest rSC, especially during saccades that relied on working memory. Such dependence of rSC on functional class and cognitive demand underscores the importance of taking functional subpopulations into account when attempting to model or infer population coding principles. |
Kenji W. Koyano; Elena M. Esch; Julie J. Hong; Elena N. Waidmann; Haitao Wu; David A. Leopold Progressive neuronal plasticity in primate visual cortex during stimulus familiarization Journal Article In: Science Advances, vol. 9, no. 12, pp. 1–12, 2023. @article{Koyano2023, The primate brain is equipped to learn and remember newly encountered visual stimuli such as faces and objects. In the macaque inferior temporal (IT) cortex, neurons mark the familiarity of a visual stimulus through response modification, often involving a decrease in spiking rate. Here, we investigate the emergence of this neural plasticity by longitudinally tracking IT neurons during several weeks of familiarization with face images. We found that most neurons in the anterior medial (AM) face patch exhibited a gradual decline in their late-phase visual responses to multiple stimuli. Individual neurons varied from days to weeks in their rates of plasticity, with time constants determined by the number of days of exposure rather than the cumulative number of presentations. We postulate that the sequential recruitment of neurons with experience-modified responses may provide an internal and graded measure of familiarity strength, which is a key mnemonic component of visual recognition. |
Rosa Lafer-Sousa; Karen Wang; Reza Azadi; Emily Lopez; Simon Bohn; Arash Afraz Behavioral detectability of optogenetic stimulation of inferior temporal cortex varies with the size of concurrently viewed objects Journal Article In: Current Research in Neurobiology, vol. 4, pp. 1–7, 2023. @article{LaferSousa2023, We have previously demonstrated that macaque monkeys can behaviorally detect a subtle optogenetic impulse delivered to their inferior temporal (IT) cortex. We have also shown that the ability to detect the cortical stimulation impulse varies depending on some characteristics of the visual images viewed at the time of brain stimulation, revealing the visual nature of the perceptual events induced by stimulation of the IT cortex. Here we systematically studied the effect of the size of viewed objects on behavioral detectability of optogenetic stimulation of the central IT cortex. Surprisingly, we found that behavioral detection of the same optogenetic impulse highly varies with the size of the viewed object images. Reduction of the object size in four steps from 8 to 1 degree of visual angle significantly decreased detection performance. These results show that identical stimulation impulses delivered to the same neural population induce variable perceptual events depending on the mere size of the objects viewed at the time of brain stimulation. |
Aaron J. Levi; Yuan Zhao; Il Memming Park; Alexander C. Huk Sensory and choice responses in MT distinct from motion encoding Journal Article In: Journal of Neuroscience, vol. 43, no. 12, pp. 2090–2103, 2023. @article{Levi2023, The macaque middle temporal (MT) area is well known for its visual motion selectivity and relevance to motion perception, but the possibility of it also reflecting higher-level cognitive functions has largely been ignored. We tested for effects of task performance distinct from sensory encoding by manipulating subjects' temporal evidence-weighting strategy during a direction discrimination task while performing electrophysiological recordings from groups of MT neurons in rhesus macaques (one male, one female). This revealed multiple components of MT responses that were, surprisingly, not interpretable as behaviorally relevant modulations of motion encoding, or as bottom-up consequences of the readout of motion direction from MT. The time-varying motion-driven responses of MT were strongly affected by our strategic manipulation—but with time courses opposite the subjects' temporal weighting strategies. Furthermore, large choice-correlated signals were represented in population activity distinct from its motion responses, with multiple phases that lagged psychophysical readout and even continued after the stimulus (but which preceded motor responses). In summary, a novel experimental manipulation of strategy allowed us to control the time course of readout to challenge the correlation between sensory responses and choices, and population-level analyses of simultaneously recorded ensembles allowed us to identify strong signals that were so distinct from direction encoding that conventional, single-neuron-centric analyses could not have revealed or properly characterized them. Together, these approaches revealed multiple cognitive contributions to MT responses that are task related but not functionally relevant to encoding or decoding of motion for psychophysical direction discrimination, providing a new perspective on the assumed status of MT as a simple sensory area. |
John P. Liska; Declan P. Rowley; Trevor T. K. Nguyen; Jens-Oliver Muthmann; Daniel A. Butts; Jacob L. Yates; Alexander C. Huk; Liska John P.; Rowley Declan P.; Nguyen Trevor T. K.; Muthmann Jens-Oliver; Butts Daniel A.; Yates Jacob L.; Huk Alexander C. Running modulates primate and rodent visual cortex differently Journal Article In: eLife, vol. 12, no. 415, pp. 1–30, 2023. @article{Liska2023, When mice run, activity in their primary visual cortex (V1) is strongly modulated. This observation has altered conception of a brain region assumed to be a passive image processor. Extensive work has followed to dissect the circuits and functions of running-correlated modulation. However, it remains unclear whether visual processing in primates might similarly change during locomotion. We measured V1 activity in marmosets while they viewed stimuli on a treadmill. In contrast to mouse V1, marmoset V1 was slightly but reliably suppressed during running. Population-level analyses revealed trial-to-trial fluctuations of shared gain across V1 in both species, but these gain modulations were smaller and more often negatively correlated with running in marmosets. Thus, population-scale gain fluctuations of V1 reflect a common feature of mammalian visual cortical function, but important quantitative differences yield distinct consequences for the relation between vision and action in primates versus rodents. |
Xin He Liu; Lu Gan; Zhi Ting Zhang; Pan Ke Yu; Ji Dai Probing the processing of facial expressions in monkeys via time perception and eye tracking Journal Article In: Zoological Research, vol. 44, no. 5, pp. 882–893, 2023. @article{Liu2023e, Accurately recognizing facial expressions is essential for effective social interactions. Non-human primates (NHPs) are widely used in the study of the neural mechanisms underpinning facial expression processing, yet it remains unclear how well monkeys can recognize the facial expressions of other species such as humans. In this study, we systematically investigated how monkeys process the facial expressions of conspecifics and humans using eye-tracking technology and sophisticated behavioral tasks, namely the temporal discrimination task (TDT) and face scan task (FST). We found that monkeys showed prolonged subjective time perception in response to Negative facial expressions in monkeys while showing longer reaction time to Negative facial expressions in humans. Monkey faces also reliably induced divergent pupil contraction in response to different expressions, while human faces and scrambled monkey faces did not. Furthermore, viewing patterns in the FST indicated that monkeys only showed bias toward emotional expressions upon observing monkey faces. Finally, masking the eye region marginally decreased the viewing duration for monkey faces but not for human faces. By probing facial expression processing in monkeys, our study demonstrates that monkeys are more sensitive to the facial expressions of conspecifics than those of humans, thus shedding new light on inter-species communication through facial expressions between NHPs and humans. |
Shira M. Lupkin; Vincent B. McGinty Monkeys exhibit human-like gaze biases in economic decisions Journal Article In: eLife, vol. 12, pp. 1–27, 2023. @article{Lupkin2023, In economic decision-making individuals choose between items based on their perceived value. For both humans and nonhuman primates, these decisions are often carried out while shifting gaze between the available options. Recent studies in humans suggest that these shifts in gaze actively influence choice, manifesting as a bias in favor of the items that are viewed first, viewed last, or viewed for the overall longest duration in a given trial. This suggests a mechanism that links gaze behavior to the neural computations underlying value-based choices. In order to identify this mechanism, it is first necessary to develop and validate a suitable animal model of this behavior. To this end, we have created a novel value-based choice task for macaque monkeys that captures the essential features of the human paradigms in which gaze biases have been observed. Using this task, we identified gaze biases in the monkeys that were both qualitatively and quantita-tively similar to those in humans. In addition, the monkeys' gaze biases were well-explained using a sequential sampling model framework previously used to describe gaze biases in humans—the first time this framework has been used to assess value-based decision mechanisms in nonhuman primates. Together, these findings suggest a common mechanism that can explain gaze-related choice biases across species, and open the way for mechanistic studies to identify the neural origins of this behavior. |
Samuel Madariaga; Cecilia Babul; José Ignacio Egaña; Iván Rubio-Venegas; Gamze Güney; Miguel Concha-Miranda; Pedro E. Maldonado; Christ Devia In: MethodsX, vol. 10, pp. 1–10, 2023. @article{Madariaga2023, In this work we present SaFiDe, a deterministic method to detect eye movements (saccades and fixations) from eye-trace data. We developed this method for human and nonhuman primate data from video- and coil-recorded eye traces and further applied the algorithm to eye traces computed from electrooculograms. All the data analyzed were from free-exploration paradigms, where the main challenge was to detect periods of saccades and fixations that were uncued by the task. The method uses velocity and acceleration thresholds, calculated from the eye trace, to detect saccade and fixation periods. We show that our fully deterministic method detects saccades and fixations from eye traces during free visual exploration. The algorithm was implemented in MATLAB, and the code is publicly available on a GitHub repository. • The algorithm presented is entirely deterministic, simplifying the comparison between subjects and tasks. • Thus far, the algorithm presented can operate over video-based eye tracker data, human electrooculogram records, or monkey scleral eye coil data. |
Kazutaka Maeda; Ken Inoue; Masahiko Takada; Okihide Hikosaka Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques Journal Article In: Nature Communications, vol. 14, no. 1, pp. 1–12, 2023. @article{Maeda2023, Seeking out good and avoiding bad objects is critical for survival. In practice, objects are rarely good every time or everywhere, but only at the right time or place. Whereas the basal ganglia (BG) are known to mediate goal-directed behavior, for example, saccades to rewarding objects, it remains unclear how such simple behaviors are rendered contingent on higher-order factors, including environmental context. Here we show that amygdala neurons are sensitive to environments and may regulate putative dopamine (DA) neurons via an inhibitory projection to the substantia nigra (SN). In male macaques, we combined optogenetics with multi-channel recording to demonstrate that rewarding environments induce tonic firing changes in DA neurons as well as phasic responses to rewarding events. These responses may be mediated by disinhibition via a GABAergic projection onto DA neurons, which in turn is suppressed by an inhibitory projection from the amygdala. Thus, the amygdala may provide an additional source of learning to BG circuits, namely contingencies imposed by the environment. |
Taylor D. Webb; Matthew G. Wilson; Henrik Odéen; Jan Kubanek Sustained modulation of primate deep brain circuits with focused ultrasonic waves Journal Article In: Brain Stimulation, vol. 16, no. 3, pp. 798–805, 2023. @article{Webb2023, Background: Transcranial focused ultrasound has the potential to noninvasively modulate deep brain circuits and impart sustained, neuroplastic effects. Objective: Bring the approach closer to translations by demonstrating sustained modulation of deep brain circuits and choice behavior in task-performing non-human primates. Methods: Low-intensity transcranial ultrasound of 30 s in duration was delivered in a controlled manner into deep brain targets (left or right lateral geniculate nucleus; LGN) of non-human primates while the subjects decided whether a left or a right visual target appeared first. While the animals performed the task, we recorded intracranial EEG from occipital screws. The ultrasound was delivered into the deep brain targets daily for a period of more than 6 months. Results: The brief stimulation induced effects on choice behavior that persisted up to 15 minutes and were specific to the sonicated target. Stimulation of the left/right LGN increased the proportion of rightward/leftward choices. These effects were accompanied by an increase in gamma activity over visual cortex. The contralateral effect on choice behavior and the increase in gamma, compared to sham stimulation, suggest that the stimulation excited the target neural circuits. There were no detrimental effects on the animals' discrimination performance over the months-long course of the stimulation. Conclusion: This study demonstrates that brief, 30-s ultrasonic stimulation induces neuroplastic effects specifically in the target deep brain circuits, and that the stimulation can be applied daily without detrimental effects. These findings encourage repeated applications of transcranial ultrasound to malfunctioning deep brain circuits in humans with the goal of providing a durable therapeutic reset. |
Jacob A. Westerberg; Jeffrey D. Schall; Geoffrey F. Woodman; Alexander Maier Feedforward attentional selection in sensory cortex Journal Article In: Nature Communications, vol. 14, no. 1, pp. 1–17, 2023. @article{Westerberg2023, Salient objects grab attention because they stand out from their surroundings. Whether this phenomenon is accomplished by bottom-up sensory processing or requires top-down guidance is debated. We tested these alternative hypotheses by measuring how early and in which cortical layer(s) neural spiking distinguished a target from a distractor. We measured synaptic and spiking activity across cortical columns in mid-level area V4 of male macaque monkeys performing visual search for a color singleton. A neural signature of attentional capture was observed in the earliest response in the input layer 4. The magnitude of this response predicted response time and accuracy. Errant behavior followed errant selection. Because this response preceded top-down influences and arose in the cortical layer not targeted by top-down connections, these findings demonstrate that feedforward activation of sensory cortex can underlie attentional priority. |