Non-Human Primate Eye-Tracking Publications
All EyeLink eye tracker non-human primate research publications up until 2025 (with some early 2026s) are listed below by year. You can search the eye-tracking 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!
2026 |
Xin Huang; Bikalpa Ghimire; Anjani Sreeprada Chakrala; Steven Wiesner Neural coding of multiple motion speeds in visual cortical area MT Journal Article In: eLife, vol. 13, pp. 1–43, 2026. @article{Huang2026,Motion speed is a salient cue for visual segmentation, yet how the visual system represents and differentiates multiple speeds remains unclear. Here, we investigated the encoding and decoding of multiple speeds. We first characterized the perceptual capacity of human and macaque subjects to segment overlapping stimuli moving at different speeds. We then determined how neurons in area MT of macaque monkeys represent multiple speeds. We found that the responses of MT neurons to two speeds showed a robust bias toward the faster speed component. This faster-speed bias occurred when both speeds were slow (≤20°/s) and diminished as stimulus speed increased. Our findings can be explained by a modified divisive normalization model, in which the weights for the speed components are proportional to the responses of a population of neurons (the weighting pool) with a broad range of speed preferences, elicited by the individual speeds. Regarding decoding, a classifier could distinguish MT responses to two speeds from those to a corresponding log-mean speed. We further found that it was possible to decode two speeds from the MT population response, supporting the theoretical framework of coding multiplicity in neuronal populations. The decoded speeds can account for perceptual performance in segmenting two speeds with a large (4x) but not a small (2x) separation. Our findings help define the neural coding rule of multiple speeds. The faster-speed bias in MT could benefit important behavioral tasks, such as figure-ground segregation, as figural objects tend to move faster than the background in the natural environment. |
Xuefei Yu; Atul Gopal; Ken-ichi Inoue; Martin O. Bohlen; Genevieve M. Kuczewski; Marc A. Sommer; Hendrikje Nienborg; Masahiko Takada; Okihide Hikosaka Retrograde optogenetics reveals sensorimotor convergence within a corticotectal pathway of non-human primates Journal Article In: Current Biology, vol. 36, no. 1, pp. 236–242, 2026. @article{Yu2026,Understanding how the cerebral cortex communicates with subcortical areas to drive behavior remains a central question in system neuroscience. One key unresolved issue is whether prefrontal cortical outputs to motor-related subcortical regions carry predominantly motor commands1 or mixed sensory-motor signals.2,3 Retrograde optogenetics offers a powerful way to interrogate such projection-defined circuits,4–7 but its use in non-human primates has been limited.8–11 Here, we applied retrograde optogenetics in awake macaques to directly test the functional organization of the corticotectal projection from the frontal eye field (FEF) to the superior colliculus (SC). We asked whether the FEF output signals to SC are motor-dominant or broadly sensory-motor. Optical activation of this pathway evoked robust, contralateral saccades and selectively modulated reaction times, demonstrating its causal role in saccade generation. Optogenetically tagging FEF neurons pro- jecting to SC revealed a heterogeneous population of visual, visuomotor, and motor neurons. This diverse output converged predominantly onto motor-related neurons in the SC. These findings support a visuomotor convergence model, in which diverse FEF outputs drive motor-selective SC neurons with activity sufficient for saccade generation, and thus resolve long-standing questions over the composition of FEF outputs. Additionally, our results establish retrograde optogenetics as a tool for dissecting projection-defined circuits in primates and for precisely probing the neural pathways that link perception to action. |
2025 |
Yusuke Akiyama; Hiroshi Yamada; Masayuki Matsumoto; Jun Kunimatsu Sustained visual signals in the primate cerebellar dentate nucleus drive associative learning Journal Article In: Communications Biology, vol. 8, no. 1, pp. 1–12, 2025. @article{Akiyama2025,A number of studies have suggested that the cerebellum has cognitive functions; however, the underlying neuronal mechanisms remain unclear. In this study, we demonstrated that sustained visual signals in the cerebellar dentate nucleus represent the visuomotor associative information. We recorded neuronal activity from the dentate nucleus when monkeys performed a learning task involving the association between visual objects and saccade directions. We found that sustained visual activity was greater during learning than during memory retrieval. This enhancement disappeared under the uncertain reward condition, in which the monkeys did not engage in learning behavior. Furthermore, sustained visual signals changed the response to visual objects depending on the associated saccade direction. This direction selectivity was positively correlated with modulation during learning. These results suggest that sustained visual signals in the dentate nucleus reflect learning related motivation and drive learning by increasing the strength of discrimination among visual objects. |
Lukas K. Amann; Virginia Casasnovas; Alexander Gail Visual target and task-critical feedback uncertainty impair different stages of reach planning in motor cortex Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–15, 2025. @article{Amann2025,Sensory uncertainty jeopardizes accurate movement. During reaching, visual uncertainty can affect the estimation of hand position (feedback) and the desired movement endpoint (target). While impairing motor learning, it is unclear how either form of uncertainty affects cortical reach goal encoding. We show that reach trajectories vary more with higher visual uncertainty of the target, but not the feedback. Accordingly, cortical motor goal activities in male rhesus monkeys are less accurate during planning and movement initiation under target but not feedback uncertainty. Yet, when monkeys critically depend on visual feedback to conduct reaches via a brain-computer interface, then visual feedback uncertainty impairs reach accuracy and neural motor goal encoding around movement initiation. Neural state space analyses reveal a dimension that separates population activity by uncertainty level in all tested conditions. Our findings demonstrate that while both target and feedback uncertainty always reflect in neural activity, uncertain feedback only deteriorates neural reach goal information and behavior when it is task-critical, i.e., when having to rely on the sensory feedback and no other more reliable sensory modalities are available. Further, uncertain target and feedback impair reach goal encoding in a time-dependent manner, suggesting that they are integrated during different stages of reach planning. |
Esmaeil Farhang; Ramin Toosi; Behnam Karami; Roxana Koushki; Narges Kheirkhah; Farideh Shakerian; Jalaledin Noroozi; Ehsan Rezayat; Abdol Hossein Vahabie; Mohammad Reza A. Dehaqani The impact of spatial frequency on hierarchical category representation in macaque temporal cortex Journal Article In: Communications Biology, vol. 8, no. 1, pp. 1–15, 2025. @article{Farhang2025,Objects are recognized in three hierarchical levels: superordinate, mid-level, and subordinate. Psychophysics shows that mid-level categories and low spatial frequency (LSF) information are rapidly recognized. However, the interaction between spatial frequency (SF) and abstraction is not well understood. To address this, we examine neural responses in the inferior temporal cortex and superior temporal sulcus of two male macaque monkeys. Our findings reveal that mid-level categories are well represented at both LSF and high SF (HSF), suggesting robust mid-level boundary maps in these areas, unaffected by SF changes. Conversely, superordinate category representation depends on HSF, indicating its crucial role in encoding global category information. The absence of subordinate representation in both LSF and HSF compared to intact stimuli further implies that full SF content is essential for fine-category processing. A supporting human psychophysics task confirms that superordinate categorization relies on HSF, while subordinate object recognition requires both LSF and HSF. |
Tingting Feng; Yun Zhang; Wenhao Han; Xiaoling Luo; Yifei Han; Wenjie Wei; Hong Qu; Shenbing Kuang; Tao Zhang; Yi Zhang Hierarchical and distinct biological motion processing in macaque visual cortical areas MT and MST Journal Article In: Communications Biology, vol. 8, no. 1, pp. 1–14, 2025. @article{Feng2025,It is widely accepted that biological motion (BM) perception involves the posterior superior temporal sulcus (pSTS). Yet, how individual neurons and neural circuits in pSTS encode BM remains unclear. Here we combined electrophysiological recordings with neural network modeling to elucidate BM computations in two subregions of pSTS. We recorded single-cell activity from the middle temporal area (MT) and the medial superior temporal area (MST) of three macaque monkeys when they viewed point-light displays portraying BM walking in different directions (left vs. right), orientations (upright vs. inverted), and forms (intact vs. scrambled). We found that, while individual neurons in both MT and MST showed selectivity for these features, neural populations in MST but not MT exhibit BM-specific encoding, i.e., preferential representation of intact upright BM—the defining characteristic of BM recognition. A neural network model trained to replicate these neurophysiological findings implicated that, BM-specific encoding in MST may arise from feedforward connectivity patterns, i.e., MT subpopulations selective for linear translational motion and nonlinear optic flow projected preferentially to distinct MST cells. Taken together, our findings highlight hierarchical and distinct BM processing in MT and MST, advancing our understanding of BM computations in pSTS at the single-cell and neural circuit levels in the primate brain. |
Whitney S. Griggs; Sumner L. Norman; Mickael Tanter; Charles Liu; Vasileios Christopoulos; Mikhail G. Shapiro; Richard A. Andersen Functional ultrasound neuroimaging reveals mesoscopic organization of saccades in the lateral intraparietal area Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–19, 2025. @article{Griggs2025,The lateral intraparietal cortex (LIP), contained within the posterior parietal cortex (PPC), is crucial for transforming spatial information into saccadic eye movements, yet its functional organization for movement direction remains unclear. Here, we used functional ultrasound imaging (fUSI), a technique with high sensitivity, large spatial coverage, and good spatial resolution, to map movement direction encoding across the PPC by recording local changes in cerebral blood volume within PPC as two male monkeys performed memory-guided saccades. Our analysis revealed a heterogeneous organization where small patches of neighboring LIP cortex encoded different directions. These subregions demonstrated consistent tuning across several months to years. A rough topography emerged where anterior LIP represented more contralateral downward movements and posterior LIP represented more contralateral upward movements. These results address two fundamental gaps in our understanding of LIP's functional organization: the neighborhood organization of patches and the stability of these populations across long periods of time. By tracking LIP populations over extended periods, we developed mesoscopic maps of direction specificity previously unattainable with fMRI or electrophysiology methods. |
Seyed-Reza Hashemirad; Mojtaba Abbaszadeh; Ali Ghazizadeh Prefrontal cortex temporally multiplexes slow and fast dynamics in value learning and memory Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–17, 2025. @article{Hashemirad2025,Seyed-Reza Hashemirad 1,Mojtaba Abbaszadeh 1 & Ali Ghazizadeh 2 Balancing stability and flexibility is a fundamental challenge in value-based learning: how does the brain maintain long-term value memories while adapting to new environmental contingencies? To address this, we propose a reinforcement learning model composed of two distinct processes with fast and slow dynamics for updating and forgetting object values. Using a combined theoretical and experimental approach in male macaque monkeys, we validate a key behavioral prediction of this two-rate system—spontaneous recovery of prior value memories following value reversal. At the neural level, we show that single neurons in the ventrolateral prefrontal cortex (vlPFC) temporally multiplex these dynamics, with distinct firing components reflecting fast and slow learning processes. Together, these findings suggest that reward learning and memory are supported by a two-rate system that enables both flexibility and stability, and identify the vlPFC as a critical neural substrate for this mechanism. Foods, |
Maryam Nouri Kadijani; Theda Backen; Kaustubh Manchanda; Sandeep K. Mody; Stefan Treue; Julio C. Martinez-Trujillo Bilateral field advantage of spatial attention in macaque lateral prefrontal cortex Journal Article In: Journal of Cognitive Neuroscience, vol. 37, no. 12, pp. 2430–2444, 2025. @article{Kadijani2025,Allocating visual attention to behaviorally relevant stimuli is easier when distractors are in the opposite visual hemifield relative to when they are in the same hemifield. The neural mechanisms underlying this bilateral field advantage remains unclear. We documented this effect in two macaques performing a covert spatial attention task in two different conditions: when the target and distracter were positioned in different hemifields (across condition), and when they were positioned on the top and bottom quadrants within the same visual hemifield (within condition). The animals' behavioral performance at detecting a change in the attended stimulus was higher in the across relative to the within condition. We recorded the responses of lateral prefrontal cortex (LPFC, area 8A) neurons in one animal. The proportion of LPFC neurons encoding the allocation of attention was larger in the across relative to the within condition. The latter was accompanied by an increase in the ability of single neurons to discriminate the allocation of attention in the across relative to the within condition. Finally, we used linear classifiers to decode the allocation of attention from the activity of neuronal ensembles and found a similar bilateral field advantage in decoding performance in the across relative to the within condition that generalized to different integration time windows and number of neurons used by the classifier. Our finding provides a neural correlate of the bilateral field advantage reported in behavioral studies of attention and suggest a role of the LPFC circuitry in its origin. |
Siwei Li; Jingwen Chen; Cong Zhang; Shiming Tang; Yang Xie; Liping Wang Flexible use of limited resources for sequence working memory in macaque prefrontal cortex Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–18, 2025. @article{Li2025m,Our brain is remarkably limited in how many items it can hold simultaneously, but it can also represent unbounded novel items through generalization. How the brain rationally uses limited resources in working memory (WM) remains unexplored. We investigated mechanisms of WM resource allocation using calcium imaging and electrophysiological recording in the prefrontal cortex of monkeys performing sequence WM (SWM) tasks. We found that changes in the neural representation of SWM, including geometry, generalizable and separate rank subspaces, reflected WM load. SWM resources, represented by neurons' signal strength and spatial tuning projected onto each rank subspace, were shared flexibly between ranks. Crucially, the prefrontal cortex dynamically utilized shared tuning neurons to ensure generalization, while engaging disjoint and spatially shifted neurons to minimize interference, thus achieving a trade-off between behavioral and neural costs within capacity. The allocated resources can predict monkeys' behavior. Thus, the geometry of compositionality underlies the flexible use of limited resources in SWM. |
Surpiya Murali; Beshoy Agayby; Michael C. Schmid; Barbara F. Händel Multiunit and oscillatory activity in macaque V1 is modulated by blinking in a context-dependent way Journal Article In: Cerebral Cortex, vol. 35, no. 12, pp. 1–14, 2025. @article{Murali2025,Eye blinks modulate neural activity in visual areas even if the visual input is unchanged. Is the influence of blinking defined by the motor output of the blink? We analyzed blink-related neural activity with laminar resolution in V1 of two macaque monkeys in two conditions, viewing a video and at rest. During free viewing a video, blinks induced a modulation of the local field potential (LFP) in the theta, beta, and gamma band with a granular/infragranular focus. The multiunit activity (MUA) decreased around blink execution. Surprisingly, when comparing the results to blinks executed during the rest condition, we found that MUA increased around blinks. The blink-related LFP power changes, while increasing after a blink in both conditions, were significantly different in amplitude and latency. Our findings show that the blink induced modulation of V1 activity is not determined by the motor execution but depends on the condition in which the movement is executed. This suggests that interactions between movement and neural processes in sensory areas are context-dependent. These interactions may play an important role in predictive coding within the framework of active sensing. |
Sorin Pojoga; Ariana Andrei; Valentin Dragoi Unsupervised learning of temporal regularities in visual cortical populations Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–12, 2025. @article{Pojoga2025,The brain's ability to extract temporal information from dynamic stimuli in the environment is essential for everyday behavior. To extract temporal statistical regularities, neural circuits must possess the ability to measure, produce, and anticipate sensory events. Here we report that when neural populations in macaque primary visual cortex are triggered to exhibit a periodic response to a repetitive sequence of optogenetic laser flashes, they learn to accurately reproduce the temporal sequence even when light stimulation is turned off. Despite the fact that individual cells had a poor capacity to extract temporal information, the population of neurons reproduced the periodic sequence in a temporally precise manner. The same neural population could learn different frequencies of external stimulation, and the ability to extract temporal information was found in all cortical layers. These results demonstrate a remarkable ability of sensory cortical populations to extract and reproduce complex temporal structure from unsupervised external stimulation even when stimuli are perceptually irrelevant. |
Rajani Raman; Anna Bognár; Ghazaleh Ghamkhari Nejad; Albert Mukovskiy; Lucas Martini; Martin Giese; Rufin Vogels Keypoint-based modeling reveals fine-grained body pose tuning in superior temporal sulcus neurons Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–16, 2025. @article{Raman2025,Body pose and orientation serve as vital visual signals in primate non-verbal social communication. Leveraging deep learning algorithms that extract body poses from videos of behaving monkeys, applied to a monkey avatar, we investigated neural tuning for pose and viewpoint, targeting fMRI-defined mid and anterior Superior Temporal Sulcus (STS) body patches. We modeled the pose and viewpoint selectivity of the units with keypoint-based principal component regression with cross-validation and applied model inversion as a key approach to identify effective body parts and views. Mid STS units were effectively modeled using view-dependent 2D keypoint representations, revealing that their responses were driven by specific body parts that differed among neurons. Some anterior STS units exhibited better predictive performances with a view-dependent 3D model. On average, anterior STS units were better fitted by a keypoint-based model incorporating mirror-symmetric viewpoint tuning than by view-dependent 2D and 3D keypoint models. However, in both regions, a view-independent keypoint model resulted in worse predictive performance. This keypoint-based approach provides insights into how the primate visual system encodes socially relevant body cues, deepening our understanding of body pose representation in the STS. |
Dixit Sharma; Bart Krekelberg Predicting spiking activity from scalp EEG Journal Article In: Journal of Neural Engineering, vol. 22, no. 6, pp. 1–16, 2025. @article{Sharma2025,Objective. Despite decades of electroencephalography (EEG) research, the relationship between EEG and underlying spiking dynamics remains unclear. This limits our ability to infer neural dynamics reflected in intracranial signals from EEG, a critical step to bridge electrophysiological findings across species and to develop non-invasive brain–machine interfaces (BMIs). In this study, we aimed to estimate spiking activity in the visual cortex using non-invasive scalp EEG. Approach . We recorded spiking activity from a 32-channel floating microarray permanently implanted in parafoveal V1 and scalp-EEG in a male macaque monkey. While the animal fixated, the screen flickered at different temporal frequencies to induce steady-state visual evoked potentials. We analyzed the relationship between the V1 multi-unit spiking activity envelope (MUAe) and EEG frequency bands to predict MUAe at each time point from EEG. We extracted instantaneous spectrotemporal features of the EEG signal, including phase, amplitude, and phase-amplitude coupling of its frequency bands. Main results . Although the relationship between these spectrotemporal features and the V1 MUAe was complex and frequency-dependent, they were reliably predictive of the MUAe. Specifically, in a linear regression predicting MUAe from EEG, each EEG feature (phase, amplitude, coupling) contributed to model predictions. In addition, we found that MUAe predictions were better in shallow than deep cortical layers, and that the phase of stimulus frequency further improved MUAe predictions. Significance. Our study shows that a comprehensive account of spectrotemporal features of non-invasive EEG provides information on underlying spiking activity beyond what is available when only the amplitude or phase of the EEG signal is considered. This demonstrates the richness of the EEG signal and its complex relationship with neural spiking activity and suggests that using more comprehensive spectrotemporal signatures could improve BMI applications. |
Ramanujan Srinath; Amy M. Ni; Claire Marucci; Marlene R. Cohen; David H. Brainard Orthogonal neural representations support perceptual judgments of natural stimuli Journal Article In: Scientific Reports, vol. 15, no. 1, pp. 1–17, 2025. @article{Srinath2025a,In natural visually guided 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 blank backgrounds. Natural images, however, contain task-irrelevant background elements that might interfere with the perception of object features. Recent studies suggest that visual feature estimation can be modeled through the linear decoding of task-relevant information from visual cortex. So, if the representations of task-relevant and irrelevant features are not orthogonal in the neural population, then variation in the task-irrelevant features would impair task performance. We tested this hypothesis using human psychophysics and monkey neurophysiology combined with parametrically variable naturalistic stimuli. We demonstrate that (1) the neural representation of one feature (the position of an 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 those background features, and (3) many features of the object and the background (and of objects from a separate stimulus set) are orthogonally represented in V4 neural population responses. Our observations are consistent with the hypothesis that orthogonal neural representations can support stable perception of object features despite the richness of natural visual scenes. |
Zhao Zeng; Ce Zhang; Yue Xu; Hua He; Yong Gu Distinct neural population code and causal roles of primate caudate nucleus in multimodal decision-making Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–16, 2025. @article{Zeng2025b,Perceptual decision-making involves distributed networks spanning both association cortices and subcortical areas. A fundamental question is whether such a network is highly redundant, or each node is distinct with unique function. Using a visuo-vestibular decision-making task, here we show the subcortical caudate nucleus (CN) of male primates displays distinct population code compared to association cortices along the modality dimension. Specifically, in a low-dimensional state subspace, neural trajectory in the frontal and posterior-parietal association cortical activity during multimodal-stimulus condition evolves along the visual trajectory, whereas along the vestibular trajectory in the CN. We then show CN population activity is consistent with the animal's behavioral strategy employed within a generalized drift-diffusion framework. Importantly, causal-link experiments, including application of GABAa-receptor agonist, D1-receptor antagonist, and electrical microstimulation, further confirmed CN's critical contributions to perceptual behavior. Our results confirm CN's vital importance to decision making in complex environments with multimodal information. |
Cong Zheng; Qifan Wang; He Cui Continuous sensorimotor transformation enhances robustness of neural dynamics to perturbation in macaque motor cortex Journal Article In: Nature Communications, vol. 16, no. 1, pp. 1–17, 2025. @article{Zheng2025a,Neural activity in the motor cortex evolves dynamically to prepare and generate movement. Here, we investigate how motor cortical dynamics adapt to dynamic environments and whether these adaptations influence robustness against disruptions. We apply intracortical microstimulation (ICMS) in the motor cortex of monkeys performing delayed center-out reaches to either a static target (static) or a rotating target (moving) that required interception. While ICMS prolongs reaction times (RTs) in the static condition, it does not increase RTs in the moving condition, correlating with faster recovery of neural population activity post-perturbation. Neural dynamics suggests that the moving condition involves ongoing sensorimotor transformations during the delay period, whereas motor planning in the static condition is completed shortly. A neural network model shows that continuous feedback input rapidly corrects perturbation-induced errors in the moving condition. We conclude that continuous sensorimotor transformations enhance the motor cortex's resilience to perturbations, facilitating timely movement execution. |
Hamidreza Abdoljabbari; Fatemeh Balapour; Scott L. Brincat; Constantin Nicolai; Markus Siegel; Earl K. Miller; Mohammad Reza Daliri Neuron-type-specific contributions to dynamic coding during flexible sensorimotor decisions in frontoparietal cortex Journal Article In: Journal of Cognitive Neuroscience, vol. 37, no. 11, pp. 2295–2312, 2025. @article{Abdoljabbari2025,Neocortical circuits consist of multiple neuronal cell types, each likely playing distinct roles in flexible behavior. However, studies of decision-making have often overlooked these cell types, limiting our understanding of their specific contributions to local circuit functions. To address this, we simultaneously recorded neuronal activity from the frontal eye field (FEF), lateral PFC, and lateral intraparietal area (LIP) in a macaque monkey performing a visuomotor decision-making task. We used extracellular spike waveforms to reliably identify two functional classes of neurons: broad-spiking (BS) putative pyramidal cells and narrow-spiking (NS) putative interneurons. These cell types exhibited distinct response dynamics and choice-related information encoding across cortical regions. NS neurons in LIP and PFC showed higher choice-related activity and contributed to early encoding of decisions, whereas in FEF, NS neurons demonstrated dynamic encoding patterns, with BS neurons exhibiting significantly more stable encoding. Our findings reveal that choice information is represented differently across cell types and cortical regions, with NS neurons favoring early population coding in PFC and LIP and BS neurons exhibiting more static encoding in FEF. This heterogeneous coding strategy suggests that decision-related dynamics in the frontoparietal network are shaped by interactions between these distinct neuronal populations. The results provide new insights into cortical circuit dynamics and cell-type-specific contributions to decision-making. |
Anna Bognár; Ghazaleh Ghamkhari Nejad; Rufin Vogels Effects of partial occlusion on response dynamics and interregional processing within primate superior temporal sulcus Journal Article In: The Journal of Neuroscience, vol. 45, no. 47, pp. 1–15, 2025. @article{Bognar2025,Recognizing partially occluded objects is a critical visual function that primates perform with ease, yet the underlying neural mechanisms remain incompletely understood. Previous studies in the macaque inferotemporal cortex have reported mixed results on whether occlusion delays and reduces responses to partially occluded objects. To address this, we recorded single-unit activity from body-responsive regions of the middle and anterior superior temporal sulcus (STS) in male macaques while presenting body stimuli with varying levels of occlusion using a dot pattern. Occlusion reduced response strength and increased onset latency in both regions, and even low occlusion levels altered response dynamics by increasing the difference between the response trough and second peak. While body selectivity was preserved, body decoding accuracy declined and was delayed as occlusion increased. In contrast to some prior reports, we found no consistent enhancement of body decoding during the late response phase. By controlling for information loss and clutter introduced by the occluder, we found that reductions in response strength were partly due to the deletion of body features, whereas changes in response dynamics primarily reflected interactions between the occluder and the remaining body features. Occlusion delayed the first but not the second response peak, suggesting distinct mechanisms for these phases. Peak decoding at high occlusion levels emerged later in anterior than middle STS, indicating a feedforward component. However, representational similarity analysis combined with Granger causality suggested enhanced feedback from anterior to middle STS under high occlusion. Together, these results highlight the response dynamics supporting robust recognition under occlusion. |
Jon S. Guez; Bart Krekelberg Preemptive gain control in primary visual cortex Journal Article In: Current Biology, vol. 35, no. 21, pp. 5230–5237, 2025. @article{Guez2025,Neurons continuously adapt their response properties to their environment. In the visual cortex, this includes gain control processes such as contrast normalization, which matches neurons' limited dynamic response range to the prevailing contrasts. Contrast normalization converges to a state that is optimal for processing the current visual input but not for the new, unknown input that impinges on the retina after each eye movement. We hypothesized that this conflict between current (pre-saccadic) and future (post-saccadic) needs could be resolved by a preemptive reset of the contrast response function with every saccade. We investigated this hypothesis using multi-electrode array recordings in the primary visual cortex of the macaque monkey. As expected, exposure to high contrast during steady fixation led to reduced gain and a compressed contrast response function. In support of our preemptive gain control hypothesis, these gain changes were partially reversed during saccades, resulting in a contrast response function with a higher gain and a broader, more linear response range. Post-saccadic gain increases were accompanied by pre-saccadic gain decreases, which were anticorrelated, suggesting that a common mechanism underlies both changes. Our findings indicate that the ubiquitous biphasic peri-saccadic neural response is a signature of a pause-rebound mechanism that prepares for unknown future visual inputs by resetting the contrast response function. At the perceptual level, this leads us to reinterpret the pre-saccadic reduction in visual sensitivity (i.e., saccadic suppression) as a side effect of the beneficial signal-processing strategy of preemptive gain control. |
Matthew B. Broschard; Jefferson E. Roy; Scott L. Brincat; Meredith K. Mahnke; Earl K. Miller Evidence for an active handoff between hemispheres during target tracking Journal Article In: The Journal of Neuroscience, vol. 45, no. 44, pp. 1–11, 2025. @article{Broschard2025,The brain has somewhat separate cognitive resources for the left and right sides of our visual field. Despite this lateralization, we have a smooth and unified perception of our environment. This raises the question of how the cerebral hemispheres are coordinated to transfer information between them. We recorded neural activity in the lateral prefrontal cortex, bilaterally, as two male nonhuman primates covertly tracked a target that moved from one visual hemifield (i.e., from one hemisphere) to the other. Beta (15-30 Hz) power, gamma (30-80 Hz) power, and spiking information reflected sensory processing of the target. In contrast, alpha (10-15 Hz) power, theta (4-10 Hz) power, and spiking information seemed to reflect an active handoff of attention as target information was transferred between hemispheres. Specifically, alpha power and spiking information ramped up in anticipation of the hemifield cross. Theta power peaked after the cross, signaling its completion. Our results support an active handoff of information between hemispheres. This "handshaking" operation may be critical for minimizing information loss, much like how mobile towers handshake when transferring calls between them. |
Joanita F. D'souza; Jessima M. Rich; Shaun L. Cloherty; Nicholas S. C. Price; Maureen A. Hagan Topographic organization of saccade-related response field properties in the marmoset posterior parietal cortex Journal Article In: eNeuro, vol. 12, no. 10, pp. 1–12, 2025. @article{Dsouza2025,Despite various histological, electrophysiological, and imaging studies, the topographic organization of saccade-related activity in the posterior parietal cortex (PPC) has been notoriously difficult to characterize. In part, this is because areas of interest in PPC are often embedded deep in sulci in macaques and humans. Understanding the extent of topographic organization in PPC can provide insights into the computation contributions of PPC. The lissencephalic cortex of the common marmoset offers a unique opportunity to investigate fine-scale topographic organization in PPC. Recordings were obtained from the PPC of two male marmosets performing a visually guided center-out saccade task with 8 or 36 peripheral targets using multichannel electrode arrays with 100 μm spacing. By plotting the pattern of saccade direction tuning preferences across all penetrations and cortical depths, we uncovered topographic organizational features within the PPC. Like other primates, multiunits in marmoset PPC tend to prefer saccade targets in the contralateral visual field. The results detail how preference for saccadic direction changes in a systematic manner across cortical distance, such that response units closer in proximity tend to show systematic changes in their tuning preferences. Across cortical distance, the visual field was also systematically encoded but reversals in direction varied across penetrations. The analysis highlights the likelihood of multiple representations of the visual field for saccade direction preference across PPC. These novel findings suggest a possible functional organization of saccade-related activity in marmoset PPC, giving insights into the computational capacity of the PPC. |
Shrabasti Jana; Lucio Condro; Frédéric V. Barthélemy; Junji Ito; Alexa Riehle; Sonja Grün; Thomas Brochier Energy constraints determine the selection of reaching movement trajectories in macaque monkeys Journal Article In: eNeuro, vol. 12, no. 10, pp. 1–16, 2025. @article{Jana2025,Reaching movements, while seemingly simple, involve complex motor control mechanisms that select specific trajectories from infinite possibilities. Despite inherent variability in volitional movements, both humans and monkeys frequently exhibit stereotyped trajectories. The literature has offered numerous explanations for invariant trajectory shapes, including a common planning space in hand space or joint space, as well as factors like kinetic energy (KE) minimization and sensory feedback. However, since most studies have relied on single-session data, crucial insights into the motor principles guiding trajectory selection and their evolution through extended practice remain underexplored. This study fills this gap by investigating how specific trajectories are selected and evolve with practice across multiple sessions, using data from two rhesus monkeys (one male, one female) performing a reaching task in a biomechanically constrained 2D setup. Our behavioral study challenges the idea of a common planning space, revealing instead a significant influence of KE on trajectory shapes. Through a novel biomechanical modeling, we quantified KE for a wide range of trajectory shapes. We discovered that trajectory selection and evolution are not simply about minimizing KE or achieving straight paths. Instead, the monkeys' motor systems appear to prioritize maintaining a “safe KE range,” where slight changes in trajectory shapes have minimal impact on energy expenditure. These findings provide new insights into the adaptive motor control strategies, suggesting that trajectory selection involves balancing energy efficiency and flexibility. Our study enhances the understanding of trajectory selection principles, with implications for rehabilitation strategies, robotics, and broader study of motor control mechanisms. |
Pooya Laamerad; Matthew R. Krause; Daniel Guitton; Christopher C. Pack Inactivation of primate cortex reveals inductive biases in visual learning Journal Article In: Current Biology, vol. 35, no. 19, pp. 4699–4713, 2025. @article{Laamerad2025,Humans and other primates are capable of learning to recognize new visual stimuli throughout their lifetimes. Most theoretical models assume that such learning occurs through the adjustment of the large number of synaptic weights connecting the visual cortex to downstream decision-making areas. While this approach to learning can optimize performance on behavioral tasks, it can also be costly in terms of time and energy. An alternative hypothesis is that the brain favors simpler learning rules that do not necessarily optimize the readout of information from visual cortical neurons. Here, we have examined these hypotheses by reversibly inactivating visual area V4 in non-human primates at different stages of training on form discrimination tasks. We find that V4 inactivation generally has a behavioral effect for only a subset of the stimuli that are encoded in the V4 population activity, specifically those that can be represented efficiently in the population firing rate. As a result, neural measures of discriminability do not necessarily predict the causal contribution of V4 neurons to task performance. This pattern of results can be explained by incorporating a strong inductive bias for simpler perceptual readouts into existing theoretical frameworks. Such a simplicity bias is suboptimal in the sense that it ignores information that could theoretically be extracted from the neural population, but it has the likely advantage of facilitating efficient learning on ecologically relevant timescales. |
Frank F. Lanfranchi; Joseph Wekselblatt; Daniel A. Wagenaar; Doris Y. Tsao A compressed hierarchy for visual form processing in the tree shrew Journal Article In: Nature, vol. 646, no. 8086, pp. 872–882, 2025. @article{Lanfranchi2025,Our knowledge of the brain processes that govern vision is largely derived from studying primates, whose hierarchically organized visual system1 inspired the architecture of deep neural networks2. This raises questions about the universality of such hierarchical structures. Here we examined the large-scale functional organization for vision in one of the closest living relatives to primates, the tree shrew. We performed Neuropixels recordings3,4 across many cortical and thalamic areas spanning the tree shrew ventral visual system while presenting a large battery of visual stimuli in awake tree shrews. We found that receptive field size, response latency and selectivity for naturalistic textures, compared with spectrally matched noise5, all increased moving anteriorly along the tree shrew visual pathway, consistent with a primate-like hierarchical organization6,7. However, tree shrew area V2 already harboured a high-level representation of complex objects. First, V2 encoded a complete representation of a high-level object space8. Second, V2 activity supported the most accurate object decoding and reconstruction among all tree shrew visual areas. In fact, object decoding accuracy from tree shrew V2 was comparable to that in macaque posterior IT and substantially higher than that in macaque V2. Finally, starting in V2, we found strongly face-selective cells resembling those reported in macaque inferotemporal cortex9. Overall, these findings show how core computational principles of visual form processing found in primates are conserved, yet hierarchically compressed, in a small but highly visual mammal. |
Enrico Ferrea; Pierre Morel; Alexander Gail Frontal and parietal planning signals encode adapted motor commands when learning to control a brain-computer interface Journal Article In: PLoS Biology, vol. 23, no. 9, pp. 1–28, 2025. @article{Ferrea2025,Perturbing visual feedback is a powerful tool for studying visuomotor adaptation. However, unperturbed proprioceptive signals in common paradigms inherently co-varies with physical movements and causes incongruency with the visual input. This can create challenges when interpreting underlying neurophysiological mechanisms. We employed a brain-computer interface (BCI) in rhesus monkeys to investigate spatial encoding in frontal and parietal areas during a 3D visuomotor rotation task where only visual feedback was movement-contingent. We found that both brain regions better reflected the adapted motor commands than the perturbed visual feedback during movement preparation and execution. This adaptive response was observed in both local and remote neurons, even when they did not directly contribute to the BCI input signals. The transfer of adaptive changes in planning activity to corresponding movement corrections was stronger in the frontal than in the parietal cortex. Our results suggest an integrated large-scale visuomotor adaptation mechanism in a motor-reference frame spanning across frontoparietal cortices. |
Olivia C. Meisner; Olga Dal Monte; Nicholas Fagan; Anirvan S. Nandy; Steve W. C. Chang Oxytocin in the amygdala sustains prosocial behavior via state-dependent amygdala–prefrontal modulation Journal Article In: Journal of Neuroscience, vol. 45, no. 36, pp. 1–14, 2025. @article{Meisner2025,Prosocial behaviors are crucial for maintaining primates' complex social relationships. As central regions involved in social decision-making, the basolateral amygdala (BLA) processes social salience and value, while the gyrus of the anterior cingulate cortex (ACCg) integrates social information to guide decision-making. Oxytocin, a key modulator of social behavior, can influence both prosocial behavior and neural activity in these regions, but the precise mechanisms remain unclear. We investigated oxytocin's effects on prosocial behavior and neural activity by infusing oxytocin or saline into the BLA (Oxt-BLA, Sal-BLA) and examining the effects of Oxt-BLA on prosocial decisions, BLA and ACCg neural activity, and the coordination between the two regions in male rhesus macaques. We found that Oxt-BLA's behavioral effects were state-dependent: during high prosocial states, it sustained prosocial choices and task engagement, counteracting the natural decline seen in the control condition. However, during low prosocial states, Oxt-BLA had minimal behavioral effects. At the neural level, Oxt-BLA enhanced BLA and ACCg activity for prosocial choices only during high prosocial states. Importantly, Oxt-BLA maintained stable BLA–ACCg coordination during high prosocial states, preventing the decline in communication observed in control conditions. These findings demonstrate that oxytocin's ability to sustain prosocial behavior depends on social motivational state. These results support that oxytocin processing in the BLA acts as a state-dependent neuromodulator that enhances BLA and ACCg neural responses and maintains BLA–ACCg communication to guide prosocial decisions. |
Yichen Qian; Roger Herikstad; Camilo Libedinsky Working memory updating in the macaque lateral prefrontal cortex Journal Article In: Journal of Neuroscience, vol. 45, no. 37, pp. 1–10, 2025. @article{Qian2025a,Working memory updating is an important executive process. Here, we study the single-neuron mechanisms involved in updating versus protecting memory from distractors in the macaque prefrontal cortex. We recorded single-neuron activity from the lateral prefrontal cortex (LPFC) and prearcuate cortex (PAC) while male monkeys performed a task that required them to update their memory of target locations while ignoring distractors. Our findings revealed that neurons in the PAC signaled updated memory locations ∼100 ms after stimulus onset, significantly faster than the ∼400 ms observed in the LPFC. Additionally, PAC neurons exhibited longer encoding of distractor information. Population decoding analyses further indicated that distractor information was maintained in orthogonal subspaces from target information in both regions, minimizing interference. These results demonstrate the distinct temporal dynamics in memory updating processes between the PAC and LPFC and highlight the interplay between robust memory maintenance and updating, suggesting that local neural mechanisms may contribute to these processes. |
Joana Soldado-Magraner; Yuki Minai; Byron M. Yu; Matthew A. Smith Robustness of working memory to prefrontal cortex microstimulation Journal Article In: The Journal of Neuroscience, vol. 45, no. 37, pp. 1–15, 2025. @article{Soldado-Magraner2025,Delay period activity in the dorsolateral prefrontal cortex (dlPFC) has been linked to the maintenance and control of sensory information in working memory. The stability of working memory-related signals found in such delay period activity is believed to support robust memory-guided behavior during sensory perturbations, such as distractors. Here, we directly probed dlPFC's delay period activity with a diverse set of activity perturbations and measured their consequences on neural activity and behavior. We applied patterned microstimulation to the dlPFC of two male rhesus macaques implanted with multielectrode arrays by electrically stimulating different electrodes in the array while they performed a memory-guided saccade task. We found that the microstimulation perturbations affected spatial working memory-related signals in individual dlPFC neurons. However, task performance remained largely unaffected. These apparently contradictory observations could be understood by examining different dimensions of the dlPFC population activity. In dimensions where working memory-related signals naturally evolved over time, microstimulation impacted neural activity. In contrast, in dimensions containing working memory-related signals that were stable over time, microstimulation minimally impacted neural activity. This dissociation could explain how working memory-related information may be stably maintained in dlPFC despite the activity changes induced by microstimulation. Thus, working memory processes are robust to a variety of activity perturbations in the dlPFC. |
Ramin Toosi; Behnam Karami; Roxana Koushki; Farideh Shakerian; Jalaledin Noroozi; Ehsan Rezayat; Abdol-Hossein Vahabie; Mohammad Ali Akhaee; Mohammad-Reza A. Dehaqani The spatial frequency representation predicts category coding in the inferior temporal cortex Journal Article In: eLife, vol. 13, pp. 1–28, 2025. @article{Toosi2025,Understanding the neural representation of spatial frequency (SF) in the primate cortex is vital for unraveling visual processing in object recognition. While many studies focus on SF in the primary visual cortex, the characteristics and interaction of SF with category representation remain unclear. To explore SF representation in the inferior temporal (IT) cortex of macaques, we conducted extracellular recordings with complex stimuli systematically filtered by SF. Our findings reveal explicit SF coding at both single-neuron and population levels. Temporal dynamics analysis of SF representation reveals that low SF (LSF) is decoded faster than high SF (HSF), and the SF preference dynamically shifts from LSF to HSF over time. Additionally, the SF representation for each neuron forms a profile that predicts category selectivity at the population level. IT neurons cluster into four groups based on SF preference, each with distinct category coding behaviors. Notably, HSF-preferring neurons show the highest category decoding for faces. Despite the existing connection between SF and category coding, we have identified uncorrelated representations of SF and category. Unlike category coding, SF is more sparsely represented and depends more on individual neurons. These findings dissociate SF and category representations, underscoring SF's pivotal role in object recognition. |
Xuanyu Wu; Yang Zhou Nonlinear feedback modulation contributes to the optimization of flexible decision-making Journal Article In: eLife, vol. 13, pp. 1–25, 2025. @article{Wu2025a,Neural activity in the primate brain correlates with both sensory evaluation and action selection aspects of decision-making. However, the intricate interaction between these distinct neural processes and their impact on decision behaviors remains unexplored. Here, we examined the interplay of these decision processes in posterior parietal cortex (PPC) when monkeys performed a flexible decision task. We found that the PPC activity related to monkeys' abstract decisions about visual stimuli was nonlinearly modulated by monkeys' following saccade choices directed outside each neuron's response field. Recurrent neural network modeling indicated that the feedback connections, matching the learned stimuli-response associations during the task, might mediate such feedback modulation. Further analysis on network dynamics revealed that selectivity-specific feedback connectivity intensified the attractor basins of population activity underlying saccade choices, thereby increasing the reliability of flexible decisions. These results highlight an iterative computation between different decision processes, mediated primarily by precise feedback connectivity, contributing to the optimization of flexible decision-making. |
Bingyu Liu; Qingyang Luo; Zhifeng Liang; Hua He; Yong Gu Robust single-trial decoding of physical self-motion from hemodynamic signals in the brain measured by functional ultrasound imaging Journal Article In: PNAS, vol. 122, no. 29, pp. 1–12, 2025. @article{Liu2025e,Physical self-motion frequently happens in daily life, during which our vestibular system is critical in various important functions including balance and visual stability maintenance, postural and motor control, locomotion, spatial perception, and path integration-based navigation. Conventional noninvasive methods for studying vestibular functions include functional MRI (fMRI) that conveniently measures brain-wide signals; however, subjects are required to be physically restricted in the scanner. In such cases, caloric or galvanic vestibular stimulation is applied to stimulate peripheral vestibular organs, suffering a loss of precise stimulation of peripheral vestibular organs as during physical motion conditions. In this study, we adopted functional ultrasound (fUS) imaging, a newly emerging minimally invasive technique with high spatiotemporal resolution, to measure vestibular related signals in primates under passive, physical self-motion conditions that selectively activate vestibular organs. We found that robust fUS signals were evoked in brain-wide regions. While many areas overlapped with those previously reported by fMRI or electrophysiology, significant activations were also seen in areas that were not clearly identified previously including area 5, 1-2, M1, V3A, and 7 m. Importantly, using a linear discriminant analysis algorithm, physical self-motion information, including both translation directions, and translation-vs.-rotation, could be reliably decoded from fUS signals on a single-trial basis. In addition to vestibular-related activity, many areas also exhibited visual-motion response, indicating possible multisensory interactions. Our findings suggest that fUS imaging holds a promising tool for studying vestibular functions in tasks under physical self-motion conditions, as well as interactions with visual or motor systems. |
Atsushi Yoshida; Okihide Hikosaka Contribution of glutamatergic projections to neurons in the nonhuman primate substantia nigra pars reticulata for reactive inhibition Journal Article In: PNAS, vol. 122, no. 26, pp. 1–11, 2025. @article{Yoshida2025,The basal ganglia play a crucial role in action selection by facilitating desired movements and suppressing unwanted ones. The substantia nigra pars reticulata (SNr), a key output nucleus, facilitates movement through disinhibition of the superior colliculus (SC). However, its role in action suppression, particularly in primates, remains less clear. We investigated whether individual SNr neurons in three male macaque monkeys bidirectionally modulate their activity to both facilitate and suppress actions and examined the role of glutamatergic inputs in suppression. Monkeys performed a sequential choice task, selecting or rejecting visually presented targets. Electrophysiological recordings showed that SNr neurons decreased firing rates during target selection and increased firing rates during rejection, demonstrating bidirectional modulation. Pharmacological blockade of glutamatergic inputs to the lateral SNr disrupted saccadic control and impaired suppression of reflexive saccades, providing causal evidence for the role of excitatory input in behavioral inhibition. These findings suggest that glutamatergic projections, potentially originating from sources including the subthalamic nucleus, contribute to the increased SNr activity during action suppression. Our results highlight conserved basal ganglia mechanisms across species and offer insights into the neural substrates of action selection and suppression in primates, with implications for understanding disorders such as Parkinson's disease. |
Anna Bognár; Ghazaleh Ghamkhari Nejad; Guy Rens; Rajani Raman; Rufin Vogels Expanding the stimulus domain: Co-occurrence of motion and body-category selectivity in the macaque ventral STS Journal Article In: Progress in Neurobiology, vol. 249, pp. 1–15, 2025. @article{Bognar2025a,The primate Superior Temporal Sulcus (STS) plays a pivotal role in the recognition of bodies and their actions, which is essential for survival and social interaction with conspecifics. Here, we show that, surprisingly, a sizable proportion of macaque middle ventral STS units are selective for static bodies and random dot motion. They show a faithful representation of random dot motion direction, with motion directions differing by 180 degrees being represented distinctly, although responding more strongly to complex optic flow patterns. This aligns with an fMRI experiment in which we show that the mid-STS body patch, defined by a greater activation to static bodies compared to faces and objects, is also more strongly activated by moving random dot patterns compared to static ones, especially when including complex optic flow patterns. More anterior ventral STS body-selective units demonstrate a less pronounced random dot motion selectivity and this is mainly for complex optic flow patterns. Moreover, middle STS units, but rarely those of the anterior STS, respond selectively to dynamic dot patterns in which body parts are visible solely through motion, and their preference correlates with those for videos of acting monkeys. Overall, these findings highlight an association between body and motion processing in the macaque ventral STS, which might result from the co-occurrence of body features and motion during the observation of bodily actions. |
Emily E. Oor; Emilio Salinas; Terrence R. Stanford Location- and feature-based selection histories make independent, qualitatively distinct contributions to urgent visuomotor performance Journal Article In: eLife, vol. 13, pp. 1–25, 2025. @article{Oor2025,Attention mechanisms guide visuomotor behavior by weighing physical salience and internal goals to prioritize stimuli as choices for action. Although less well studied, selection history, which reflects multiple facets of experience with recent events, is increasingly recognized as a distinct source of attentional bias. To examine how selection history impacts saccadic choices, we trained two macaque monkeys to perform an urgent version of an oddball search task in which a red target appeared among three green distracters or vice versa. By imposing urgency, performance could be tracked continuously as it transitioned from uninformed guesses to informed choices as a function of processing time. This, in turn, permitted assessment of attentional control as manifest in motor biases, processing speed, and asymptotic accuracy. Here, we found that the probability of making a correct choice was strongly modulated by the histories of preceding target locations and target colors. Crucially, although both effects were gated by success (or reward), their dynamics were clearly distinct: whereas location history promoted a motor bias, color history modulated perceptual sensitivity, and these influences acted independently. Thus, combined selection histories can give rise to enormous swings in visuomotor performance even in simple tasks with highly discriminable stimuli. |
Pengcheng Li; Heng Ma; Haidong D. Lu Direction-selective neurons in macaque V4 Journal Article In: Journal of Neurophysiology, vol. 133, no. 5, pp. 1572–1582, 2025. @article{Li2025j,In mammalian visual system, direction-selective (DS) neurons prefer visual motion in a particular direction and are specialized for visual motion processing. In area V4 of the macaque, about 13% neurons are direction-selective and form clusters (DS domains). The functional role of DS neurons in this form-processing area is still unknown. We implanted electrode arrays targeting these DS domains and recorded neurons' responses to moving stimuli such as gratings and simple shapes. We found that DS neurons were similar to non-DS neurons in their receptive field sizes and orientation-selectivity properties. However, population-wise, DS neurons responded slower and had lower firing rates than non-DS neurons, contrary to their traditional role in motion processing. In addition, direction selectivity of V4 neurons was stimulus-dependent (i.e., not invariant). DS neurons identified with grating stimuli may not exhibit direction selectivity to other types of stimuli such as random dots or contour shapes. These results suggest that, unlike DS neurons in other areas, V4 DS neurons may have a unique origin for their direction selectivity and nontraditional roles in visual motion processing. |
Bikash Sahoo; Adam C. Snyder Neural dynamics in extrastriate cortex underlying false alarms Journal Article In: The Journal of Neuroscience, vol. 45, no. 20, pp. 1–16, 2025. @article{Sahoo2025,The unfolding of neural population activity can be described as a dynamical system. Stability in the latent dynamics that characterize neural population activity has been linked with consistency in animal behavior, such as motor control or value-based decision-making. However, whether such characteristics of neural dynamics can explain visual perceptual behavior is not well understood. To study this, we recorded V4 populations in two male monkeys engaged in a non-match-to-sample visual change-detection task that required sustained engagement. We measured how the stability in the latent dynamics in V4 might affect monkeys' perceptual behavior. Specifically, we reasoned that unstable sensory neural activity around dynamic attractor boundaries may make animals susceptible to taking incorrect actions when withholding action would have been correct (“false alarms”). We made three key discoveries: (1) greater stability was associated with longer trial sequences; (2) false alarm rate decreased (and response times slowed) when neural dynamics were more stable; and (3) low stability predicted false alarms on a single-trial level, and this relationship depended on the position of the neural activity within the state space, consistent with the latent neural state approaching an attractor boundary. Our results suggest the same outward false alarm behavior can be attributed to two different potential strategies that can be disambiguated by examining neural stability: (1) premeditated false alarms that might lead to greater stability in population dynamics and faster response time and (2) false alarms due to unstable sensory activity consistent with misperception. |
Dixit Sharma; Shira M. Lupkin; Vincent B. McGinty Orbitofrontal high-gamma reflects spike-dissociable value and decision mechanisms Journal Article In: The Journal of Neuroscience, vol. 45, no. 20, pp. 1–17, 2025. @article{Sharma2025a,The orbitofrontal cortex (OFC) plays a crucial role in value-based decisions. While much is known about how OFC neurons represent values, far less is known about information encoded in OFC local field potentials (LFPs). LFPs are important because they can reflect subthreshold activity not directly coupled to spiking and because they are potential targets for less invasive forms of brain–machine interface (BMI). We recorded neural activity in the OFC of male macaques performing a two-option value-based decision task. We compared the value- and decision-coding properties of high-gamma LFPs (HG, 50–150 Hz) to the coding properties of spiking multiunit activity (MUA) recorded concurrently on the same electrodes. HG and MUA both represented the values of decision targets, but HG signals had value-coding features that were distinct from concurrently measured MUA. On average HG amplitude increased monotonically with value, whereas in MUA the value encoding was net neutral on average. HG encoded a signal consistent with a comparison between target values, a signal which was negligible in MUA. In individual channels, HG could predict choice outcomes more accurately than MUA; however, when channels were combined in a population-based decoder, MUA was more accurate than HG. In summary, HG signals reveal value-coding features in OFC that could not be observed from spiking activity, including representation of value comparisons and more accurate behavioral predictions. These results have implications for the role of OFC in value-based decisions and suggest that high-frequency LFPs may be a viable—or even preferable—target for BMIs to assist cognitive function. |
Wajd Amly; Chih-Yang Chen; Hirotaka Onoe; Tadashi Isa Different properties of successful and error saccades in marmosets Journal Article In: Neuroscience Research, vol. 213, pp. 60–71, 2025. @article{Amly2025,Various oculomotor tasks have been used to study eye movements, cognitive control, attention, and neurological disorders. Typically, analysis focuses on successful trials, where the saccade lands very close to the intended target, in both humans or non-human primates (NHPs). Error trials, in which the saccade fails to land on the intended target, are often excluded from these analyses. In this study, we hypothesized that saccades contain information that can predict whether they will result in success or not. We collected data from common marmosets performing the gap saccade task and the oculomotor delayed response task. Successful saccades in both tasks were characterized by higher peak velocities, shorter durations, and shorter latencies compared to errant saccades, regardless of whether the amplitudes were matched or not. These results were further validated using a generalized linear model, with saccade velocity, duration, and latency as predictors. The model demonstrated high accuracy in distinguishing between behavioural outcomes. Our findings suggest that the likelihood of a saccadic eye movement leading to a successful outcome may be predetermined, potentially reflecting the interaction between cognitive processes and saccade programming. |
Runnan Cao; Jie Zhang; Jie Zheng; Yue Wang; Peter Brunner; Jon T. Willie; Shuo Wang A neural computational framework for face processing in the human temporal lobe Journal Article In: Current Biology, vol. 35, no. 8, pp. 1765–1778, 2025. @article{Cao2025,A key question in cognitive neuroscience is how unified identity representations emerge from visual inputs. Here, we recorded intracranial electroencephalography (iEEG) from the human ventral temporal cortex (VTC) and medial temporal lobe (MTL), as well as single-neuron activity in the MTL, to demonstrate how dense feature-based representations in the VTC are translated into sparse identity-based representations in the MTL. First, we characterized the spatiotemporal neural dynamics of face coding in the VTC and MTL. The VTC, particularly the fusiform gyrus, exhibits robust axis-based feature coding. Remarkably, MTL neurons encode a receptive field within the VTC neural feature space, constructed using VTC neural axes, thereby bridging dense feature and sparse identity representations. We further validated our findings using recordings from a macaque. Lastly, inter-areal interactions between the VTC and MTL provide the physiological basis of this computational framework. Together, we reveal the neurophysiological underpinnings of a computational framework that explains how perceptual information is translated into face identities. |
Steven P. Errington; Jeffrey D. Schall A preparatory cranial potential for saccadic eye movements in macaque monkeys Journal Article In: eNeuro, vol. 12, no. 4, pp. 1–10, 2025. @article{Errington2025,Response preparation is accomplished by gradual accumulation in neural activity until a threshold is reached. In humans, such a preparatory signal, referred to as the lateralized readiness potential (LRP), can be observed in the EEG over sensorimotor cortical areas before execution of a voluntary movement. Although well described for manual movements, less is known about preparatory EEG potentials for saccadic eye movements in humans and nonhuman primates. Hence, we describe a LRP over the frontolateral cortex in macaque monkeys. Homologous to humans, we observed lateralized electrical potentials ramping before the execution of both rewarded and nonrewarded contralateral saccades. This potential parallels the neural spiking of saccadic movement neurons in the frontal eye field (FEF), suggesting that it may offer a noninvasive correlate of intracortical spiking activity. However, unlike neural spiking in the FEF, polarization in frontolateral channels did not distinguish between saccade generation and inhibition. These findings provide new insights into noninvasive electrophysiological signatures of saccadic preparation in nonhuman primates, highlighting the potential of EEG measures to bridge invasive neural recordings and noninvasive studies of eye movement control in humans. |
Wen Fang; Xi Jiang; Jingwen Chen; Cong Zhang; Liping Wang Oscillatory control over representational geometry of sequence working memory in macaque frontal cortex Journal Article In: Current Biology, vol. 35, no. 7, pp. 1495–1507, 2025. @article{Fang2025,To process sequential streams of information, e.g., language, the brain must encode multiple items in sequence working memory (SWM) according to their ordinal relationship. While the geometry of neural states could represent sequential events in the frontal cortex, the control mechanism over these neural states remains unclear. Using high-throughput electrophysiology recording in the macaque frontal cortex, we observed widespread theta responses after each stimulus entry. Crucially, by applying targeted dimensionality reduction to extract task-relevant neural subspaces from both local field potential (LFP) and spike data, we found that theta power transiently encoded each sequentially presented stimulus regardless of its order. At the same time, theta-spike interaction was rank-selectively associated with memory subspaces, thereby potentially supporting the binding of items to appropriate ranks. Furthermore, this putative theta control can generalize to length-variable and error sequences, predicting behavior. Thus, decomposed entry/rank-WM subspaces and theta-spike interactions may underlie the control of SWM. |
Paul Hage; Mohammad Amin Fakharian; Alden M. Shoup; Jay S. Pi; Ehsan Sedaghat-Nejad; Simon P. Orozco; In Kyu Jang; Vivian Looi; Hisham Y. Elseweifi; Nazanin Mohammadrezaei; Alexander N. Vasserman; Toren Arginteanu; Reza Shadmehr Purkinje cells of the cerebellum control deceleration of tongue movements Journal Article In: PLoS Biology, vol. 23, no. 4, pp. 1–28, 2025. @article{Hage2025,We use our tongue much like our hands: to interact with objects and transport them. For example, we use our hands to sense properties of objects and transport them in the nearby space, and we use our tongue to sense properties of food morsels and transport them through the oral cavity. But what does the cerebellum contribute to control of tongue movements? Here, we trained head-fixed marmosets to make skillful tongue movements to harvest food from small tubes that were placed at sharp angles to their mouth. We identified the lingual regions of the cerebellar vermis and then measured the contribution of each Purkinje cell (P-cell) to control of the tongue by relying on the brief but complete suppression that they experienced following an input from the inferior olive. When a P-cell was suppressed during protraction, the tongue's trajectory became hypermetric, and when the suppression took place during retraction, the tongue's return to the mouth was slowed. Both effects were amplified when two P-cells were simultaneously suppressed. Moreover, these effects were present even when the pauses were not due to the climbing fiber input. Therefore, suppression of P-cells in the lingual vermis disrupted the forces that would normally decelerate the tongue as it approached the target. Notably, the population simple spike activity peaked near deceleration onset when the movement required precision (aiming for a tube), but not when the movement was for the purpose of grooming. Thus, the P-cells appeared to signal when to stop protrusion as the tongue approached its target. |
Kyoko Leaman; Nadira Yusif Rodriguez; Aarit Ahuja; Debaleena Basu; Theresa H. McKim; Theresa M. Desrochers Monkey lateral prefrontal cortex subregions differentiate between perceptual exposure to visual stimuli Journal Article In: Journal of Cognitive Neuroscience, vol. 37, no. 4, pp. 802–814, 2025. @article{Leaman2025,Each day, humans must parse visual stimuli with varying amounts of perceptual experience, ranging from incredibly familiar to entirely new. Even when choosing a novel to buy at a bookstore, one sees covers they have repeatedly experienced intermixed with recently released titles. Visual exposure to stimuli has distinct neural correlates in the lateral prefrontal cortex (LPFC) of nonhuman primates. However, it is currently unknown if this function may be localized to specific subregions within LPFC. Specifically, we aimed to determine whether the posterior fundus of Area 46 (p46f), an area that responds to deviations from learned sequences, also responds to less frequently presented stimuli outside of the sequential context. We compare responses in p46f to the adjacent subregion, posterior ventral area 46 (p46v), which we propose may be more likely to show exposure-dependent responses due to its proximity to novelty-responsive regions. To test whether p46f or p46v represent perceptual exposure, we performed awake fMRI on three male monkeys as they observed visual stimuli that varied in their number of daily presentations. Here, we show that p46v, but not p46f, shows preferential activation to stimuli with low perceptual exposure, further localizing exposure-dependent effects in monkey LPFC. These results align with previous research that has found novelty responses in ventral LPFC and are consistent with the proposal that p46f performs a sequence-specific function. Furthermore, they expand on our knowledge of the specific role of LPFC subregions and localize perceptual exposure processing within this broader brain region. |
Matthew C. Rosen; David J. Freedman Multiplexing of cognitive encoding by oculomotor networks leads to incidental gaze shifts Journal Article In: PNAS, vol. 122, no. 15, pp. 1–11, 2025. @article{Rosen2025,Humans and other animals are adept at learning to perform cognitively demanding behavioral tasks. Neurophysiological recordings in nonhuman primates during such tasks find that the requisite cognitive variables are encoded strongly in core oculomotor brain regions. Here, we assembled a large dataset—11 monkeys performing an abstract visual categorization task, surveyed across more than 1,000 neural recording sessions— to reveal that this produces a robust but uninstructed behavioral “tell,” observed in all subjects and experiments: small, cognitively modulated eye movements. We find that these eye movements are causally linked to activity in SC but not LIP, and that they occur following transient alignment of cognitive and saccadic population coding subspaces in SC. This behavioral signature of oculomotor engagement is absent during a similar task that does not require rule-based categorization, suggesting that abstract task behaviors recruit primate oculomotor networks more strongly than previously understood. |
Hayden Scott; Allison J. Murphy; Farran Briggs; Adam C. Snyder Using generative models of naturalistic scenes to sample neural population tuning manifolds Journal Article In: European Journal of Neuroscience, vol. 61, no. 7, pp. 1–24, 2025. @article{Scott2025,Investigations into sensory coding in the visual system have typically relied on the use of either simple, unnatural visual stimuli or natural images. Simple stimuli, such as Gabor patches, have been effective when looking at single neurons in early visual areas such as V1 but seldom produce large responses from mid-level visual neurons or neural populations with diverse tuning. Many types of “naturalistic” image models have been developed recently, which bridge the gap between overly simple stimuli and experimentally infeasible natural images. These stimuli can vary along a large number of feature dimensions, introducing new challenges when trying to map those features to neural activity. This “curse of dimensionality” is exacerbated when neural responses are themselves high dimensional, such as when recording neural populations with implanted multielectrode arrays. We propose a method that searches high-dimensional stimulus spaces for characterizing neural population manifolds in a closed-loop experimental design. Stimuli were generated using a deep neural network in each block by using neural responses to previous stimuli to make predictions about the relationship between the latent space of the image model and neural responses. We found that these latent variables from the deep generative image model explained stronger linear relationships with neural activity than various alternative forms of image compression. This result reinforces the potential for deep generative image models for efficient characterization of high-dimensional tuning manifolds for visual neural populations. |
Kiomars Sharifi; Mojtaba Abbaszadeh; Ali Ghazizadeh Spatial processing enhancement in the prefrontal cortex for rapid detection of valuable objects Journal Article In: The Journal of Neuroscience, vol. 45, no. 16, pp. 1–13, 2025. @article{Sharifi2025,It is recently shown that objects with long-term reward associations can be efficiently located during visual search. The neural mechanism for valuable object pop-out is unknown. In this work, we recorded neuronal responses in the ventrolateral prefrontal cortex (vlPFC) with known roles in visual search and reward processing in macaques while monkeys engaged in efficient versus inefficient visual search for high-value fractal objects (targets). Behavioral results and modeling using multialternative attention-modulated drift-diffusion indicated that efficient search was concurrent with enhanced processing for peripheral objects. Notably, neural results showed response amplification and receptive field widening to peripherally presented targets in vlPFC during visual search. Both neural effects predict higher target detection and were found to be correlated with it. Our results suggest that value-driven efficient search independent of low-level visual features arises from reward-induced spatial processing enhancement of peripheral valuable objects. |
Xing Nan Zhao; Sheng Hui Zhang; Shi Ming Tang; Cong Yu Surround modulation is predominantly orientation-unspecific in macaque V1 Journal Article In: Progress in Neurobiology, vol. 247, pp. 1–11, 2025. @article{Zhao2025d,Surround modulation is a fundamental property of V1 neurons, playing critical roles in stimulus integration and segregation. It is believed to be orientation-specific, as neurons' responses at preferred orientations are suppressed more by iso-oriented surrounds than by cross-oriented surrounds. Here, we investigated an alternative hypothesis that surround modulation is primarily orientation-unspecific, in that the observed “orientation-specific” surround effects actually reflect overall gain changes that affect neurons tuned to all orientations. We employed two-photon calcium imaging to compare V1 population orientation tuning functions under iso- and cross-surround modulation in awake, fixating macaques. While confirming “orientation-specific” surround suppression in individual neurons, our analysis of the population orientation tuning functions revealed that iso-surrounds induce a general orientation-unspecific suppression across all orientation-tuned neurons, plus weak orientation-specific suppression to neurons tuned to the center stimulus orientation. Furthermore, cross-surrounds mainly reduce orientation-unspecific suppression by scaling up responses of all orientation-tuned neurons. These findings suggest a model of population gain control where surround stimuli mostly scale the responses of the neuronal population. Further population coding analyses supported this conclusion, demonstrating that surround suppression leads to degraded target orientation information at least partially due to a reduced number of contributing neurons with diverse orientation preferences. |
Donatas Jonikaitis; Ruobing Xia; Tirin Moore Robust encoding of stimulus–response mapping by neurons in visual cortex Journal Article In: PNAS, vol. 122, no. 9, pp. 1–10, 2025. @article{Jonikaitis2025,Neural activity in sensory cortex is modulated by behavioral and cognitive factors, and this modulation is thought to contribute to the selection of specific sensory information needed to achieve behavioral goals. In contrast, more abstract behavioral variables that are independent of stimulus selection, such as stimulus–response mapping, are thought to be encoded by neurons outside of sensory cortex. We show that information about such mapping is robustly encoded in the responses of neurons in primate visual cortex. Monkeys were trained to alternate between two tasks that differed in the rule governing the mapping of a remembered visual cue onto an eye movement response. During the memory-delay period, neurons in area V4 reliably signaled the remembered cue location in both tasks. However, the encoding of cue location depended critically on the stimulus–response mapping rule. Thus, V4 delay activity encoded the mapping rule and signaled the preparation of the appropriate motor response rather than spatial working memory per se, contrary to previous assumptions. In addition, we probed the origins of motor-related delay activity and found that it was reduced during local inactivation of the frontal eye field (FEF). The results demonstrate that behavioral modulation of visual cortical activity is not solely related to the selection of sensory stimuli but instead reflects a distinct mechanism for sensory-guided motor output. |
Atsushi Noritake; Masaki Isoda The macaque medial prefrontal cortex simultaneously represents self and others' reward prediction error Journal Article In: Cell Reports, vol. 44, no. 3, pp. 1–31, 2025. @article{Noritake2025,Learning the causal structures of social environments involves predicting significant events (e.g., rewards) and detecting prediction errors for each agent. Whether the brain can simultaneously compute reward prediction errors for self (S-RPE) and others (O-RPE), and which neurons are responsible, is unclear. Here, we condition two monkeys with identical visual stimuli predicting different reward outcomes and find that dorsomedial prefrontal neurons represent both S-RPE and O-RPE simultaneously. Neuronal signatures of RPE are agent and sign specific, forming distinct populations for positive and negative S-RPE and O-RPE. A linear decoder trained on neurons encoding O-RPE, but not S-RPE, successfully discriminates RPE. Further investigation identifies coexisting actual reward and prediction confirmation signals for others. These results highlight the presence of neuronal mechanisms in the primate brain that update the value of environmental stimuli simultaneously for oneself and others, enabling primates to comprehend the causal structure of the world from the perspective of others. |
Thomas W. Elston; Joni D. Wallis Context-dependent decision-making in the primate hippocampal–prefrontal circuit Journal Article In: Nature Neuroscience, vol. 28, no. 2, pp. 374–382, 2025. @article{Elston2025,What is good in one scenario may be bad in another. Despite the ubiquity of such contextual reasoning in everyday choice, how the brain flexibly uses different valuation schemes across contexts remains unknown. We addressed this question by monitoring neural activity from the hippocampus (HPC) and orbitofrontal cortex (OFC) of two monkeys performing a state-dependent choice task. We found that HPC neurons encoded state information as it became available and then, at the time of choice, relayed this information to the OFC via theta synchronization. During choice, the OFC represented value in a state-dependent manner; many OFC neurons uniquely coded for value in only one state but not the other. This suggests a functional dissociation whereby the HPC encodes contextual information that is broadcast to the OFC via theta synchronization to select a state-appropriate value subcircuit, thereby allowing for contextual reasoning in value-based choice. |
Kenji W. Koyano; Jessica Taubert; William Robison; Elena N. Waidmann; David A. Leopold Face pareidolia minimally engages macaque face selective neurons Journal Article In: Progress in Neurobiology, vol. 245, pp. 1–12, 2025. @article{Koyano2025,The macaque cerebral cortex contains concentrations of neurons that prefer faces over inanimate objects. Although these so-called face patches are thought to be specialized for the analysis of facial signals, their exact tuning properties remain unclear. For example, what happens when an object by chance resembles a face? Everyday objects can sometimes, through the accidental positioning of their internal components, appear as faces. This phenomenon is known as face pareidolia. Behavioral experiments have suggested that macaques, like humans, perceive illusory faces in such objects. However, it is an open question whether such stimuli would naturally stimulate neurons residing in cortical face patches. To address this question, we recorded single unit activity from four fMRI-defined face-selective regions: the anterior medial (AM), anterior fundus (AF), prefrontal orbital (PO), and perirhinal cortex (PRh) face patches. We compared neural responses elicited by images of real macaque faces, pareidolia-evoking objects, and matched control objects. Contrary to expectations, we found no evidence of a general preference for pareidolia-evoking objects over control objects. Although a subset of neurons exhibited stronger responses to pareidolia-evoking objects, the population responses to both categories of objects were similar, and collectively much less than to real macaque faces. These results suggest that neural responses in the four regions we tested are principally concerned with the analysis of realistic facial characteristics, whereas the special attention afforded to face-like pareidolia stimuli is supported by activity elsewhere in the brain. |
Timo Kerkoerle; Louise Pape; Milad Ekramnia; Xiaoxia Feng; Jordy Tasserie; Morgan Dupont; Xiaolian Li; Bechir Béchir 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. |
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. |
Zoe M Boundy-Singer; Corey M Ziemba; Robbe L T Goris Sensory population activity reveals downstream confidence computations in the primate visual system Journal Article In: PNAS, vol. 122, no. 26, pp. 1–11, 2025. @article{BoundySinger2025,Perception is fallible. Humans know this, and so do some nonhuman animals like macaque monkeys. When monkeys report more confidence in a perceptual decision, that decision is more likely to be correct. It is not known how neural circuits in the primate brain assess the quality of perceptual decisions. Here, we test two hypotheses. First, that decision confidence is related to the structure of population activity in the sensory cortex. And second, that this relation differs from the one between sensory activity and decision content. We trained macaque monkeys to judge the orientation of ambiguous stimuli and additionally report their confidence in these judgments. We recorded population activity in the primary visual cortex and used decoders to expose the relationship between this activity and the choice-confidence reports. Our analysis validated both hypotheses and suggests that perceptual decisions arise from a neural computation downstream of visual cortex that estimates the most likely interpretation of a sensory response, while decision confidence instead reflects a computation that evaluates whether this sensory response will produce a reliable decision. Our work establishes a direct link between neural population activity in the sensory cortex and the metacognitive ability to introspect about the quality of perceptual decisions. |
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. |
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. |
Dennis Y. Jung; Bikash C. Sahoo; Adam C. Snyder Distractor anticipation during working memory is associated with theta and beta oscillations across spatial scales Journal Article In: Frontiers in Integrative Neuroscience, vol. 19, pp. 1–4, 2025. @article{Jung2025,Introduction: Anticipating distractors during working memory maintenance is critical to reduce their disruptive effects. In this study, we aimed to identify the oscillatory correlates of this process across different spatial scales of neural activity. Methods: We simultaneously recorded local field potentials (LFP) from the lateral prefrontal cortex (LPFC) and electroencephalograms (EEG) from the scalp of monkeys performing a modified memory-guided saccade (MGS) task. The monkeys were required to remember the location of a target visual stimulus while anticipating distracting visual stimulus, flashed at 50% probability during the delay period. Results: We found significant theta-band activity across spatial scales during anticipation of a distractor, closely linked with underlying working memory dynamics, through decoding and cross-temporal generalization analyses. EEG particularly reflected reactivation of memory around the anticipated time of a distractor, even in the absence of stimuli. During this anticipated time, beta-band activity exhibited transiently enhanced intrahemispheric communication between the LPFC and occipitoparietal brain areas. These oscillatory phenomena were observed only when the monkeys successfully performed the task, implicating their possible functional role in mitigating anticipated distractors. Discussion: Our results demonstrate that distractor anticipation recruits multiple oscillatory processes across the brain during working memory maintenance, with a key activity observed predominantly in the theta and beta bands. |
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. |
Yavar Korkian; Nardin Nakhla; Christopher C. Pack Feature selectivity of corticocortical feedback along the primate dorsal visual pathway Journal Article In: Journal of Neurophysiology, vol. 133, no. 3, pp. 799–814, 2025. @article{Korkian2025,Anatomical studies have revealed a prominent role for feedback projections in the primate visual cortex. Theoretical models suggest that these projections support important brain functions such as attention, prediction, and learning. However, these models make different predictions about the relationship between feedback connectivity and neuronal stimulus selectivity. We have therefore performed simultaneous recordings in different regions of the primate dorsal visual pathway. Specifically, we recorded neural activity from the medial superior temporal (MST) area, and one of its main feedback targets, the middle temporal (MT) area. We estimated functional connectivity from correlations in the single-neuron spike trains and performed electrical microstimulation in MST to determine its causal influence on MT. Both methods revealed that inhibitory feedback occurred more commonly when the source and target neurons had very different stimulus preferences. At the same time, the strength of feedback suppression was greater for neurons with similar preferences. Excitatory feedback projections, in contrast, showed no consistent relationship with stimulus preferences. These results suggest that corticocortical feedback could play a role in shaping sensory responses according to behavioral or environmental context. |
Xinhe Liu; Zhiting Zhang; Ji Dai Evaluating pupillometry as a tool for assessing facial and emotional processing in nonhuman primates Journal Article In: Applied Sciences, vol. 15, no. 6, pp. 1–14, 2025. @article{Liu2025r,Non-human primates (NHPs) are extensively utilized to investigate the neural mechanisms underlying face processing; however, measuring their brain activity necessitates a diverse array of technologies. Pupillometry emerges as a convenient, cost-effective, and non-invasive alternative for indirectly assessing brain activity. To evaluate the efficacy of pupillometry in assessing facial and emotional processing in NHPs, this study designed a face fixation task for experimental monkeys (Rhesus macaque) and recorded variations in their pupil size in response to face images with differing characteristics, such as species, emotional expression, viewing angles, and orientation (upright vs. inverted). All face images were balanced with luminance and spatial frequency. A sophisticated eye-tracking system (Eye-link 1000 plus) was employed to observe the pupils and track the viewing trajectories of monkeys as they examined images of faces. Our findings reveal that monkeys exhibited larger pupil sizes in response to carnivore faces (versus human faces |
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, vol. 12, no. 16, 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. |
Tomoyuki Namima; Erin Kempkes; Polina Zamarashkina; Natalia Owen; Anitha Pasupathy High-density recording reveals sparse clusters (but not columns) for shape and texture encoding in macaque V4 Journal Article In: The Journal of Neuroscience, vol. 45, no. 5, pp. 1–17, 2025. @article{Namima2025,Macaque area V4 includes neurons that exhibit exquisite selectivity for visual form and surface texture, but their functional organization across laminae is unknown. We used high-density Neuropixels probes in two awake monkeys (one female and one male) to characterize the shape and texture tuning of dozens of neurons simultaneously across layers. We found sporadic clusters of neurons that exhibit similar tuning for shape and texture: ∼20% exhibited similar tuning with their neighbors. Importantly, these clusters were confined to a few layers, seldom “columnar” in structure. This was the case even when neurons were strongly driven and exhibited robust contrast invariance for shape and texture tuning. We conclude that functional organization in area V4 is not columnar for shape and texture stimulus features and in general organization may be at a coarser stimulus category scale (e.g., selectivity for stimuli with vs without 3D cues) and a coarser spatial scale (assessed by optical imaging), rather than at a fine scale in terms of similarity in single-neuron tuning for specific features. We speculate that this may be a direct consequence of the great diversity of inputs integrated by V4 neurons to build variegated tuning manifolds in a high-dimensional space. |
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. |
Luke Priestley; Mark Chiew; Mo Shahdloo; Ali Mahmoodi; Xinghao Cheng; Robin Cleveland; Matthew Rushworth; Nima Khalighinejad Dorsal raphe nucleus controls motivation-state transitions in monkeys Journal Article In: Science Advances, vol. 11, no. 26, pp. 1–20, 2025. @article{Priestley2025,The dorsal raphe nucleus (DRN) is an important source of serotonin in the brain, but fundamental aspects of its function remain elusive. Here, we present a combination of minimally invasive recording and disruption studies to show that DRN brings about changes in motivation states. We use recently developed methods for identifying temporal patterns in behavior to show that monkeys change their motivation depending on the availability of rewards in the environment. Distinctive patterns of DRN activity occur when monkeys transition between a high-motivation state occupied when rewards are abundant, to a low-motivation state engendered by reward scarcity. Disrupting DRN diminishes sensitivity to the reward environment and perturbs transitions in motivational states. |
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. |
Alexander Schielke; Bart Krekelberg N-Methyl D-aspartate receptor hypofunction reduces steady-state visual-evoked potentials Journal Article In: Journal of Neurophysiology, vol. 134, no. 2, pp. 591–601, 2025. @article{Schielke2025,The dynamic coordination of neural activity across populations of neurons is impaired in neuropsychiatric disorders. Here, we focused on the large-scale rhythmic responses induced by flickering light. These so-called steady-state visual-evoked potentials (SSVEPs) are reduced in people with schizophrenia (Sz). A large body of work has identified hypofunction of the N-methyl D-aspartate receptor (NMDAR) as a potential contributor to the symptoms of Sz. Here, we tested the hypothesis that NMDAR hypofunction can account for a reduced ability to generate the coordinated activity reflected in SSVEPs. We recorded SSVEPs using multielectrode arrays permanently implanted in the primary visual cortex of nonhuman primates. In separate sessions, animals were injected with saline (control) or a subanesthetic dose of ketamine (an NMDAR antagonist) to induce an NMDAR hypofunction state. SSVEPs generated during NMDAR hypofunction were substantially reduced and, consistent with findings in Sz, this reduction was found across a range of frequencies from 5 to 40 Hz. These findings provide novel insight into the role of NMDAR hypofunction in the generation of altered coordinated activity and provide experimental support for the hypothesis that NMDAR hypofunction underlies some of the symptoms of schizophrenia. |
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. |
Sina Tafazoli; Flora M. Bouchacourt; Adel Ardalan; Nikola T. Markov; Motoaki Uchimura; Marcelo G. Mattar; Nathaniel D. Daw; Timothy J. Buschman Building compositional tasks with shared neural subspaces Journal Article In: Nature, pp. 1–36, 2025. @article{Tafazoli2025,Cognition is highly flexible—we perform many different tasks1 and continually adapt our behaviour to changing demands2,3. Artificial neural networks trained to perform multiple tasks will reuse representations4 and computational components5 across tasks. By composing tasks from these subcomponents, an agent can flexibly switch between tasks and rapidly learn new tasks6,7. Yet, whether such compositionality is found in the brain is unclear. Here we show the same subspaces of neural activity represent task-relevant information across multiple tasks, with each task flexibly engaging these subspaces in a task-specific manner. We trained monkeys to switch between three compositionally related tasks. In neural recordings, we found that task-relevant information about stimulus features and motor actions were represented in subspaces of neural activity that were shared across tasks. When monkeys performed a task, neural representations in the relevant shared sensory subspace were transformed to the relevant shared motor subspace. Monkeys adapted to changes in the task by iteratively updating their internal belief about the current task and then, based on this belief, flexibly engaging the shared sensory and motor subspaces relevant to the task. In summary, our findings suggest that the brain can flexibly perform multiple tasks by compositionally combining task-relevant neural representations. |
Miguel Vivar-Lazo; Christopher R. Fetsch Neural basis of concurrent deliberation toward a choice and confidence judgment Journal Article In: Nature Neuroscience, vol. 29, pp. 159–170, 2025. @article{VivarLazo2025,Decision confidence plays a key role in flexible behavior and (meta)cognition, but its underlying neural mechanisms remain elusive. To uncover the latent dynamics of confidence formation at the level of single neurons and population activity, we trained nonhuman primates to report a perceptual choice and the associated level of confidence with a single eye movement on every trial. Monkey behavior was well fit by a bounded accumulator model, where choice and confidence are processed concurrently, but not by a serial model, where choice is resolved first, followed by postdecision accumulation for confidence. Neurons in the lateral intraparietal area (LIP) reflected concurrent accumulation, showing covariation of choice and confidence signals across the population, and within-trial dynamics consistent with parallel updating at near-zero time lag. The results demonstrate that the primate brain can process a single stream of evidence in service of two computational goals simultaneously and suggest area LIP as a candidate neural substrate for this ability. |
Yordanka Zafirova; Rufin Vogels Integration of head and body orientations in the macaque superior temporal sulcus is stronger for upright bodies Technical Report 2025. @techreport{Zafirova2025,The neural processing of faces and bodies is often studied separately, despite their natural integration in perception. Unlike prior research on the neural selectivity for either head or body orientation, we investigated their interaction in macaque superior temporal sulcus (STS) using a monkey avatar with diverse head–body orientation angles. STS neurons showed selectivity for specific combinations of head–body orientations. Anterior STS (aSTS) neurons enabled more reliable decoding of head–body configuration angles compared to middle STS neurons. Decoding accuracy in aSTS was lowest for head–body angle pairs differing only in sign (e.g. head–body orientation difference of ±90° relative to the anatomical midline), and highest for aligned (0°) head–body orien- tations versus those with maximum angular difference. Inverted bodies showed diminished decoding of head–body orientation angle compared to upright bodies. These findings show that aSTS inte- grates head and body orientation cues, revealing configuration- specific neural mechanisms, and advance our understanding of social perception. |
2024 |
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. |
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. |
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. |