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Duhamel, J.-R.

Publications and source records attributed to Duhamel, J.-R..

7 recordsLinked to original sources

Chemogenetic activation of hypothalamic oxytocin neurons reorients face exploration toward the eyes in macaques

Oxytocin (OT) shapes social behavior across species. However, in humans and non-human primates, its effects have been studied mainly through exogenous administration, despite uncertainty about the extent to which peripherally administered OT reaches the brain and limited control over the neural pathways it engages. To overcome these limitations, we developed a chemogenetic approach targeting the endogenous OT system by selectively activating OT neurons in the paraventricular nucleus (PVN) and supraoptic nucleus (SON) of macaques using excitatory DREADDs. We combined this approach with digit-tracking, a non-invasive, calibration-free assay of face exploration in freely moving animals. In this task, subjects explored blurred face images through a finger-controlled viewing window, providing a proxy for gaze exploration and enabling behavioral assessment of OT neuron activation. DREADD-mediated activation redirected ongoing face exploration toward the eyes at the expense of non-face regions, increasing the consistency of eye-directed exploration and the time spent inspecting the eyes once reached. Immunohistochemical analysis confirmed selective DREADD expression in OT neurons of the PVN and SON. These findings provide the first causal evidence in primates that hypothalamic OT neurons regulate social visual orienting by increasing exploration of the eyes, thereby linking a hallmark effect of intranasal OT administration to defined central OT pathways and establishing chemogenetic access to this system in freely behaving macaques.

neuroscience↗

Frontal cortex encodes action goals and social context in freely moving and socially interacting macaques

Classic studies of goal-directed behavior in primates have investigated frontal cortical circuits under restraint conditions, leaving their role in natural social contexts largely unknown. We wirelessly recorded neural activity from freely moving macaques to study how frontal areas encode actions during naturalistic interactions. Neurons in ventral premotor and ventrolateral prefrontal cortex distinguished identical motor acts, such as grasping, depending on whether they occurred during foraging or grooming, indicating sensitivity to social meaning. Some units were selectively tuned to socially directed goals, while population analyses showed both regions flexibly integrated motor plans with social context. These results provide direct evidence that these regions, long considered key motor hubs, also encode the social dimension of action, redefining current models of frontal lobe function. One-Sentence SummaryFreely-moving, social-interacting macaques reveal new properties of frontal circuits in encoding motor goals and social context.

neuroscience↗

Primate ACC encodes natural vocal interactions in a cocktail party

The Cocktail Party Problem (CPP)--extracting meaningful signals amid competing voices--remains poorly understood at the neural level, particularly in real-world contexts where it emerges naturally. We investigated the role of the anterior cingulate cortex (ACC), a structure implicated in social monitoring but rarely examined in relation to audition, to resolve the CPP in freely-moving marmoset monkeys engaged in ecological vocal exchanges. Analyses revealed that ACC is seemingly integral to resolving the CPP. Not only did neurons encode the calls of either the conversational partner or background callers, but this selectivity persisted even with overlapping background sounds, a hallmark of the CPP. Moreover, ACC activity reflected the conversational dynamics by encoding turn-taking structure, highlighting the importance of CPP resolution for navigating social interactions in complex natural soundscapes.

neuroscience↗

Digit-Tracking Reveals Curiosity-Driven Visual Attention in Macaque Monkeys

We used digit-tracking, a touch-based method for assessing visual attention, to investigate spontaneous exploration in macaque monkeys. By engaging with degraded images on a touch-sensitive display, monkeys could uncover high-resolution portions through finger movements, allowing for natural and unrestricted interaction. Monkeys received juice rewards after touching a predetermined number of pixels, but no specific regions were targeted. Attention maps were generated from their interactions, along with data from human digit-tracking and monkey eye-tracking experiments. We applied a saliency model and a Convolutional Neural Network (CNN) model to predict the empirical explorations. The correlation between model prediction maps and empirical attention maps indicated that monkeys focused non-randomly on information-rich regions, with the CNN model providing the most accurate predictions. These findings suggest that exploration was driven by intrinsic curiosity, beyond the extrinsic rewards for interaction. Digit-tracking offers a minimally invasive, portable alternative to eye-tracking, expanding research opportunities in visual cognition within ecologically valid settings.

animal behavior and cognition↗

Spatio-temporal dynamics of ingroup interactions in macaques

When sharing a space with others, many species including humans evolved a compromise regulating occupancy influenced by social determinants. For example, students in a classroom tend to sit close to their friends, keeping the same spots across days, revealing the social structure in the classroom. This place preference suggests that factors such as social hierarchy and affiliation can shape space utilization; contrasting with random walk models of agents moving at random in any given direction. Here, we asked whether spatial occupancy of macaques (Macaca fascicularis and M. mulatta) within a unisex group, reveals a structured space utilization beyond simple spatial affordance within the finite space. To this end, in two groups of four animals, we analyzed the simultaneously recorded positions of each individual while the group roamed in an enclosure. The data was gathered using automated devices that allow measuring accurate concomitant positions and calculate precise inter-individual distance, which is impossible in classical ethology even using GPS devices. Thus, our setup opens new possibilities using modelling approach, to characterize social interaction dynamics in small enclosures. We found that (1) The identity of each animal could be decoded from its individual pattern of spatial occupancy, revealing that each animal sustained a spatial footprint across multiple days. (2) Average distance between monkeys was a proxy of their social hierarchy, confirming that interpersonal distance is correlated to affiliation and dominance hierarchy. (3) Alternating the social context by removing one of the monkeys revealed that only removing the closest social partner influenced occupancy. (4) Finally, the distribution of distance between pairs of monkeys was bimodal and was modeled using random walk approach with an additional parameter reflecting propensity to stay in close proximity, which was again related to dominance hierarchy. These analyses reveal that space utilization is structured as a function of social determinants in macaques and simple modeling approach to further study group organization in neuro-ethological settings.

animal behavior and cognition↗

Linking place and view: Organizing space through saccades and fixations between primate posterior parietal cortex and hippocampus

Humans primarily rely on vision to explore and guide actions in spatial environments. The parietal cortex is thought to withhold a unified representation of the visual space allowing to direct saccades to salient cues, while the hippocampus provides a memory-based cognitive place map of the environment. Understanding how these two representations interact during navigation is a key question. To probe the link between view and place, we compared neural activity in the posterior parietal cortex and hippocampus of macaques navigating in a virtual maze. When analyzed as a function of the animals position in the virtual environment, more neurons in the parietal cortex displayed spatial selectivity compared to the hippocampus. We hypothesized that such modulation by self-position in the parietal cortex might stem from processing visual cues of the environment through exploratory saccades and fixations. However, we established that position-selectivity was not solely correlated with simple oculomotor dynamics. Rather, spatial selectivities in the PPC and the HPC originated from cells driven by direct fixations of maze paths or landmarks. However, while a substantial proportion of PPC and HPC cells displayed selectivity towards landmarks features, such as their side of appearance or their identity, we also revealed different task-related maze segmentation between regions. Indeed, when animal gazed at paths, activity in parietal cortex revealed anticipation of reward while that of the hippocampus suggested reward outcome processing. On the other hand, when animals gazed at a landmark already present in the field of view, parietal activity tended to occur close to intersections, while that of hippocampus was more spatially distributed. Finally, at the population level, neurons in both regions anticipated landmarks before they appeared in the field of view, suggesting a shared knowledge of the spatial layout and a collective active role in memory-guided visual exploration across regions. Taken together, these findings shed light on the neural processes that link place and view, through action- and memory-driven exploration of objects in space.

neuroscience↗

Short-term reciprocity in macaques social decision-making

Primates live in complex social environments, where individuals create meaningful networks by adapting their behavior according to past experiences with others. Although free-ranging primates do show signs of reciprocity, experiments in more controlled environments have mainly failed to reproduce such social dynamics. Hence, the cognitive and neural processes allowing monkeys to reciprocate during social exchanges remains elusive. Here, pairs of long-tailed macaques (Macaca fascicularis) took turns into a social decision task involving the delivery of positive (juice reward) or negative (airpuff) outcomes. By analyzing the contingencies of one partners past decisions on the others future decisions, we demonstrate the presence of reciprocity, but only for the exchange of negative outcomes. Importantly, to display this decisional bias, the monkey needs to witness its partners decisions, since non-social deliveries of the same outcome did not have such effect. Withholding of negative outcomes also predicted future social decisions, which suggest that the observed tit-for-tat strategy may not only be motivated by retaliation after receiving an airpuff but also by the gratefulness of not having received one. These results clarify the apparent dichotomy within the scientific literature of reciprocity in non-human primates and suggest that their social cognition comprise revenge and gratitude.

animal behavior and cognition↗