Biology subjects

Ballesta, S.

Publications and source records attributed to Ballesta, S..

12 recordsLinked to original sources

bioRxiv2026

Risk management strategies in social grooming among Tonkean and rhesus macaques

Group-living individuals interact constantly, maintaining cohesion, stability, and security within their social groups. However, these interactions can entail risks that individuals must manage to optimize their social navigation through complex social groups, such as those of non-human primates. Here, we investigated how macaques manage risk during social grooming by analysing its somatic modalities, including body orientation and body site being groomed. We compared two macaque species with contrasting social styles: the more despotic rhesus macaque and the more tolerant Tonkean macaque. Using dyadic analyses including species, kinship, age difference, rank difference, and male presence as predictors, we found marked species differences in grooming patterns. Tonkean macaques engaged more frequently in face-to-face grooming and less in face-to-back grooming compared to rhesus macaques. They also groomed body sites associated with high eye-contact probability, such as the head, neck, and chest, more often than rhesus macaques. Kin dyads groomed these body sites more often, particularly in rhesus macaques. These findings suggest that avoiding body sites associated with potential eye-contact may constitute a risk management strategy during grooming. Overall, our results reveal a previously overlooked dimension of primate social cognition that may shape dyadic relationships and social network structure.

animal behavior and cognition↗

bioRxiv2026

Attention Across Scales: From Individual Variation to Social Hierarchies and Brain Networks in Semi-Free-Ranging Macaques

Attention is a fundamental brain function supporting perception, decision-making, and social behavior, and its dysfunction profoundly impairs daily life. It is both dynamic and stable, varying across observations and individuals, changing across the lifespan, and being shaped by social and environmental experience. Yet capturing this complexity remains a central challenge in neuroscience. Here, we integrated longitudinal behavioral assessments of semi-free-ranging macaques living in naturalistic social groups with resting-state fMRI. We quantified performance across days, ages, and social hierarchies and related it to intrinsic brain organization. Distinct attentional phenotypes emerged, including individuals with reduced attentional control. Performance followed an inverted-U lifespan trajectory, improving from childhood to adulthood before declining. Social status modulated attentional performance. Critically, nonlinear lifespan trajectories and associations with individual attentional differences were most clearly expressed in frontoparietal connectivity. Together, these findings reveal how sustained attention is organized across scales, providing a biological framework for its individual diversity, social modulation, and neural basis.

neuroscience↗

bioRxiv2026

A Social Affordance Framework for Understanding Approach Decisions in Wild Crested Macaques (Macaca nigra)

Approaching conspecifics is a fundamental component of social interactions. Such decisions are typically investigated through the study of social relationships (e.g., kinship, dominance, affiliation) and their impact. In the framework, the role of social affordances, i.e., interaction opportunities arising from the immediate social environment, remains poorly understood. We investigated how context-dependent factors shape approach decisions in wild crested macaques (Macaca nigra) in North Sulawesi, Indonesia. From September 2024 to May 2025, we collected data on 27 adults (20 females, 7 males) using focal observations and an approach-specific protocol recording neighbours identities and behaviours at the initiation of close-proximity approaches (<1 body length). We first compared data collected during approaches with focal data, then conducted within-approach analyses contrasting approached partners and bystanders. We further tested the effects of behavioural state, subgroup size and composition, including infant presence. Bayesian models revealed that affiliative, neutral, and grooming behaviours were more frequent in approach contexts than in general observations. Within approaches, individuals avoided congeners already engaged in grooming and approached individuals in neutral or affiliative states (e.g., lip-smacking, embracing). Macaques globally approached more isolated individuals or dyads. When multiple subgroups were present (i.e., multiple choices), the likelihood of being approached increased with subgroup size and was higher in subgroups containing infants. These findings indicate that macaques use behavioural cues and local social density as affordance signals, adjusting approach decisions to maximize interaction opportunities and navigate complex social environments.

animal behavior and cognition↗

bioRxiv2025

Neuroanatomical foundations of social tolerance across macaque species

The macaque genus includes 25 species with diverse social systems, ranging from low to high social tolerance grades. Such interspecific behavioral variability provides a unique model to tackle the evolutionary foundation of primate social brain. Yet, the neuroanatomical correlates of these social tolerance grades remain unknown. To address this question, we expressed social tolerance grades within a novel cognitive framework and analyzed post-mortem structural scans from 12 macaque species. Our results show that amygdala volume is a subcortical predictor of macaques social tolerance, with high tolerance species exhibiting larger amygdala than low tolerance ones. We further investigated the developmental trajectory of amygdala across social grades and found that intolerant species showed a gradual increase in relative amygdala volume across the lifespan. Unexpectedly, tolerant species exhibited a decrease in relative amygdala volume across the lifespan, contrasting with the age-related increase observed in intolerant species--a developmental pattern previously undescribed in primates. Taken together, these findings provide valuable insights into the cognitive, neuroanatomical and evolutionary basis of primates social behaviors.

neuroscience↗

bioRxiv2025

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↗

bioRxiv2021

Orbitofrontal cortex contributes to the comparison of values underlying economic choices

Economic choices between goods entail the computation and comparison of subjective values. Previous studies examined neuronal activity in the orbitofrontal cortex (OFC) of monkeys choosing between different types of juices. Three groups of neurons were identified: offer value cells encoding the value of individual offers, chosen juice cells encoding the identity of the chosen juice, and chosen value cells encoding the value of the chosen offer. The encoded variables capture both the input (offer value) and the output (chosen juice, chosen value) of the decision process, suggesting that values are compared within OFC. Recent work demonstrates that choices are causally linked to the activity of offer value cells. Conversely, the hypothesis that OFC contributes to value comparison has not been confirmed. Here we show that weak electrical stimulation of OFC specifically disrupts value comparison without altering offer values. This result implies that neuronal populations in OFC participate in the decision process. SignificanceEconomic choices encompass two mental stages: values are assigned to the available offers, and a decision is made by comparing values. Previous work showed that choices are causally related to offer values encoded in the orbitofrontal cortex (OFC). Conversely, the neural underpinnings of value comparison remain poorly understood. Here we show that weak electrical stimulation of OFC selectively disrupts the decision process without affecting offer values. Hence, neurons in OFC contribute to value comparison.

neuroscience↗

bioRxiv2021

Neuronal origins of biases in economic choices under sequential offers

Economic choices are characterized by a variety of biases. Understanding their origins is a long-term goal for neuroeconomics, but progress on this front has been limited. Here we examined choice biases observed when two goods are offered sequentially. In the experiments, rhesus monkeys chose between different juices offered simultaneously or in sequence. Choices under sequential offers were less accurate (higher variability). They were also biased in favor of the second offer (order bias) and in favor of the preferred juice (preference bias). Analysis of neuronal activity recorded in orbitofrontal cortex revealed that these phenomena emerged at different computational stages. The lower choice accuracy reflected weaker offer value signals (valuation stage), the order bias emerged during value comparison (decision stage), and the preference bias emerged late in the trial (post-comparison). Our approach, leveraging recent notions on the neural mechanisms of economic decisions, may shed light on other aspects of choice behavior.

neuroscience↗

bioRxiv2021

Economic Choices under Simultaneous or Sequential Offers Rely on the Same Neural Circuit

A series of studies in which monkeys chose between two juices offered in variable amounts identified in the orbitofrontal cortex (OFC) different groups of neurons encoding the value of individual options (offer value), the binary choice outcome (chosen juice) and the chosen value. These variables capture both the input and the output of the choice process, suggesting that the cell groups identified in OFC constitute the building blocks of a decision circuit. Several lines of evidence support this hypothesis. However, in previous experiments offers were presented simultaneously, raising the question of whether current notions generalize to when goods are presented or are examined in sequence. Recently, Ballesta and Padoa-Schioppa (2019) examined OFC activity under sequential offers. An analysis of neuronal responses across time windows revealed that a small number of cell groups encoded specific sequences of variables. These sequences appeared analogous to the variables identified under simultaneous offers, but the correspondence remained tentative. Thus in the present study we examined the relation between cell groups found under sequential versus simultaneous offers. We recorded from the OFC while monkeys chose between different juices. Trials with simultaneous and sequential offers were randomly interleaved in each session. We classified cells in each choice modality and we examined the relation between the two classifications. We found a strong correspondence - in other words, the cell groups measured under simultaneous offers and under sequential offers were one and the same. This result indicates that economic choices under simultaneous or sequential offers rely on the same neural circuit. Significance StatementResearch in the past 20 years has shed light on the neuronal underpinnings of economic choices. A large number of results indicates that decisions between goods are formed in a neural circuit within the orbitofrontal cortex (OFC). In most previous studies, subjects chose between two goods offered simultaneously. Yet, in daily situations, goods available for choice are often presented or examined in sequence. Here we recorded neuronal activity in the primate OFC alternating trials under simultaneous and under sequential offers. Our analyses demonstrate that the same neural circuit supports choices in the two modalities. Hence current notions on the neuronal mechanisms underlying economic decisions generalize to choices under sequential offers.

neuroscience↗

bioRxiv2020

Assessing the reliability of an automated method for measuring dominance hierarchy in nonhuman primates

Among animals societies, dominance is an important social factor that influences inter-individual relationships. However, assessing dominance hierarchy can be a time-consuming activity which is potentially impeded by environmental factors, difficulties in the recognition of animals, or through the disturbance of animals during data collection. Here we took advantage of novel devices, Machines for Automated Learning and Testing (MALT), designed primarily to study nonhuman primates cognition - to additionally measure the social structure of a primate group. When working on a MALT, an animal can be replaced by another; which could reflect an asymmetric dominance relationship (or could happen by chance). To assess the reliability of our automated method, we analysed a sample of the automated conflicts with video scoring and found that 75% of these replacements include genuine forms of social displacements. We thus first designed a data filtering procedure to exclude events that should not be taken into account when automatically assessing social hierarchies in monkeys. Then, we analysed months of daily use of MALT by 25 semi-free ranging Tonkean macaques (Macaca tonkeana) and found that dominance relationships inferred from these interactions strongly correlate with the ones derived from observations of spontaneous agonistic interactions collected during the same time period. We demonstrate that this method can be used to assess the evolution of individual social status, as well as group-wide hierarchical stability longitudinally with minimal research labour. Further, it facilitates a continuous assessment of dominance hierarchies, even during unpredictable environmental or challenging social events. Altogether, this study supports the use of MALT as a reliable tool to automatically and dynamically assess social status within groups of nonhuman primates, including juveniles.

animal behavior and cognition↗

bioRxiv2020

Values Encoded in Orbitofrontal Cortex Are Causally Related to Economic Choices

It has long been hypothesized that economic choices rely on the assignment and comparison of subjective values. Indeed, when agents make decisions, neurons in orbitofrontal cortex encode the values of offered and chosen goods. Moreover, neuronal activity in this area suggests the formation of a decision. However, it is unclear whether these neural processes are causally related to choices. More generally, the evidence linking economic choices to value signals in the brain remains correlational. We address this fundamental issue using electrical stimulation in rhesus monkeys. We show that suitable currents bias choices by increasing the value of individual offers. Furthermore, high-current stimulation disrupts both the computation and the comparison of subjective values. These results demonstrate that values encoded in orbitofrontal cortex are causal to economic choices.

neuroscience↗

bioRxiv2019

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↗

bioRxiv2019

Mechanisms of Economic Decisions under Sequential Offers

Binary choices between goods are thought to take place in orbitofrontal cortex (OFC). However, current notions emerged mostly from studies where two offers were presented simultaneously, and other work suggested that choices under sequential offers rely on fundamentally different mechanisms. Here we recorded from the OFC of macaques choosing between two juices offered sequentially. Analyzing neuronal responses across time windows, we discovered different groups of neurons that closely resemble those identified under simultaneous offers, suggesting that decisions in the two modalities are formed in the same neural circuit. Building on this result, we examined four hypotheses on the decision mechanisms. OFC neurons encoded goods and values in a juice-based representation (labeled lines). Contrary to previous assessments, decisions did not involve mutual inhibition between pools of offer value cells. Instead, decisions involved mechanisms of circuit inhibition, whereby each offer value indirectly inhibits neurons encoding the opposite choice outcome. These results reconcile disparate findings and provide a unitary account for the neuronal mechanisms underlying economic decisions.

neuroscience↗