Biology subjects

Chang, S. W. C.

Publications and source records attributed to Chang, S. W. C..

13 recordsLinked to original sources

bioRxiv2026

Division of vocal signaling in cooperating marmoset dyads

Communication enables partners to coordinate actions toward shared goals, but how vocal communication is organized during cooperation remains poorly understood. We recorded vocalizations from three common marmoset (Callithrix jacchus) dyads as they learned a mutual cooperation task requiring coordinated lever pulls for reward. Vocal behavior was divided by social hierarchy: dominants produced t-peeps, whereas subordinates produced chirps. Interestingly, dominant t-peeps followed failed cooperative pulls, peaked when cooperative bouts broke down, and declined after learning. By contrast, subordinate chirps followed successful pulls, accumulated during sustained cooperation, and persisted after learning. Each call was linked to the task role of the caller: dominant animals t-peeped more in sessions they led, and subordinates chirped mainly after cooperations they initiated, associations that sharpened with learning. Thus, social rank determined which vocal signal a partner used, whereas task role and the state of cooperation determined when to communicate. These complementary vocal signals of failure and success reveal how hierarchy, task role and task phase organize communication during joint action in cooperating marmosets.

neuroscience↗

bioRxiv2025

Canonical decision computations underlie behavioral and neural signatures of cooperation in primates

Successful cooperation requires dynamic integration of social cues. However, the neural mechanisms supporting this complex process remain unknown. Here, we reveal that the primate dorsomedial prefrontal cortex (dmPFC) implements a gaze-dependent social evidence accumulation process to guide cooperative decisions in freely moving marmoset dyads. A drift-diffusion process in which the partners action variability is accumulated by social gaze best explains the cooperative actions of the actor. Single-neuron recordings in dmPFC revealed a direct neural correlate: the slope of predictive ramping activity mapped directly onto the rate of evidence accumulation, while baseline firing, modulated by prior outcomes, mapped onto the initial bias. At the population level, the geometry of dmPFC neural trajectories reflected the strength of social evidence and was linked to cooperative success. Together, these findings establish a multi-level neural mechanism for transforming active sensing into a decision variable, linking a canonical computation to cooperative behavior in a naturalistic setting.

neuroscience↗

bioRxiv2025

Compositionality of social gaze in the prefrontal-amygdala circuits

Social gaze underpins primate communication, yet the neural principles enabling its flexibility remain unknown. Each social gaze can be deconstructed into three primitives: gaze content, social state, and gaze duration. To reduce dimensionality and facilitate generalization, the brain needs to represent these primitives in an abstract format. Here we show that social gaze is governed by a compositional code built from these primitives in the brain. In male and female macaques (neural recordings in two males) engaged in real-life social gaze interaction, behavior analyses revealed that partner responses were determined by how primitives were combined, rather than by their independent sums, providing evidence for behavioral compositionality. The basolateral amygdala and the anterior cingulate gyrus represented content and state in an abstract format and orthogonally to one another, whereas the dorsomedial prefrontal and orbitofrontal cortices exhibited limited generalization. Linear mixed-selective neurons encoding both content and state in the basolateral amygdala and the anterior cingulate gyrus, but not in the other two areas, facilitated the abstraction underlying generalization. Moreover, distinct channels routed content and state information across prefrontal-amygdala circuits to minimize interference, which was mediated by linear mixed selectivity neurons. These findings identify a neural grammar for social gaze, revealing compositional computations as a principle of flexible social communication.

neuroscience↗

bioRxiv2025

Diverse and Flexible Strategies Enable Successful Cooperation in Marmoset Dyads

In humans, cooperation relies on advanced social cognition, but the extent to which these mechanisms support cooperation in nonhuman primates remains unclear. To investigate this, we examined freely moving marmoset dyads in a cooperative lever-pulling task. Marmosets successfully coordinated actions, relying on social vision rather than environmental cues. Blocking visual access or replacing the partner with an automated agent disrupted coordination. Causal dependencies between social gaze and pull actions revealed both gaze-dependent and gaze-independent strategies. Cooperation depended on social relationships, including dominance, kinship, and sex. Remarkably, marmosets adapted strategies based on partner identity, indicating rapid social learning and memory. Altogether, these findings show that flexible, cognitively driven cooperation extends more broadly across primates than previously recognized, informing our understanding of cooperative behaviors mechanisms and evolution.

neuroscience↗

bioRxiv2024

Development of a Marmoset Apparatus for Automated Pulling (MarmoAAP) to Study Cooperative Behaviors

In recent years, the field of neuroscience has increasingly recognized the importance of studying animal behaviors in naturalistic environments to gain deeper insights into ethologically relevant behavioral processes and neural mechanisms. The common marmoset (Callithrix jacchus), due to its small size, prosocial nature, and genetic proximity to humans, has emerged as a pivotal model toward this effort. However, traditional research methodologies often fail to fully capture the nuances of marmoset social interactions and cooperative behaviors. To address this critical gap, we developed the Marmoset Apparatus for Automated Pulling (MarmoAAP), a novel behavioral apparatus designed for studying cooperative behaviors in common marmosets. MarmoAAP addresses the limitations of traditional behavioral research methods by enabling high-throughput, detailed behavior outputs that can be integrated with video and audio recordings, allowing for more nuanced and comprehensive analyses even in a naturalistic setting. We also highlight the flexibility of MarmoAAP in task parameter manipulation which accommodates a wide range of behaviors and individual animal capabilities. Furthermore, MarmoAAP provides a platform to perform investigations of neural activity underlying naturalistic social behaviors. MarmoAAP is a versatile and robust tool for advancing our understanding of primate behavior and related cognitive processes. This new apparatus bridges the gap between ethologically relevant animal behavior studies and neural investigations, paving the way for future research in cognitive and social neuroscience using marmosets as a model organism.

neuroscience↗

bioRxiv2024

Automated 3D analysis of social head-gaze behaviors in freely moving marmosets

Social communication relies on the ability to perceive and interpret the direction of others attention, and is commonly conveyed through head orientation and gaze direction in humans and nonhuman primates. However, traditional social gaze experiments in nonhuman primates require restraining head movements, significantly limiting their natural behavioral repertoire. Here, we developed a novel framework for accurately tracking facial features and three-dimensional head gaze directions of multiple freely moving common marmosets (Callithrix jacchus). By combining deep learning-based computer vision tools with triangulation algorithms, we were able to track the facial features of marmoset dyads within an arena. This method effectively generates dynamic 3D geometrical facial frames while overcoming common challenges like occlusion. To detect the head gaze direction, we constructed a virtual cone, oriented perpendicular to the facial frame. Using this pipeline, we quantified different types of interactive social gaze events, including partner-directed gaze and joint gaze to a shared spatial location. We observed clear effects of sex and familiarity on both interpersonal distance and gaze dynamics in marmoset dyads. Unfamiliar pairs exhibited more stereotyped patterns of arena occupancy, more sustained levels of social gaze across social distance, and increased social gaze monitoring. On the other hand, familiar pairs exhibited higher levels of joint gazes. Moreover, males displayed significantly elevated levels of gazes toward females faces and the surrounding regions, irrespective of familiarity. Our study reveals the importance of two key social factors in driving the gaze behaviors of a prosocial primate species and lays the groundwork for a rigorous quantification of primate behaviors in naturalistic settings.

animal behavior and cognition↗

bioRxiv2023

Closed-loop microstimulations of the orbitofrontal cortex during real-life gaze interaction enhance dynamic social attention

The prefrontal cortex is extensively involved in social exchange. During dyadic gaze interaction, multiple prefrontal areas exhibit neuronal encoding of social gaze events and context-specific mutual eye contact, supported by a widespread neural mechanism of social gaze monitoring. To explore causal manipulation of real-life gaze interaction, we applied weak closed-loop microstimulations that were precisely triggered by specific social gaze events to three prefrontal areas in monkeys. Microstimulations of orbitofrontal cortex (OFC), but not dorsomedial prefrontal or anterior cingulate cortex, enhanced momentary dynamic social attention in the spatial dimension by decreasing distance of ones gaze fixations relative to partner monkeys eyes. In the temporal dimension, microstimulations of OFC reduced the inter-looking interval for attending to another agent and the latency to reciprocate others directed gaze. These findings demonstrate that primate OFC serves as a functionally accessible node in controlling dynamic social attention and suggest its potential for a therapeutic brain interface.

neuroscience↗

bioRxiv2022

Individual Decision-Making Underlying the Tragedy of the Commons

Group decision-making is common in everyday life, whether a family is sharing a meal or a corporation is dividing profits. Research in economics on group decision-making has coalesced into a theory known as the tragedy of the commons, which states that resources are inevitably overused when shared by a group. However, even while multiple approaches to mitigating overuse of common resources have been put forward, notable counterexamples to the tragedy of the commons exist such that groups are ultimately able to avoid resource overuse. Development of a computerized paradigm amenable to behavioral modeling and simulation analyses could allow for exploration of whether resources will be overused in a given group of individuals and allow for the rapid testing of behavioral interventions designed to reduce instances of resource overuse. Using a newly developed group decision-making task, we studied how participants made decisions to utilize shared resources for the potential to receive a larger amount of money or conserve resources for a smaller amount of money. Using behavioral modeling, we found that valuation of resource overuse is most impacted only when an exceptionally small amount of resources are remaining. Using computational analyses, we were able to differentiate individual participants by both group earnings and self-reported social attitudes in ways that correlated with their willingness to utilize resources. These results signify the importance of individual differences in group composition regarding the tragedy of the commons, emphasizing the impact of the attitudes and behaviors of individual group members in predicting shared resource use.

animal behavior and cognition↗

bioRxiv2022

Social Curiosity in Monkeys

Humans and nonhuman animals derive value from many different sources. Some of these sources, notably primary reinforcers like food, are clearly rewarding and can powerfully shape our behaviors. Other sources of reward, such as information, are more intangible and abstract. Like humans, nonhuman primates also find information inherently rewarding, displaying a preference to reveal information about upcoming primary reinforcers even though the information has no bearing on the outcome itself. For animals living in social groups, the need for information extends beyond primary reinforcers like food. They need to acquire information from others or about others. This is especially true for animals, such as nonhuman primates, which live in large and often hierarchically organized societies, where processing social information for the purpose of learning and socializing can be just as critical to survival. To quantify curiosity for knowing social information in monkeys, we extend the advanced informationseeking paradigm (Bromberg-Martin and Hikosaka, 2009) into the realm of abstract, social information. We first replicated the finding that monkeys prefer advanced information about juice size (Bromberg-Martin and Hikosaka, 2009). We next trained monkeys on a social variant of this task. In the advanced social information-seeking task, monkeys had the option to choose a cue that tells them in advance the valence, or facial expression, on a monkeys face that they will be viewing before receiving the invariant amount of juice. Even though this cue did not impact which facial expression the monkeys would see, they preferred to know the valence of the facial expression in advance. Our results indicate that information-seeking behavior generalizes to seeking social information. Our findings also suggest that curiosity in nonhuman primates can be translated into increasingly abstract levels of information.

animal behavior and cognition↗

bioRxiv2021

Single-cell foundations of live social gaze interaction in the prefrontal cortex and amygdala

Social gaze interaction powerfully shapes interpersonal communication in humans and other primates. However, little is known about the neural underpinnings of these social behavioral exchanges. Here, we studied neural responses associated with naturalistic, face-to-face, social gaze interactions between pairs of macaques. We examined spiking activity in a large number of neurons spanning four different brain regions involved in social behaviors - the amygdala, orbitofrontal cortex, anterior cingulate cortex, and dorsomedial prefrontal cortex. We observed widespread single-cell representations of social gaze interaction functionalities in these brain regions - social discriminability, social gaze monitoring, and mutual eye contact selectivity. Many of these neurons discriminated looking at social versus non-social stimuli with rich temporal heterogeneity, or parametrically tracked the gaze positions of oneself or the conspecific. Furthermore, many neurons displayed selectivity for mutual eye contact as a function of the initiator or follower of mutual gaze events. Crucially, a significant proportion of neurons coded for more than one of these three signatures of social gaze interaction, supporting the recruitment of partially overlapping neuronal ensembles. Our findings emphasize integrated contributions of the amygdala and prefrontal circuits within the social interaction networks in processing real-life social interactions.

neuroscience↗

bioRxiv2021

Increasing central serotonin with 5-HTP disrupts the inhibition of social gaze in non-human primates

To competently navigate the world, individuals must flexibly balance distinct aspects of social gaze, orienting toward others and inhibiting orienting responses, depending on the context. These behaviors are often disrupted in patient populations treated with serotonergic drugs. However, the field lacks a clear understanding of how the serotonergic system mediates social orienting and inhibiting behaviors. Here, we tested how increasing central concentrations of serotonin with the direct precursor 5-Hydroxytryptophan (5-HTP) would modulate the ability of rhesus macaques to use eye movements to flexibly orient to, or inhibit orienting to, faces. Systemic administrations of 5-HTP effectively increased central serotonin levels and impaired flexible orientation and inhibition. Critically, 5-HTP selectively impaired the ability of monkeys to inhibit orienting to face images, whereas it similarly impaired orienting to face and control images. 5-HTP also caused monkeys to perseverate on their gaze responses, making them worse at flexibly switching between orientating and inhibiting behaviors. Furthermore, the effects of 5-HTP on performance correlated with a constriction of the pupil, an increased time to initiate trials, and an increased reaction time, suggesting that the disruptive effects of 5-HTP on social gaze behaviors are likely driven by a downregulation of arousal and motivational states. Taken together, these findings provide causal evidence for a modulatory relationship between 5-HTP and social gaze behaviors in non-human primates and offer translational insights for the role of the serotonergic system in social gaze.

neuroscience↗

bioRxiv2020

Autonomic arousal tracks outcome salience not valence in monkeys making social decisions

The evolutionary and neural underpinnings of human prosociality are still largely unknown. A growing body of evidence suggests that some species find the sight of another individual receiving a reward reinforcing, often called vicarious reinforcement. One hypothesis is that vicarious reward is reinforcing because it is arousing like a primary reward. We evaluated this hypothesis by measuring the autonomic pupil response of eight monkeys across two laboratories in two different versions of a vicarious reinforcement paradigm. Monkeys were cued as to whether an upcoming reward would be delivered to them, another monkey, or nobody and could accept or decline the offer. As expected, all monkeys in both laboratories showed a marked preference for juice to the self, together with a reliable prosocial preference for juice to a social partner compared to juice to nobody. However, contrary to the autonomic arousal hypothesis, we found that pupils were widest in anticipation of juice to the self, moderately-sized in anticipation of juice to nobody, and narrowest in anticipation of juice to a social partner. This effect was seen across both laboratories and regardless of specific task parameters. The seemingly paradoxical pupil effect can be explained by a model in which pupil size tracks outcome salience, prosocial tendencies track outcome valence, and the relation between salience and valence is U-shaped.

animal behavior and cognition↗

bioRxiv2019

Specialized medial prefrontal-amygdala coordination in prosocial and antisocial decision-making

Social behaviors recruit multiple cognitive processes requiring coordinated interactions among brain regions. Oscillatory coupling provides one mechanism for cortical and subcortical neurons to synchronize their activity. However, it remains unknown how neurons from different nodes in the social brain network interact when making social decisions. We investigated neuronal coupling between the rostral anterior cingulate gyrus of the medial prefrontal cortex and the basolateral amygdala while monkeys expressed context-dependent positive other-regarding preference (ORP) or negative ORP impacting the reward of another monkey. We found an enhanced synchronization between the two nodes for positive ORP, but a suppressed synchronization for negative ORP. These interactions occurred in dedicated frequency channels depending on the area contributing spikes, exhibited a specific directionality of information flow associated with expressing positive ORP, and could be used to decode social decisions. These findings support that specialized coordination in the medial prefrontal-amygdala network underlies social decision preference.

neuroscience↗