Biology subjects

Fagan, N. A.

Publications and source records attributed to Fagan, N. A..

6 recordsLinked to original sources

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↗

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

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

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↗