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An understanding of third-party friendships in a tolerant macaque.

ABSTRACT: Complex societies are shaped by social relationships between multiple individuals. The pressure to track these relationships has driven the evolution of social cognition in primates. Importantly, it can be adaptive to track not only personal relationships, but also those established between third-parties. Primates have knowledge about others' dominance hierarchies and kinship, but we do not know to what extent they also understand friendships. In a playback experiment, Tonkean macaques were presented with simulated conflicts involving third-party female dyads who were established friends or non-friends. Hearing a conflict between friends elicited a stronger behavioural response in listeners (i.e. an increase in looking time) compared to hearing a conflict between non-friends. Conflicts between friends are likely to represent a greater disruption of the social group and structure of the network, and therefore this difference in response may represent an adaptive strategy employed by the macaques to selectively monitor important social interactions in the group. These findings provide evidence that Tonkean macaques (and potentially other primates) can classify the relationships of others based on their degree of friendship and additionally, confirms the important role friendships have within the societies of social primates.

SUBMITTER: Whitehouse J

PROVIDER: S-EPMC7300006 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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An understanding of third-party friendships in a tolerant macaque.

Whitehouse Jamie J Meunier Hélène H

Scientific reports 20200617 1

Complex societies are shaped by social relationships between multiple individuals. The pressure to track these relationships has driven the evolution of social cognition in primates. Importantly, it can be adaptive to track not only personal relationships, but also those established between third-parties. Primates have knowledge about others' dominance hierarchies and kinship, but we do not know to what extent they also understand friendships. In a playback experiment, Tonkean macaques were pres ...[more]

PMID: 32555440

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Project description:UNLABELLED:The evolved capacity for third-party punishment is considered crucial to the emergence and maintenance of elaborate human social organization and is central to the modern provision of fairness and justice within society. Although it is well established that the mental state of the offender and the severity of the harm he caused are the two primary predictors of punishment decisions, the precise cognitive and brain mechanisms by which these distinct components are evaluated and integrated into a punishment decision are poorly understood. Using fMRI, here we implement a novel experimental design to functionally dissociate the mechanisms underlying evaluation, integration, and decision that were conflated in previous studies of third-party punishment. Behaviorally, the punishment decision is primarily defined by a superadditive interaction between harm and mental state, with subjects weighing the interaction factor more than the single factors of harm and mental state. On a neural level, evaluation of harms engaged brain areas associated with affective and somatosensory processing, whereas mental state evaluation primarily recruited circuitry involved in mentalization. Harm and mental state evaluations are integrated in medial prefrontal and posterior cingulate structures, with the amygdala acting as a pivotal hub of the interaction between harm and mental state. This integrated information is used by the right dorsolateral prefrontal cortex at the time of the decision to assign an appropriate punishment through a distributed coding system. Together, these findings provide a blueprint of the brain mechanisms by which neutral third parties render punishment decisions. SIGNIFICANCE STATEMENT:Punishment undergirds large-scale cooperation and helps dispense criminal justice. Yet it is currently unknown precisely how people assess the mental states of offenders, evaluate the harms they caused, and integrate those two components into a single punishment decision. Using a new design, we isolated these three processes, identifying the distinct brain systems and activities that enable each. Additional findings suggest that the amygdala plays a crucial role in mediating the interaction of mental state and harm information, whereas the dorsolateral prefrontal cortex plays a crucial, final-stage role, both in integrating mental state and harm information and in selecting a suitable punishment amount. These findings deepen our understanding of how punishment decisions are made, which may someday help to improve them.

Dataset Information

An understanding of third-party friendships in a tolerant macaque.

Publications

An understanding of third-party friendships in a tolerant macaque.

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