Toward neuroanatomical and cognitive foundations of macaque social tolerance grades.

内容摘要

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. Macaque monkeys live under a variety of social regimes. Some species flourish within highly structured, hierarchical societies, while others navigate more tolerant yet less predictable social networks. Primatologists have categorised these social differences, including how often reconciliation occurs after conflicts, into four levels of social tolerance. However, the neuronal mechanisms underlying these social variations remain poorly understood. Closely related species offer a natural laboratory for studying the social brain in primates. To investigate how neural networks may have evolved in response to differing social challenges, Silvère et al. analysed 43 brain scans from 12 macaque species. All data were gathered from animals that had died of natural or accidental causes The scans showed that the relative size of a species’ amygdala – a brain region involved in emotional responses, decision-making, and memory – correlates with its level of social tolerance. For example, low-tolerance species are born with a smaller amygdala, which grows larger with age. Conversely, in more socially tolerant species, the amygdala decreases in size as they age, contrasting with findings in other primates, including humans. These findings imply that living in a more tolerant social environment could impose greater cognitive demands on the brain, with the amygdala possibly playing a part in complex social cognition. In contrast, the volume of a brain region called the hippocampus revealed more variable differences across social grades among macaques, with a more significant effect observed only in individuals aged between 13 and 18 years. Additionally, differences in hippocampal volume also varied among monkeys living in different areas, supporting the idea that certain regions contribute to social cognitive processes in tolerant species, particularly during developmental phases linked to social maturation. Exploring natural variation in brain evolution and function opens new avenues for primate neuroscience. A more extensive comparative analysis across all living primate species could further clarify evolutionary pathways. Moreover, identifying neural networks that are either evolutionarily conserved or highly variable may help shape new research directions aimed at understanding the biological basis of neurodivergence.