Researchers have found that the size of the amygdala – a region of the brain involved in processing emotions – could be linked to social tolerance in macaque monkeys.
Their research, published today in eLife as the final Version of Record after appearing previously as a Reviewed Preprint, is described by the editors as important work with a convincing methodological approach, offering new insights into the neural basis of social and emotional processing.
Navigating social life in primate societies requires substantial cognitive resources. Individuals must track multiple relationships, regulate their own behaviour and adapt flexibly to changing social contexts. The macaque genus includes 25 species with diverse social systems, ranging from low to high social tolerance grades.
"Links between the size of brain structures and social environment have been reported in humans and non-human primates," says lead author Sarah Silvère, a PhD student at the Laboratoire de Neurosciences Cognitives et Adaptatives (LNCA), Strasbourg, France, and le Centre de Primatologie (CdP) of the University of Strasbourg, Niederhausbergen, France. "We wanted to understand how variation in brain structure volume is linked to social tolerance, and whether this is an innate feature or acquired through socialisation within more or less tolerant social environments."
The team used a database of magnetic resonance imaging (MRI) scans of macaque brains – built from opportunistically collected samples, including individuals housed in zoos and animals from the Simian Laboratory Europe (SILABE) platform of the University of Strasbourg – to compare the size of the amygdala and the hippocampus across 12 species. They organised 18 well-known behavioural traits into three core aspects of social tolerance. The first, socio-cognitive demands, refer to the cognitive resources needed to process, monitor and adapt to complex social environments. The second – behavioural inhibition – includes regulating impulsive behaviour, aggression or inappropriate responses during social interactions. And the third category, predictability of the social environment, reflects how structured and foreseeable social interactions are in a community, with tolerant species having more fluid relationships.
For each category, the team produced hypotheses for how the volume of the amygdala and hippocampus might vary and tested them using MRI data for 12 macaque species that represent four grades of social tolerance, including two that had never been scanned before and another rarely studied species.
The team found that the volume of the amygdala – but not the hippocampus – was positively linked to the grade of social tolerance, with high-tolerance species showing larger amygdala than low-tolerance species. This differs from previous studies that say the amygdala primarily supports aggressive behaviours and suggests instead that the amygdala also acts as a multifunctional hub embedded within complex social networks in the brain.
"Larger amygdala in socially tolerant species may reflect an enhanced capacity to process complex social information, facilitate better social interactions and manage conflicts," explains Silvère.
For the hippocampus, a smaller volume was observed in socially intolerant species compared with tolerant species between the age of 13 and 18 years but, besides this, there was inconclusive evidence of any difference.
The team also found, to their surprise, that the developmental trajectories of the amygdala differed. Grade 1 intolerant species showed an increase in amygdala volume across their lifespan, while grade 4 tolerant species had a significantly higher amygdala volume at the start of their lives, which decreased with age.
In accordance with the team's hypotheses, their results showed that social tolerance is rooted in neuroanatomical differences that can be observed early in life, and that these structural differences are influenced by social styles throughout individual lifespans.
"To our knowledge, our study is the first to report neuroanatomical links to social tolerance grades based on MRI data, and provides novel insights into the relationship between amygdala volume and social tolerance in macaques," concludes senior author Sébastien Ballesta, Associate Professor at LNCA and CdP of the University of Strasbourg.
"These findings have profound implications for our understanding of social brain evolution, as well as underscoring the importance of developmental stage and the social environment in shaping neuroanatomical adaptations. Our work highlights that comparing closely related macaque species represents a valuable natural framework for investigating the impact of the social environment on brain development, paving the way for future research to unravel the complexities of brain evolution and sociality."
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