Neuroimaging of social networks in semi-free ranging monkeys – SocialNeuroNet

Most primates live in complex societies composed of dozens of individuals and structured by features such as dominance hierarchy, friendship and kinship; giving rise to topological variables such as centrality, social distance or betweenness. Being able to represent these features is key to social navigation success. How can primates’ nervous system handle and represent the complexity emerging from their own social networks? To which extent these mental and neural representations will be the same in species of monkeys living in more tolerant societies?

This interdisciplinary project, at the interface of Neuroscience and Cognitive Ethology, will tackle this issue by bringing neuroimaging to semi-free ranging macaques from 3 species. While we know that monkeys possess representations of their own group structures and members, quantitative data are missing to investigate the level of abstraction involved in such challenging mental processes. Inter-individual and -species differences in social cognition within the macaque genus will be investigated (Aim1). Pictures and video footage of each member of semi-free ranging troops of macaques will be taken. Using these stimuli in cognitive tasks displayed with innovative autonomous, we will address the mental representation of hierarchy, friendship and kinship of monkey’s own social group.

Further, these representations are thought to be formed by the social brain, an evolutionary conserved set of brain regions associated with social cognition in primates. Neural representation of social networks has been studied in Humans using fMRI. Topological variables have been found to be represented by three different networks of brain areas. Social distance is represented in a large cluster centered notably in the posterior superior temporal cortex; centrality in mPFC, temporal pole, precuneus; and betweenness in middle superior temporal cortex. However, the evolutionary trajectories and the causal role of these neural networks in social cognition are yet to be discovered. Under laboratory conditions, reproducing, and thus studying, the neural representation of the natural complexity of monkeys’ social networks is challenging, if not impossible. Addressing this neuroethological question in non-human primates has been hampered by scientific and technical barriers. Lifting them requires a novel approach that brings together neuroimaging, neuro-perturbation techniques and social knowledge of semi-free ranging monkeys. Six monkeys from a semi-free ranging social group, will be involved in our neuroimaging and neuroperturbation studies. Neural circuits necessary for representing social networks in rhesus macaques (Aim2), will be investigated with neuroimaging. Causal relationship between the identified neural networks and mental representation of own social networks will be studied using transcranial ultrasound brain stimulation while the animal will perform previously learned cognitive tasks.

Finally, different macaque species display different social behaviours and structures that have been conceptualized as a continuum in a social tolerance. The neural basis of these differences are yet to be uncovered. Previous studies of non-human primates’ social brains have been mostly restricted to rhesus macaques, an aggressive and intolerant species. Continuities and singularities in the social brain within the macaque genus (Aim3) will be characterized using comparative anatomical and resting-state MRI carried in 65 semi-free ranging animals from 3 macaque species.

The description of the nervous system of socially tolerant species of monkeys will help to puzzle out the functioning and evolutionary roots of our social brain. Combining these different but complementary approaches will uncover mental and neural representations of primate social network topology and thus provide fundamental insight into how brains and social beings engage in a shared complex world.