Neuroethology of monkey social behavior – NEMOS

Humans live in a complex environment within which they can navigate in purposeful or exploratory manners, seeking shelter, resources, or mere entertainment. With the exception of forest-dwelling hermits, the human living space is intrinsically social. In recent years, social scientists and ethologists have been using similar approaches to investigate the evolution and dynamics of social networks. In parallel, efforts have been made to uncover the brain mechanisms of sociality, with important implications for pathologies like autistic spectrum disorders, anxiety or depression, that are often characterized by anomalous or reduced social interactions. Animal studies, mostly conducted in small rodents, have identified genes and neuromodulators systems that are implicated in social behaviours. Yet, our knowledge remains somewhat fragmentary as key data is lacking on animal species close to humans both in brain structure and behavioural repertoire. The non-human primate may constitute a valuable model in this respect since, like humans, monkeys live in large groups, collectively seek and share food resources, use multimodal communication involving visual and vocal signals. We propose to investigate the neural systems implicated in naturally occurring social behaviour of macaque monkeys, combining quantitative measures of social interactions in a semi-naturalistic setting with pharmacological manipulations and remote recording of brain activity. We adopt a neuro-ethological approach that is both exploratory and hypothesis-driven. In a first step, species-typical behaviours will be recorded in small groups of monkeys, using “high-throughput” video tracking and social network analysis to quantify use of space, connectedness, dominance hierarchy, strength and directionality of social interactions among individuals, and these data will be related to hormonal variations thanks to biochemical assays of several naturally occurring hormones and central neurotransmitter metabolites. We will analyse the effects of environmental and pharmacological manipulations, focusing on the oxytocin (OT) system, which has been implicated in rodent and human affiliative behaviours, but has been little studied thus far in non-human primates. Of particular interest will be the potential interactions between OT signalling, environmental factors, and individual differences in dominance rank and degree of sociality. For instance, we predict that OT facilitation will produce a greater increase in affiliative behaviour (e.g. huddling and allogrooming) caused by the stress associated with a brief a period of isolation from the group in animals with low sociality (and presumably low basal brain OT levels) than in animals with high sociality. By contrast, OT inhibition might induce a decrease in the frequency of such behaviour primarily in high-ranking individuals who occupy a pivotal role in the social network and thrive on high OT levels. We will also conduct remote wireless recordings in the amygdala and anterior hippocampus, which are known to participate in memory and emotional salience mechanisms. Our main goals will be to relate changes in oscillatory activity and synchronization of neuronal populations to the nature of the observed interactions (affiliative vs agonistic), the respective roles of the agents (donor vs. recipient) and behavioural phases (initiation vs. termination), and to analyse the impact of OT facilitation and inhibition at the neuronal level activity. We expect that a better understanding of the neural circuits underlying variations in monkey behaviour will provide important insight into those contributing to variations in analogous human behaviour and set empirical bases for new non-human primate models of normal and pathological social behaviour.