Interbrain cortical synchronization encodes multiple aspects of social interactions in monkey pairs

Po-He Tseng,Sankaranarayani Rajangam,Miguel A L Nicolelis,Gary Lehew,Mikhail A Lebedev

doi:10.1038/s41598-018-22679-x

Po-He Tseng, Sankaranarayani Rajangam + Show 3 more

Open Access

https://doi.org/10.1038/s41598-018-22679-x

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Journal: Scientific Reports	Publication Date: Mar 29, 2018
Citations: 25	License type: open-access

Affiliation: Duke University

Abstract

While it is well known that the primate brain evolved to cope with complex social contingencies, the neurophysiological manifestation of social interactions in primates is not well understood. Here, concurrent wireless neuronal ensemble recordings from pairs of monkeys were conducted to measure interbrain cortical synchronization (ICS) during a whole-body navigation task that involved continuous social interaction of two monkeys. One monkey, the passenger, was carried in a robotic wheelchair to a food dispenser, while a second monkey, the observer, remained stationary, watching the passenger. The two monkeys alternated the passenger and the observer roles. Concurrent neuronal ensemble recordings from the monkeys’ motor cortex and the premotor dorsal area revealed episodic occurrence of ICS with probability that depended on the wheelchair kinematics, the passenger-observer distance, and the passenger-food distance – the social-interaction factors previously described in behavioral studies. These results suggest that ICS represents specific aspects of primate social interactions.

Highlights

Observing the behaviors of others is essential for primates, including humans, to be able to handle the complex dynamics of their social groups
In monkey pair C-J, the pattern change could not be described as a symmetric reflection, suggesting that cortical neuronal modulation was affected by the arrangement of the observer and dispenser positions in room-centered coordinates
One monkey remained stationary while another monkey navigated using a robotic wheelchair. This paradigm allowed us to examine how the social interaction between the monkey pair was affected by whole-body movements of either the dominant or the subordinate animals

Summary

Introduction

Observing the behaviors of others is essential for primates, including humans, to be able to handle the complex dynamics of their social groups. In monkey pair C-K, the probability of ICS episodes increased when the passenger (C or K) approached the grape dispenser (Fig. 2A,C; Spearman correlation = −0.28 ± 0.18).

Results

Conclusion