A causal role for frontal cortico-cortical coordination in social action monitoring

Taihei Ninomiya,Kenta Kobayashi,Masaki Isoda,Atsushi Noritake

doi:10.1038/s41467-020-19026-y

Abstract

Decision-making via monitoring others’ actions is a cornerstone of interpersonal exchanges. Although the ventral premotor cortex (PMv) and the medial prefrontal cortex (MPFC) are cortical nodes in social brain networks, the two areas are rarely concurrently active in neuroimaging, inviting the hypothesis that they are functionally independent. Here we show in macaques that the ability of the MPFC to monitor others’ actions depends on input from the PMv. We found that delta-band coherence between the two areas emerged during action execution and action observation. Information flow especially in the delta band increased from the PMv to the MPFC as the biological nature of observed actions increased. Furthermore, selective blockade of the PMv-to-MPFC pathway using a double viral vector infection technique impaired the processing of observed, but not executed, actions. These findings demonstrate that coordinated activity in the PMv-to-MPFC pathway has a causal role in social action monitoring.

Highlights

Decision-making via monitoring others’ actions is a cornerstone of interpersonal exchanges
We developed an experimental procedure in which monkeys alternated making choices with three different types of partners: a real monkey or a human experimenter [real agent (RA) condition, Fig. 1b, left)], a filmed monkey replayed on a monitor (FM condition, Fig. 1b, center), and a filmed object replayed on the monitor (FO condition, Fig. 1b, right)
We found by using a double viral vector infection technique[37,38] that the PMv-toMPFC pathway was causally involved in monitoring observed, but not executed, actions, for determining optimal choices, when the observed actions were performed by real social agents

Summary

Introduction

Decision-making via monitoring others’ actions is a cornerstone of interpersonal exchanges. In the MPFC, activation is selective for biological interactions as assessed using functional neuroimaging methods[3]; this issue has never been addressed systematically at the single-neuron level It is highly controversial whether the PMv and MPFC coordinate with one another for social information processing. Several neuroimaging and theoretical studies[29,30,31,32,33,34,35,36] suggest possible interactions between the PMv and MPFC, or between neural systems to which these areas are thought to belong separately, this issue has never been addressed electrophysiologically in the macaque Clarifying these unsolved issues is fundamental to understanding the organizing principles of the primate social brain. The observed deficits in social action monitoring resembled peculiar behavioral disorders reported previously in a monkey with an autistic phenotype[13]

Methods

Results

Conclusion