Dynamic Social Adaptation of Motion-Related Neurons in Primate Parietal Cortex

Citation: Fujii N, Hihara S, Iriki A ( Dynamic Social Adaptation of Motion-Related Neurons in Primate Parietal Cortex Naotaka Fujii 0 1 Sayaka Hihara 0 1 Atsushi Iriki 0 1 0 Funding: This research was supported by Grant-in-Aid for Scientific Research on Priority Areas Integrative Brain Research from the MEXT of Japan (17021048), Grant-in-Aid for Scientific Research on Priority Areas Mobiligence from the MEXT of Japan (18047029) and 2006 Riken Strategic Programs for R&D (President's Discretionary Fund) 1 Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute , Wako , Japan Social brain function, which allows us to adapt our behavior to social context, is poorly understood at the single-cell level due largely to technical limitations. But the questions involved are vital: How do neurons recognize and modulate their activity in response to social context? To probe the mechanisms involved, we developed a novel recording technique, called multi-dimensional recording, and applied it simultaneously in the left parietal cortices of two monkeys while they shared a common social space. When the monkeys sat near each other but did not interact, each monkey's parietal activity showed robust response preference to action by his own right arm and almost no response to action by the other's arm. But the preference was broken if social conflict emerged between the monkeys-specifically, if both were able to reach for the same food item placed on the table between them. Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other. Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations. Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network. - INTRODUCTION The complexity of human social organization dwarfs that of any other species. This complexity often results in a heavy cognitive load on our brains, as we are expected to behave in a socially correct manner. The coordination of internal demands and social rules has been called the social brain function [1,2]. Human social brain function, while adapted to unique evolutionary heights, surely shares many mechanisms in common with that of monkeys, who are therefore ideal subjects in which to study social brain function. But various technical difficulties have made the study of social brain function extremely difficult. Social brain function is tightly linked to social context, and social context consists of multimodal social properties including the behaviors of individuals and details in the environment. Social context changes continuously and is often unpredictable. An action that was socially appropriate a few seconds ago is not guaranteed to be appropriate now. Therefore, if social conflict is to be avoided, frequent updates of each agents internal representation of the social environment must be an essential brain function. Social brain function tracks current social state and can choose the best solution at the moment. To probe the mechanisms behind social brain function, we must monitor and control a huge number of environmental parameters together with neural activity. Since conventional methods could not handle such massive data, to date there has been almost no study of social brain function at the single-cell level. To solve the technical problem we developed the multidimensional recording (MDR) technique [3], which combines of a motion capture system and chronic multi-electrode recording techniques. We used MDR to simultaneously record behavior and parietal neuron activity in two monkeys, M1 and M2, acting in a shared social space. The parietal cortex is thought to contribute to spatial and movement-related cognition [4,5]. Our aim was to investigate how parietal neurons recognize the actions of self and other, and how they modulate their action-recognition response properties in situations of social conflict arising from unequal social rank. Subjects and preparation Two male Japanese macaque monkeys (Macaca fuscata), here called M1 and M2, were used. All procedures were approved in advance by the RIKEN Animal Committee (H18-2B012). A recording chamber was surgically implanted in the left hemisphere of each monkey. We chronically implanted twelve tungsten electrodes (FHC: impedance 800 K1 M ohm), aiming to record neural activity in an area anterior to the intra-parietal sulcus (IPS) [6]. Most of the motion-related neurons from which we recorded were located in the anterior/medial wall of the IPS (Figure 1D), and were identified by MRI images taken before the experiment. Neuronal activity was recorded by the Digital Lynx system (Neuralynx, Tucson, AZ) and subsequently sorted individually by manual parameters with the Offline Sorter (Plexon, Dallas, TX). Before starting neural recording, we tested t (...truncated)