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)