Local and system mechanisms for action execution and observation in parietal and premotor cortices

Carolina G Ferroni,Davide Albertini,Marco Lanzilotto,Alessandro Livi,Monica Maranesi,Luca Bonini

doi:10.1016/j.cub.2021.04.034

Abstract

SummaryThe action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates. Yet temporal and tuning specificities of distinct areas and of physiologically identified neuronal classes in the encoding of self and others’ action remain unknown. We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it. At the system level, during task execution, F6 displays a prevalence of suppressed neurons and signals whether an action has to be performed, whereas AIP and F5 share a prevalence of facilitated neurons and remarkable target selectivity; during task observation, F5 stands out for its unique prevalence of facilitated neurons and its stronger and earlier modulation than AIP and F6. By applying unsupervised clustering of spike waveforms, we found distinct cell classes unevenly distributed across areas, with different firing properties and carrying specific visuomotor signals. Broadly spiking neurons exhibited a balanced amount of facilitated and suppressed activity during action execution and observation, whereas narrower spiking neurons showed more mutually facilitated responses during the execution of one’s own and others’ action, particularly in areas AIP and F5. Our findings elucidate the time course of activity and firing properties of neurons in the AON during one’s own and others’ action, from the system level of anatomically distinct areas to the local level of physiologically distinct cell classes.

Highlights

Action execution and observation recruit the same neural substrates in a wide set of brain regions in both human[1,2,3] and nonhuman primates.[4,5,6] after the discovery of mirror neurons, a class of cells in the premotor area F5 of the macaque that become active during both the execution and observation of actions,[7,8] similar neuronal properties have been found in a larger network of anatomically connected brain regions,[9,10,11] which form the so-called action observation network (AON)
The action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates
We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it

Summary

Introduction

Action execution and observation recruit the same neural substrates in a wide set of brain regions in both human[1,2,3] and nonhuman primates.[4,5,6] after the discovery of mirror neurons, a class of cells in the premotor area F5 of the macaque that become active during both the execution and observation of actions,[7,8] similar neuronal properties have been found in a larger network of anatomically connected brain regions,[9,10,11] which form the so-called action observation network (AON). The ventral premotor area F5 is thought to be the core of the AON and is certainly the most widely studied region.[4,12] More recently, two other AON areas have attracted increasing interest: the anterior intraparietal area (AIP) and the pre-supplementary area F6. AIP plays a role in routing to F5 visual information regarding manipulative actions of other[13,14,15] and area F6 hosts neurons that selectively encode actions and targets of self and others.[11,16,17,18,19] Despite these recent advances in our understanding of the AON, two critical questions remain unanswered

Methods

Results

Conclusion