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

The 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...

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Bibliographic Details
Published in:Current biology 2021-07, Vol.31 (13), p.2819-2830.e4
Main Authors: Ferroni, Carolina G., Albertini, Davide, Lanzilotto, Marco, Livi, Alessandro, Maranesi, Monica, Bonini, Luca
Format: Article
Language:English
Subjects:
action organization
cell classes
mirror neuron
parietal cortex
premotor cortex
pyramidal neurons
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Summary:The 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. •F6 neurons show a prevalence of suppressed activity, encoding whether to act•Area F5 and AIP share a prevalence of facilitated neurons and target selectivity•Across-areas, waveform-based clustering distinguished three neuronal classes•Narrow-spiking neurons exhibit mutual modulation during self and others’ action A system of parietal and frontal areas in the primates’ brain is shared by action execution and observation. In this single-cell study, Ferroni et al. shed new light on the time course of system-level processing of executed and observed actions in the monkey and reveal differential contributions of waveform-based classes of neurons.
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2021.04.034