Check or Go? Impact of Doubt on the Hierarchical Organization of the Mediofrontal Area

Marion Bosc, Bernard Bioulac, Thomas Michelet
Biological Psychiatry. 2022-05-01; :
DOI: 10.1016/j.biopsych.2022.05.025

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Bosc M(1), Bioulac B(2), Michelet T(3).

Author information:
(1)Univ. Bordeaux, CNRS, IMN, UMR 5293, F-33000 Bordeaux, France; Neural Circuits and Immunity and Psychosis Laboratory, The Francis Crick Institute, London, United Kingdom.
(2)Univ. Bordeaux, CNRS, IMN, UMR 5293, F-33000 Bordeaux, France.
(3)Univ. Bordeaux, CNRS, INCIA, UMR 5287, F-33000 Bordeaux, France. Electronic address: .

BACKGROUND: Based on numerous imaging and electrophysiological studies, the presupplementary motor area (pre-SMA) and the rostral cingulate motor area are cortical regions considered to be essential to voluntary movement initiation and behavioral control. However, their respective roles and functional interactions remain a long-standing and still debated question.

METHODS: Here, we trained 2 rhesus monkeys (Macaca mulatta) in a complex cognitive task to compare the neuronal activity of these 2 regions on the medial wall during both perceptual and internally guided decisions.

RESULTS: We confirmed the implication of both areas throughout the decision process. Critically, we demonstrate that instead of a stable invariant role, the pre-SMA and rostral cingulate motor area manifested a versatile hierarchical relationship depending on the mode of movement initiation. Whereas pre-SMA neurons were primarily engaged in decisions based on perceptual information, rostral cingulate motor area neurons preempted the decision process in case of an internally doubt-driven checking behavior, withholding pre-SMA recruitment during the time spent inhibiting the habitual action.

CONCLUSIONS: We identified a versatile hierarchical organization of the mediofrontal area that may substantially affect normal and pathological decision processes because adaptive behaviors, such as doubt-checking and its compulsive counterpart, rely on this subtle equilibrium in controlling action initiation.

Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

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