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

Biol Psychiatry. 2022 Nov 1;92(9):722-729. doi: 10.1016/j.biopsych.2022.05.025. Epub 2022 May 27.


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.

Keywords: Animal model; Checking behavior; Doubt; Electrophysiology; Frontal cortex; OCD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Gyrus Cinguli / physiology
  • Macaca mulatta
  • Motor Cortex*
  • Movement / physiology
  • Neurons / physiology