Motor Interference, But Not Sensory Interference, Increases Midfrontal Theta Activity and Brain Synchronization during Reactive Control

J Neurosci. 2021 Feb 24;41(8):1788-1801. doi: 10.1523/JNEUROSCI.1682-20.2020. Epub 2021 Jan 13.

Abstract

Cognitive control helps us to overcome task interference in challenging situations. Resolving conflicts because of interfering influences is believed to rely on midfrontal theta oscillations. However, different sources of interference necessitate different types of control. Attentional control is needed to suppress salient distractors. Motor control is needed to suppress goal-incompatible action impulses. While previous studies mostly studied the additive effects of attentional and motor conflicts, we independently manipulated the need for attentional control (via visual distractors) and motor control (via unexpected response deviations) in an EEG study with male and female humans. We sought to find out whether these different types of control rely on the same midfrontal oscillatory mechanisms. Motor conflicts, but not attentional conflicts, elicited increases in midfrontal theta power during conflict resolution. Independent of the type of conflict, theta power was predictive of motor slowing. Connectivity analysis via phase-based synchronization indicated a widespread increase interbrain connectivity for motor conflicts, but a midfrontal-to-posterior decrease in connectivity for attentional conflicts. For each condition, we found stronger midfrontal connectivity with the parietal region contralateral to, rather than ipsilateral to, the acting hand. Parietal lateralization in connectivity was strongest for motor conflicts. Previous studies suggested that midfrontal theta oscillations might represent a general control mechanism, which aids conflict resolution independent of the conflict domain. In contrast, our results show that oscillatory theta dynamics during reactive control mostly reflect motor-related adjustments.SIGNIFICANCE STATEMENT Humans need to exercise self-control over both their attention (to avoid distraction) and their motor activity (to suppress inappropriate action impulses). Midfrontal theta oscillations have been assumed to indicate a general control mechanism, which help to exert top-down control during both motor and sensory interference. We are using a novel approach for the independent manipulation of attentional and motor control to show that increases in midfrontal theta power and brainwide connectivity are linked to the top-down adjustments of motor responses, not sensory interference. These findings clarify the function of midfrontal theta dynamics as a key aspect of neural top-down control and help to dissociate domain-general from motor-specific aspects of self-control.

Keywords: cognitive control; distraction; motor control; neural oscillations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Attention / physiology*
  • Conflict, Psychological
  • Female
  • Frontal Lobe / physiology*
  • Humans
  • Male
  • Motor Activity / physiology*
  • Self-Control
  • Theta Rhythm / physiology*
  • Young Adult