Tuning the Corticospinal System: How Distributed Brain Circuits Shape Human Actions

Abstract

Interactive behaviors rely on the operation of several processes allowing the control of actions, including their selection, withholding, and cancellation. The corticospinal system provides a unique route through which multiple brain circuits can exert control over bodily motor acts. In humans, the influence of these modulatory circuits on the corticospinal system can be probed using various transcranial magnetic stimulation (TMS) protocols. Here, we review neural data from TMS studies at the basis of our current understanding of how diverse pathways—including intra-cortical, trans-cortical, and subcortico-cortical circuits—contribute to action control by tuning the activity of the corticospinal system. Critically, when doing so, we point out important caveats in the field that arise from the fact that these circuits, and their impact on the corticospinal system, have not been considered equivalently for action selection, withholding, and cancellation. This has led to the misleading view that some circuits or regions are specialized in specific control processes and that they produce particular modulatory changes in corticospinal excitability (e.g., generic vs. specific modulation of corticospinal excitability). Hence, we point to the need for more transversal research approaches in the field of action control.

A TMS study of preparatory suppression in binge drinkers

“…In summary, our results are consistent with the view that withholding responses during action preparation involves a global suppression of motor activity ( Derosiere et al, 2020 , Derosiere and Duque, 2020 , Duque et al, 2017 ). This phenomenon was clear in HCs who systematically displayed smaller MEP amplitudes at TMS Delay in both relevant (FDI) and task-irrelevant (ADM, APB) effectors compared to MEPs probed at TMS Baseline-In .…”

“…When applied over the primary motor cortex (M1), TMS elicits motor-evoked potentials (MEPs) in targeted contralateral hand or limb muscles. Their amplitude provides a temporally precise and muscle-specific measure of the net impact of facilitatory and inhibitory inputs to corticospinal (CS) cells ( Bestmann and Duque, 2016 , Bestmann and Krakauer, 2015 , Derosiere and Duque, 2020 , Dum and Strick, 2002 ). Inhibitory control is particularly strong in stop-signal tasks where the successful suppression of actions following stop signals relies on a decrease in the excitability of the CS tract ( Duque et al, 2017 , Wessel et al, 2013 , Wessel and Aron, 2017 ).…”

Considering Motor Excitability During Action Preparation in Gambling Disorder: A Transcranial Magnetic Stimulation Study

“…As GDPs are preserved from the neurotoxic influence of drugs of abuse, one straightforward interpretation of the discrepancy between both studies is that the lack of preparatory suppression observed in ADPs arises as a consequence of chronic alcohol consumption. Accordingly, it has been shown that the lateral prefrontal cortex—i.e., the region of the alcoholic brain in which the decrease in gray matter volume is the most significant ( 82 )—generates at least part of the preparatory suppression effect ( 11 , 83 ). Hence, it is plausible that this prefrontal source of preparatory suppression is specifically reduced in ADPs after years of alcohol abuse.…”

Motor training strengthens corticospinal suppression during movement preparation

“…In humans, motor activity can be assessed by applying single-pulse TMS over the primary motor cortex (M1), eliciting motor-evoked potentials (MEPs), whose amplitude reflects the excitability of the CS output pathway (Derosiere and Duque, 2020). When applied during reaction time (RT) tasks at specific time points, TMS elicits MEPs that can be used to assess CS excitability changes associated with action preparation and initiation.…”