Feature Review
Physiological Markers of Motor Inhibition during Human Behavior

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Many aspects of behavior result in inhibition of the corticospinal motor output pathway.

The state of excitability of the corticospinal pathway can be assessed with single-pulse transcranial magnetic stimulation (TMS) over primary motor cortex (M1). The pulse elicits a temporally precise motor evoked potential (MEP) in the electromyography (EMG) recording from the targeted muscle. To measure the dynamics of excitability, MEPs are measured at various stages of task performance and compared in amplitude with MEPs measured at baseline (e.g., during the intertrial interval). Inhibition is evident when the MEPs are lower relative to baseline.

Motor inhibition is found when an ongoing or planned action needs to be aborted following a stop signal (reactive inhibition). In this context, behavioral inhibition is associated with a fast and global decrease in corticospinal excitability. This reactive inhibition is thought to rely on corticobasal ganglia loops via hyperdirect projections from the frontal cortex to the subthalamic nucleus (STN), providing a mechanism to generically brake the motor output.

Inhibition of the motor system is also evident in anticipation of a stop signal. Proactive inhibition has been characterized using selective stop tasks, where only part of an ongoing action needs to be interrupted. In this context, inhibition operates in a more focal manner, raising the hypothesis that separate basal ganglia pathways are recruited during behavioral inhibition, exerting broad or focal inhibitory influences depending on task demands.

Several markers of motor inhibition can be observed during the period preceding a voluntary movement (preparatory inhibition). These markers are modulated by various task variables, suggesting a role for inhibition in response selection and response initiation.

The functional role of preparatory inhibition has been the subject of considerable debate. One hypothesis is that preparatory inhibition serves to assist action selection through a competitive process, whereby excitation of selected action representations is associated with the suppression of unwanted (inappropriate) action representations. Another hypothesis has focused on the regulation of response initiation, with inhibition serving to prevent premature movement, while preparatory activity unfolds across the cortex. A third view is that preparatory inhibition may serve to modulate the gain of the motor system. A reduction in background motor activity could facilitate movement onset by increasing the signal:noise ratio. This last hypothesis shifts the emphasis away from inhibition as a way to suppress unwanted or nonselected movements, to one in which preparatory inhibition promotes rapid action selection and implementation.

The relationship in terms of psychological function and neural mechanisms between reactive, proactive, and preparatory inhibition is an important challenge for future research.

Transcranial magnetic stimulation (TMS) studies in humans have shown that many behaviors engage processes that suppress excitability within the corticospinal tract. Inhibition of the motor output pathway has been extensively studied in the context of action stopping, where a planned movement needs to be abruptly aborted. Recent TMS work has also revealed markers of motor inhibition during the preparation of movement. Here, we review the evidence for motor inhibition during action stopping and action preparation, focusing on studies that have used TMS to monitor changes in the excitability of the corticospinal pathway. We discuss how these physiological results have motivated theoretical models of how the brain selects actions, regulates movement initiation and execution, and switches from one state to another.

Section snippets

Multiple Forms of Motor Inhibition during Human Behavior

Behaving in a goal-directed manner often requires suppressing inappropriate movement tendencies 1, 2, 3. As such, many daily-life situations demand that humans refrain from acting in an automatic, stimulus-driven manner, subjugate internal desires that interfere with long-term plans (e.g., eating unhealthy food or drinking too much alcohol), or interrupt ongoing actions that are no longer appropriate (e.g., aborting a foot movement towards the accelerator when a pedestrian suddenly runs into

Motor Inhibition Associated with Action Stopping

We frequently encounter situations in which a motor action, once initiated, becomes unnecessary or inappropriate. Imagine sitting in your car at an intersection and the traffic light has just turned green. You begin to shift your foot from the brake to the accelerator when, suddenly, a pedestrian runs into the street. Fortunately, you are able to quickly update your action plan, aborting the movement towards the accelerator. While this may be an extreme example of the importance of inhibitory

Motor Inhibition Associated with Action Preparation

In the stop signal task, the experimenter introduces an explicit tension between implementing and aborting a planned action. At the behavioral level, there is an obvious need for inhibition, and at the neural level, we can measure the rapid attenuation of excitability in the corticospinal pathway. However, action stopping represents just one situation requiring inhibitory control. Many inappropriate behaviors have also been associated with a lack of inhibitory control in the context of action

Shared Motor Inhibition for Action Preparation and Action Stopping

Intriguingly, both action preparation and action stopping appear to recruit processes that can produce inhibition that is either focal or broad, depending on task demands. In the context of action stopping, the influence of these two inhibitory forms appears to depend on whether the emphasis is on speed or selectivity of stopping, respectively. During action preparation, the contribution of these inhibitory processes may also vary according to the complexity of the task and to whether a

Concluding Remarks

Prominent signatures of inhibition are observed from probes of corticospinal excitability during human motor behavior. In some conditions, these inhibitory effects are focal, limited to task-relevant motor representations. However, in many conditions, the inhibitory effects are broad, evident in task-irrelevant muscles. The broadest effect is found when an ongoing action must be rapidly aborted; in this context, inhibition appears to be observed across the motor system. The widespread nature of

Acknowledgments

J.D. was supported by grants from the ‘Fonds Spéciaux de Recherche’ (FSR) of the Université catholique de Louvain, the Belgian National Funds for Scientific Research (FRS-FNRS: MIS F.4512.14) and the ‘Fondation Médicale Reine Elisabeth’ (FMRE). R.B.I. was supported by grants from the National Institute of Health (NS097480, NS074917, NS092079). We are thankful to Julien Grandjean and Emmanuelle Wilhelm for their valuable comments on an earlier version of the manuscript.

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