Nonspecific Inhibition of the Motor System during Response Preparation

Abstract

Motor system excitability is transiently inhibited during the preparation of responses. Previous studies have attributed this inhibition to the operation of two mechanisms, one hypothesized to help resolve competition between alternative response options, and the other to prevent premature response initiation. By this view, inhibition should be restricted to task-relevant muscles. Although this prediction is supported in one previous study (Duque et al., 2010), studies of stopping ongoing actions suggest that some forms of motor inhibition may be widespread (Badry et al., 2009). This motivated us to conduct a series of transcranial magnetic stimulation (TMS) experiments to examine in detail the specificity of preparatory inhibition in humans. Motor-evoked potentials were inhibited in task-irrelevant muscles during response preparation, even when the muscles were contralateral and not homologous to the responding effector. Inhibition was also observed in both choice and simple response task conditions, with and without a preparatory interval. Control experiments ruled out that this inhibition is due to expectancy of TMS or a possible need to cancel the prepared response. These findings suggest that motor inhibition during response preparation broadly influences the motor system and likely reflects a process that occurs whenever a response is selected. We propose a reinterpretation of the functional significance of preparatory inhibition, one by which inhibition reduces noise to enhance signal processing and modulates the gain of a selected response.

Significance statement: Motor preparation entails the recruitment of excitatory and inhibitory neural mechanisms. The current experiments address the specificity of inhibitory mechanisms, asking whether preparatory inhibition affects task-irrelevant muscles. Participants prepared a finger movement to be executed at the end of a short delay period. Transcranial magnetic stimulation over primary motor cortex provided an assay of corticospinal excitability. Consistent with earlier work, the agonist muscle for the forthcoming response was inhibited during the preparatory period. Moreover, this inhibition was evident in task-irrelevant muscles, although the magnitude of inhibition depended on whether the response was fixed or involved a choice. These results implicate a broadly tuned inhibitory mechanism that facilitates response preparation, perhaps by lowering background activity before response initiation.

Keywords: action selection; decision-making; gain modulation; inhibition; response preparation; transcranial magnetic stimulation.

Figure 1.

The delayed response task was administered in separate blocks of choice and simple trials. A cue indicated which response to prepare, and an imperative signaled to execute the prepared response. Responses were comprised of lateral flexions of the index finger or downward flexion of the pinky finger. Experiment 1 consisted of both choice and simple blocks of trials with a cue delay (A) and without a cue delay, i.e., only the imperative was presented (B). Experiment 2 included null response trials in which the cue was replaced by an X, and no response was prepared (C). Experiment 3 included three separate conditions with different types of catch trials: (1) no catch trials at all, (2) standard catch trials (A), and (3) no imperative trials (D) in which the cue remained on the screen throughout the trial. EMG was recorded from the left first dorsal interosseous muscle and used to measure MEP amplitudes and EMG burst onset times (E).

Figure 2.

A, Experiment 1: Mean MEP amplitudes (±SE) in the left FDI muscle were reduced relative to baseline in all delay conditions (left), as well as 150 ms after a choice imperative or a simple imperative cuing the right finger, in the absence of a preparatory delay (right). B, Experiment 2: Mean left FDI MEP amplitudes (±SE) were also reduced during the delay period whenever a simple response was prepared but remained at baseline whenever a response was not being prepared and 150 ms after the right pinky was cued to respond in the absence of a preparatory delay. C, Experiment 3: the likelihood of a catch trial and the type of catch trial did not impact the observed reduction in mean MEP amplitudes (±SE). *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 3.

Mean EMG-based response times (±SE) are shown for all correct response trials in Experiment 1 (A), Experiment 2 (B), and Experiment 3 (C).

Figure 4.

The inhibitory spotlight (mesh overlay) may be centered over the selected (green bar) response representation. In the context of a choice task (top row), the tuning of the spotlight is sharper, increasing separation between the selected and nonselected (red bar) response representations. Given the lack of competition, the tuning of the spotlight can be broader in the absence of a choice (simple RT, bottom row).