Non-selective inhibition of the motor system following unexpected and expected infrequent events

Abstract

Motor inhibition is a key control mechanism that allows humans to rapidly adapt their actions in response to environmental events. One of the hallmark signatures of rapidly exerted, reactive motor inhibition is the non-selective suppression of cortico-spinal excitability (CSE): unexpected sensory stimuli lead to a suppression of CSE across the entire motor system, even in muscles that are inactive. Theories suggest that this reflects a fast, automatic, and broad engagement of inhibitory control, which facilitates behavioral adaptations to unexpected changes in the sensory environment. However, it is an open question whether such non-selective CSE suppression is truly due to the unexpected nature of the sensory event, or whether it is sufficient for an event to be merely infrequent (but not unexpected). Here, we report data from two experiments in which human subjects experienced both unexpected and expected infrequent events during a two-alternative forced-choice reaction time task while CSE was measured from a task-unrelated muscle. We found that expected infrequent events can indeed produce non-selective CSE suppression-but only when they occur during movement initiation. In contrast, unexpected infrequent events produce non-selective CSE suppression relative to frequent, expected events even in the absence of movement initiation. Moreover, CSE suppression due to unexpected events occurs at shorter latencies compared to expected infrequent events. These findings demonstrate that unexpectedness and stimulus infrequency have qualitatively different suppressive effects on the motor system. They also have key implications for studies that seek to disentangle neural and psychological processes related to motor inhibition and stimulus detection.

Keywords: Cortico-motor excitability; Motor evoked potentials; Motor inhibition; Oddball; Surprise.

Figure 1.

Diagrams of speeded response tasks participants completed in Experiments 1 and 2. In Experiment 1, participants heard the sound before an imperative stimulus (the arrow) was shown. In Experiment 2, participants heard the sound immediately following the arrow. Below the task diagrams is a diagram of the experimental setup: TMS to elicit a MEP is delivered over motor cortex contralateral to the hand muscle with EMG electrodes, while participants respond with the feet.

Figure 2.

MEP results from Experiments 1 and 2, separated into trial averages (+/− standard error) by SOUND and TMS TIMING conditions. Statistically significant comparisons are noted.