Two Types of Motor Inhibition after Action Errors in Humans.

Abstract

Adaptive behavior requires the ability to appropriately react to action errors. Post-error slowing (PES) of response times is one of the most reliable phenomena in human behavior. It has been proposed that PES is partially achieved through inhibition of the motor system. However, there is no direct evidence for this link, or indeed, that the motor system is physiologically inhibited after errors altogether. Here, we used transcranial magnetic stimulation and electromyography to measure corticospinal excitability (CSE) across four experiments using a Simon task, in which female and male human participants sometimes committed errors. Errors were followed by reduced CSE at two different time points and in two different modes. Shortly after error commission (250 ms), CSE was broadly suppressed (i.e., even task-unrelated motor effectors were inhibited). During the preparation of the subsequent response, CSE was specifically reduced at task-relevant effectors only. This latter effect was directly related to PES, with stronger CSE suppression accompanying greater PES. This suggests that PES is achieved through increased inhibitory control during post-error responses. To provide converging evidence, we then reanalyzed an openly available EEG dataset that contained both Simon- and Stop-signal tasks using independent component analysis. We found that the same neural source component that indexed action cancellation in the stop-signal task also showed clear PES-related activity during post-error responses in the Simon task. Together, these findings provide evidence that post-error adaptation is partially achieved through motor inhibition. Moreover, inhibition is engaged in two modes (first nonselective, then selective), aligning with recent multistage theories of error processing.SIGNIFICANCE STATEMENT It is a common observation that humans implement a higher degree of caution when repeating an action during which they just committed a mistake. In the laboratory, such increased "caution" is reflected in post-error slowing of response latencies. Many competing theories exist regarding the precise neural mechanisms underlying post-error slowing. Using transcranial magnetic stimulation, we show that, after error commission, the human corticomotor system is momentarily inhibited, both immediately after an error and during the preparation of the next action. Moreover, motor inhibition during the latter time period is directly predictive of post-error slowing. This shows that inhibitory control is a key mechanism humans engage to regulate their own behavior in the aftermath of error commission.