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 of response times (PES) is one of the most reliable phenomena in cognitive neuroscience. 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 cortico-spinal excitability (CSE) across four experiments using a Simon task, in which 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 (250ms) 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-related 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 re-analyzed 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 clear evidence that post-error adaptation is partially achieved through motor inhibition. Moreover, inhibition is engaged in two modes (first non-selective, then selective), aligning with recent multi-stage theories of error processing.

Measuring the non-selective effects of motor inhibition using isometric force recordings

“…Consequently, measurements of these non-selective effects of inhibitory control on CSE have been used to demonstrate the involvement of the fronto-subthalamic hyper-direct pathway in many different control-demanding scenarios, including those that do not explicitly require action-stopping. For example, unexpected perceptual stimuli (Dutra et al 2018;Tatz et al 2021), action errors (Guan and Wessel 2022), and response conflict (Wessel et al 2019) have all been shown to be followed by shortlatency, non-selective suppression of CSE -in line with prior work showing that all of these events activate the STN (Cavanagh et al 2014;Frank et al 2007;Herz et al 2017;Siegert et al 2014;Wessel et al 2016).…”

“…Consequently, measurements of these non-selective effects of inhibitory control on CSE have been used to demonstrate the involvement of the fronto-subthalamic hyper-direct pathway in many different control-demanding scenarios, including those that do not explicitly require action-stopping. For example, unexpected perceptual stimuli (Dutra et al 2018; Tatz et al 2021), action errors (Guan and Wessel 2022), and response conflict (Wessel et al 2019) have all been shown to be followed by short-latency, non-selective suppression of CSE – in line with prior work showing that all of these events activate the STN (Cavanagh et al 2014; Frank et al 2007; Herz et al 2017; Siegert et al 2014; Wessel et al 2016). Finally, the assessment of CSE using TMS and EMG has been a popular and widespread method for studying not only inhibitory control, but also response preparation (Bestmann and Duque 2016; Leocani et al 2000; Raud et al 2020), interhemispheric interactions (Fiori et al 2017; Hamada et al 2014; Hannah and Rothwell 2017), and pathological states that affect the motor system (Badawy et al 2013; Chowdhury et al 2018; Jahanshahi and Rothwell 2017; Smith and Stinear 2016).…”