A causal role for the human subthalamic nucleus in non-selective cortico-motor inhibition

Wessel, Jan R; Diesburg, Darcy A; Chalkley, Nathan H; Greenlee, Jeremy D.W.

doi:10.1016/j.cub.2022.06.067

Cited by 22 publications

(20 citation statements)

References 53 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It is part of both the indirect and hyperdirect basal ganglia pathways that ostensibly implement both selective and non-selective inhibition of the motor system via excitatory projections to the output nuclei of the basal ganglia (Parent & Hazrati, 1995; Mink, 1996; Wessel & Aron, 2017). Indeed, in two previous studies using the stop-signal task, we have found that the activity of the subthalamic nucleus after stop-signals is directly related to the observed reductions in CSE (Wessel et al, 2016a; Wessel et al, 2022a). However, since the subthalamic is purported to be involved in other, potentially non-motor functions, especially during cognitive control (e.g., Cavanagh et al, 2011; Aron et al, 2016; Zénon et al 2016; Weintraub & Zaghloul 2013; Temel et al, 2005), its activity alone does not definitively prove the presence of motor inhibition during error processing either.…”

Section: Discussionmentioning

confidence: 72%

“…Non-selective inhibition, in contrast, is broad and extends even to task-unrelated effectors (Badry et al, 2009; Wessel & Aron, 2017). It is ostensibly implemented via the hyper-direct pathway (Chen et al, 2020; Wessel et al, 2022a). Empirically, selective and non-selective inhibition can be distinguished through corticospinal excitability (CSE), which can be measured via concurrent transcranial magnetic stimulation (TMS) and electromyography (EMG; Bestmann & Krakauer, 2015; Duque et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Two types of motor inhibition after action errors in humans

Guan

Wessel

2022

Preprint

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Discussionmentioning

confidence: 72%

Section: Introductionmentioning

confidence: 99%

Two types of motor inhibition after action errors in humans

Guan

Wessel

2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The STN is at the core of most neuroscientific models of motor control (Frank et al, 2007;Jahanshahi et al, 2015) and is part of both the indirect and hyperdirect basal ganglia pathways that ostensibly implement both selective and nonselective motor inhibition (Parent and Hazrati, 1995;Mink, 1996;Wessel and Aron, 2017). Indeed, STN activity after stop-signals is directly related to the observed reductions in CSE (Wessel et al, 2016a(Wessel et al, , 2022a. However, STN activity does not prove the presence of motor inhibition during error processing (Temel et al, 2005;Cavanagh et al, 2011;Weintraub and Zaghloul, 2013;Aron et al, 2016;Zénon et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Nonselective inhibition, in contrast, is broad and extends even to task-unrelated effectors (Badry et al, 2009;Wessel and Aron, 2017). It is ostensibly implemented via the hyperdirect pathway (Chen et al, 2020;Wessel et al, 2022a). Empirically, selective and nonselective inhibition can be distinguished through corticospinal excitability (CSE), which can be measured via concurrent transcranial magnetic stimulation (TMS) and electromyography (EMG) (Bestmann and Krakauer, 2015;Duque et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Two Types of Motor Inhibition after Action Errors in Humans

Guan

Wessel

2022

J. Neurosci.

Self Cite

View full text Add to dashboard Cite

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 posterror 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.

show abstract

“…Voice data were preprocessed as in prior work from our group (Wessel et al, 2022; 2016). In brief, custom MATLAB scripts were used to playback the voice data from each trial and to visually inspect the audio data.…”

Section: Methodsmentioning

confidence: 99%

Examining motor evidence for the pause-then-cancel model of action-stopping: Insights from motor system physiology

Tatz,

Carlson,

Lovig

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

Stopping initiated actions is fundamental to adaptive behavior. Longstanding, single-process accounts of action-stopping have been challenged by recent, two-process, 'pause-then-cancel' models. These models propose that action-stopping involves two inhibitory processes: 1) a fast Pause process, which broadly suppresses the motor system as the result of detecting any salient event, and 2) a slower Cancel process, which involves motor suppression specific to the cancelled action. A purported signature of the Pause process is global suppression, or the reduced corticospinal excitability (CSE) of task-unrelated effectors early on in action-stopping. However, unlike the Pause process, few (if any) motor system signatures of a Cancel process have been identified. Here, we used single- and paired-pulse TMS methods to comprehensively measure the local physiological excitation and inhibition of both responding and task-unrelated motor effector systems during action-stopping. Specifically, we measured CSE, short-interval intracortical inhibition (SICI), and the duration of the cortical silent period (CSP). Consistent with key predictions from the pause-then-cancel model, CSE measurements at the responding effector indicated that additional suppression was necessary to counteract Go-related increases in CSE during-action-stopping, particularly at later timepoints. Increases in SICI on Stop-signal trials did not differ across responding and non-responding effectors, or across timepoints. This suggests SICI as a potential source of global suppression. Increases in CSP duration on Stop-signal trials were more prominent at later timepoints. SICI and CSP duration therefore appeared most consistent with the Pause and Cancel processes, respectively. Our study provides further evidence from motor system physiology that multiple inhibitory processes influence action-stopping.

show abstract

A causal role for the human subthalamic nucleus in non-selective cortico-motor inhibition

Cited by 22 publications

References 53 publications

Two types of motor inhibition after action errors in humans

Two types of motor inhibition after action errors in humans

Two Types of Motor Inhibition after Action Errors in Humans

Examining motor evidence for the pause-then-cancel model of action-stopping: Insights from motor system physiology

Contact Info

Product

Resources

About