Latency and amplitude of the stop-signal P3 event-related potential are related to inhibitory GABAa activity in primary motor cortex

AbstractBy stopping actions even after their initiation, humans can adapt their ongoing behavior rapidly to changing environmental circumstances. The neural processes underlying the implementation of rapid action-stopping are still controversially discussed. In the early 1990s, a fronto-central P3 event-related potential (ERP) was identified in the human EEG response following stop-signals in the classic stop-signal task, accompanied by the proposal that this ERP reflects the “inhibitory” side of the purported horse-race underlying successful action-stopping. Later studies have lent support to this interpretation by finding that the amplitude and onset of the stop-signal P3 relate to both overt behavior and to movement-related EEG activity in ways predicted by the race model. However, such studies are limited by the ability of EEG to allow direct inferences about the presence (or absence) of true, physiologically inhibitory signaling at the neuronal level. To address this, we here present a cross-modal individual differences investigation of the relationship between the features stop-signal P3 ERP and GABAergic neurotransmission in primary motor cortex (M1, as measured by paired-pulse transcranial magnetic stimulation). Following recent work, we measured short-interval intracortical inhibition (SICI), a marker of inhibitory GABAa activity in M1, in a group of 41 human participants who also performed the stop-signal task while undergoing EEG recordings. In line with the P3-inhibition hypothesis, we found that subjects with stronger inhibitory GABA activity in M1 also showed both faster onsets and larger amplitudes of the stop-signal P3. This provides direct evidence linking the properties of this ERP to a true physiological index of motor system inhibition. We discuss these findings in the context of recent theoretical developments and empirical findings regarding the neural implementation of inhibitory control during action-stopping.

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Stop Signal Task Training Strengthens GABA-mediated Neurotransmission within the Primary Motor Cortex

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01597 ◽

2020 ◽

Vol 32 (10) ◽

pp. 1984-2000

Author(s):

Nahian S. Chowdhury ◽

Evan J. Livesey ◽

Justin A. Harris

Keyword(s):

Motor Cortex ◽

Resting State ◽

Primary Motor Cortex ◽

Short Interval ◽

Intracortical Inhibition ◽

Stop Signal ◽

Stop Signal Task ◽

Time Points ◽

Task Training ◽

Experimental Group

We have recently shown that the efficiency in stopping a response, measured using the stop signal task, is related to GABAA-mediated short-interval intracortical inhibition (SICI) in the primary motor cortex. In this study, we conducted two experiments on humans to determine whether training participants in the stop signal task within one session (Experiment 1) and across multiple sessions (Experiment 2) would increase SICI strength. For each experiment, we obtained premeasures and postmeasures of stopping efficiency and resting-state SICI, that is, during relaxed muscle activity (Experiment 1, n = 45, 15 male participants) and SICI during the stop signal task (Experiment 2, n = 44, 21 male participants). In the middle blocks of Experiment 1 and the middle sessions of Experiment 2, participants in the experimental group completed stop signal task training, whereas control participants completed a similar task without the requirement to stop a response. After training, the experimental group showed increased resting-state SICI strength (Experiment 1) and increased SICI strength during the stop signal task (Experiment 2). Although there were no overall behavioral improvements in stopping efficiency, improvements at an individual level were correlated with increases in SICI strength at rest (Experiment 1) and during successful stopping (Experiment 2). These results provide evidence of neuroplasticity in resting-state and task-related GABAA-mediated SICI in the primary motor cortex after response inhibition training. These results also suggest that SICI and stopping efficiency are temporally linked, such that a change in SICI between time points is correlated with a change in stopping efficiency between time points.

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Cortical silent period reflects individual differences in action stopping performance

Scientific Reports ◽

10.1038/s41598-021-94494-w ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Mario Paci ◽

Giulio Di Cosmo ◽

Mauro Gianni Perrucci ◽

Francesca Ferri ◽

Marcello Costantini

Keyword(s):

Individual Differences ◽

Response Inhibition ◽

Primary Motor Cortex ◽

Silent Period ◽

Intracortical Inhibition ◽

Stop Signal ◽

Stop Signal Task ◽

Behavioral Differences ◽

Cortical Silent Period ◽

Stop Signal Reaction Time

AbstractInhibitory control is the ability to suppress inappropriate movements and unwanted actions, allowing to regulate impulses and responses. This ability can be measured via the Stop Signal Task, which provides a temporal index of response inhibition, namely the stop signal reaction time (SSRT). At the neural level, Transcranial Magnetic Stimulation (TMS) allows to investigate motor inhibition within the primary motor cortex (M1), such as the cortical silent period (CSP) which is an index of GABAB-mediated intracortical inhibition within M1. Although there is strong evidence that intracortical inhibition varies during action stopping, it is still not clear whether differences in the neurophysiological markers of intracortical inhibition contribute to behavioral differences in actual inhibitory capacities. Hence, here we explored the relationship between intracortical inhibition within M1 and behavioral response inhibition. GABABergic-mediated inhibition in M1 was determined by the duration of CSP, while behavioral inhibition was assessed by the SSRT. We found a significant positive correlation between CSP’s duration and SSRT, namely that individuals with greater levels of GABABergic-mediated inhibition seem to perform overall worse in inhibiting behavioral responses. These results support the assumption that individual differences in intracortical inhibition are mirrored by individual differences in action stopping abilities.

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Effects of short interval intracortical inhibition and intracortical facilitation on short interval intracortical facilitation in human primary motor cortex

The Journal of Physiology ◽

10.1113/jphysiol.2009.181446 ◽

2009 ◽

Vol 587 (23) ◽

pp. 5665-5678 ◽

Cited By ~ 53

Author(s):

Aparna Wagle-Shukla ◽

Zhen Ni ◽

Carolyn A. Gunraj ◽

Nina Bahl ◽

Robert Chen

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Short Interval ◽

Intracortical Inhibition ◽

Intracortical Facilitation

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Stopping a response has global or nonglobal effects on the motor system depending on preparation

Journal of Neurophysiology ◽

10.1152/jn.00704.2011 ◽

2012 ◽

Vol 107 (1) ◽

pp. 384-392 ◽

Cited By ~ 50

Author(s):

Ian Greenhouse ◽

Caitlin L. Oldenkamp ◽

Adam R. Aron

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Motor System ◽

Primary Motor Cortex ◽

Stop Signal ◽

Stop Signal Task ◽

Proactive Control ◽

The Subject ◽

Do So

Much research has focused on how people stop initiated response tendencies when instructed by a signal. Stopping of this kind appears to have global effects on the motor system. For example, by delivering transcranial magnetic stimulation (TMS) over the leg area of the primary motor cortex, it is possible to detect suppression in the leg when the hand is being stopped (Badry R et al. Suppression of human cortico-motoneuronal excitability during the stop-signal task. Clin Neurophysiol 120: 1717–1723, 2009). Here, we asked if such “global suppression” can be observed proactively, i.e., when people anticipate they might have to stop. We used a conditional stop signal task, which allows the measurement of both an “anticipation phase” (i.e., where proactive control is applied) and a “stopping” phase. TMS was delivered during the anticipation phase ( experiment 1) and also during the stopping phase ( experiments 1 and 2) to measure leg excitability. During the anticipation phase, we did not observe leg suppression, but we did during the stopping phase, consistent with Badry et al. (2009) . Moreover, when we split the subject groups into those who slowed down behaviorally (i.e., exercised proactive control) and those who did not, we found that subjects who slowed did not show leg suppression when they stopped, whereas those who did not slow did show leg suppression when they stopped. These results suggest that if subjects prepare to stop, then they do so without global effects on the motor system. Thus, preparation allows them to stop more selectively.

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P22.20 The relationship between short-interval intracortical inhibition and the long term potentiation-like effect of paired associative stimulation in human primary motor cortex

Clinical Neurophysiology ◽

10.1016/s1388-2457(11)60581-6 ◽

2011 ◽

Vol 122 ◽

pp. S162

Author(s):

N. Murase ◽

B. Cengiz ◽

J.C. Rothwell

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Short Interval ◽

Long Term Potentiation ◽

Intracortical Inhibition ◽

Paired Associative Stimulation ◽

Term Potentiation ◽

The Relationship

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Short-interval intracortical inhibition in human primary motor cortex: A multi-locus transcranial magnetic stimulation study

NeuroImage ◽

10.1016/j.neuroimage.2019.116194 ◽

2019 ◽

Vol 203 ◽

pp. 116194 ◽

Cited By ~ 2

Author(s):

Jaakko O. Nieminen ◽

Lari M. Koponen ◽

Niko Mäkelä ◽

Victor Hugo Souza ◽

Matti Stenroos ◽

...

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Magnetic Stimulation ◽

Primary Motor Cortex ◽

Short Interval ◽

Intracortical Inhibition

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Event-related desynchronization reflects downregulation of intracortical inhibition in human primary motor cortex

Journal of Neurophysiology ◽

10.1152/jn.01092.2012 ◽

2013 ◽

Vol 110 (5) ◽

pp. 1158-1166 ◽

Cited By ~ 108

Author(s):

Mitsuaki Takemi ◽

Yoshihisa Masakado ◽

Meigen Liu ◽

Junichi Ushiba

Keyword(s):

Motor Cortex ◽

Motor Imagery ◽

Sensorimotor Cortex ◽

Primary Motor Cortex ◽

Motor Evoked Potentials ◽

Short Interval ◽

Hand Movement ◽

Intracortical Inhibition ◽

Imagery Task ◽

Event Related Desynchronization

There is increasing interest in electroencephalogram (EEG)-based brain-computer interface (BCI) as a tool for rehabilitation of upper limb motor functions in hemiplegic stroke patients. This type of BCI often exploits mu and beta oscillations in EEG recorded over the sensorimotor areas, and their event-related desynchronization (ERD) following motor imagery is believed to represent increased sensorimotor cortex excitability. However, it remains unclear whether the sensorimotor cortex excitability is actually correlated with ERD. Thus we assessed the association of ERD with primary motor cortex (M1) excitability during motor imagery of right wrist movement. M1 excitability was tested by motor evoked potentials (MEPs), short-interval intracortical inhibition (SICI), and intracortical facilitation (ICF) with transcranial magnetic stimulation (TMS). Twenty healthy participants were recruited. The participants performed 7 s of rest followed by 5 s of motor imagery and received online visual feedback of the ERD magnitude of the contralateral hand M1 while performing the motor imagery task. TMS was applied to the right hand M1 when ERD exceeded predetermined thresholds during motor imagery. MEP amplitudes, SICI, and ICF were recorded from the agonist muscle of the imagined hand movement. Results showed that the large ERD during wrist motor imagery was associated with significantly increased MEP amplitudes and reduced SICI but no significant changes in ICF. Thus ERD magnitude during wrist motor imagery represents M1 excitability. This study provides electrophysiological evidence that a motor imagery task involving ERD may induce changes in corticospinal excitability similar to changes accompanying actual movements.

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Muscle Pain Differentially Modulates Short Interval Intracortical Inhibition and Intracortical Facilitation in Primary Motor Cortex

Journal of Pain ◽

10.1016/j.jpain.2011.10.013 ◽

2012 ◽

Vol 13 (2) ◽

pp. 187-194 ◽

Cited By ~ 57

Author(s):

Siobhan M. Schabrun ◽

Paul W. Hodges

Keyword(s):

Motor Cortex ◽

Muscle Pain ◽

Primary Motor Cortex ◽

Short Interval ◽

Intracortical Inhibition ◽

Intracortical Facilitation

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Unravelling the modulation of intracortical inhibition during motor imagery: An adaptive threshold-hunting study

10.1101/846931 ◽

2019 ◽

Author(s):

Cécilia Neige ◽

Dylan Rannaud Monany ◽

Cathy M. Stinear ◽

Winston D. Byblow ◽

Charalambos Papaxanthis ◽

...

Keyword(s):

Transcranial Magnetic Stimulation ◽

Motor Cortex ◽

Motor Imagery ◽

Magnetic Stimulation ◽

Primary Motor Cortex ◽

Short Interval ◽

Intracortical Inhibition ◽

Adaptive Threshold ◽

Mental Simulation ◽

The Right

AbstractMotor imagery (MI) is the mental simulation of an action without any apparent muscular contraction. By means of transcranial magnetic stimulation, few studies revealed a decrease of short-interval intracortical inhibition (SICI) within the primary motor cortex. However, this decrease is ambiguous, as one would expect greater inhibition during MI to prevent overt motor output. The current study investigated the extent of SICI modulation during MI through a methodological and a conceptual reconsideration of i) the importance of parameters to assess SICI (Exp.1) and ii) the inhibitory process within the primary motor cortex as an inherent feature of MI (Exp.2). Participants performed two tasks: 1) rest and 2) imagery of isometric abduction of the right index finger. Using transcranial magnetic stimulation, motor evoked potentials were elicited in the right first dorsal interosseous muscle. An adaptive threshold-hunting paradigm was used, where the stimulus intensity required to maintain a fixed motor evoked potential amplitude was quantified. To test SICI, we conditioned the test stimulus with a conditioning stimulus (CS) of different intensities. Results revealed an Intensity by Task interaction showing that SICI decreased during MI as compared to rest only for the higher CS intensity (Exp.1). At the lowest CS intensities, a Task main effect revealed that SICI increased during MI (Exp.2). SICI modulation during MI depends critically on the CS intensity. By optimising CS intensity, we have shown that SICI circuits may increase during MI, revealing a potential mechanism to prevent the production of a movement while the motor system is activated.HighlightsExcitatory and inhibitory neural processes interact during motor imagery, as the motor regions are activated but no movement is produced.The current study investigated the extent of short interval intracortical inhibition modulation (SICI) during motor imagery.When using optimal settings, SICI increased during motor imagery, likely to prevent the production of an overt movement.

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