The intracortical excitability changes underlying the enhancing effects of rewards and punishments on motor performance

Hamel, R.; Pearson, J.; Sifi, L.; Patel, D.; Hinder, M.R.; Jenkinson, N.; Galea, J.M.

doi:10.1016/j.brs.2023.09.022

Cited by 4 publications

(5 citation statements)

References 90 publications

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“…It should be noted that the present results do not fully replicate our previous work 8 . Namely, our previous work showed that SICI decreased when both the right index and little fingers initiated the sequences, suggesting finger-unspecificity.…”

Section: Bilateral Decreases Of Sici During Unilateral Motor Preparationcontrasting

confidence: 99%

“…One possibility is that SICI levels acutely decrease to support motor preparation of various tasks [6][7][8] , and tonically shift to support motor sequence learning.…”

Section: Discussionmentioning

confidence: 99%

“…To address this question, one must consider the known processes of motor preparation, neural substrates of sequence learning, and whether sequence learning alters motor preparation in these substrates. First, brain stimulation evidence suggests that one robust process of motor preparation consists of short intracortical inhibition (SICI) decreases in the contralateral motor cortex (M1) [6][7][8] , which is thought to reflect decreases in intracortical type A gamma-aminobutyric acid (GABAA)-mediated inhibition 9 . For instance, using paired-pulse transcranial magnetic stimulation (ppTMS), Hamel et al (2023) 8 showed that SICI decreases in the left M1 as participants prepare to execute sequences with their right hand.…”

Section: Introductionmentioning

confidence: 99%

“…First, brain stimulation evidence suggests that one robust process of motor preparation consists of short intracortical inhibition (SICI) decreases in the contralateral motor cortex (M1) [6][7][8] , which is thought to reflect decreases in intracortical type A gamma-aminobutyric acid (GABAA)-mediated inhibition 9 . For instance, using paired-pulse transcranial magnetic stimulation (ppTMS), Hamel et al (2023) 8 showed that SICI decreases in the left M1 as participants prepare to execute sequences with their right hand. Given that sequence learning alters motor preparation processes 4,5 , one possibility is that sequence learning alters such SICI decreases during motor preparation 8 .…”

Section: Introductionmentioning

confidence: 99%

“…For instance, using paired-pulse transcranial magnetic stimulation (ppTMS), Hamel et al (2023) 8 showed that SICI decreases in the left M1 as participants prepare to execute sequences with their right hand. Given that sequence learning alters motor preparation processes 4,5 , one possibility is that sequence learning alters such SICI decreases during motor preparation 8 . Moreover, other ppTMS studies complement this evidence by showing that resting SICI levels decrease in the contralateral M1 when learning to perform sequential pinch 10 and fast thumb abduction movements 11 , which further hints at the possibility that SICI levels are altered as sequence learning progresses.…”

Section: Introductionmentioning

confidence: 99%

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Bilateral Intracortical Inhibition during Unilateral Motor Preparation and Sequence Learning

Hamel,

Waltzing,

Hinder

et al. 2023

Preprint

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Motor sequence learning gradually quickens reaction time, suggesting that sequence learning alters motor preparation processes. Interestingly, evidence has shown that preparing sequence movements decreases short intracortical inhibition (SICI) in the contralateral motor cortex (M1), but also that sequence learning alters motor preparation processes in both the contralateral and ipsilateral M1s. Therefore, one possibility is that sequence learning alters the SICI decreases occurring during motor preparation in bilateral M1s. To examine this, two novel hypotheses were tested: unilateral sequence preparation would decrease SICI in bilateral M1s, and sequence learning would alter such bilateral SICI responses. Paired-pulse transcranial magnetic stimulation was delivered over the contralateral and ipsilateral M1s to assess SICI in an index finger muscle during the preparation of sequences initiated by either the right index or little finger. In the absence of sequence learning, SICI decreased in both the contralateral and ipsilateral M1s during the preparation of sequences initiated by the right index finger, suggesting that SICI decreases in bilateral M1s during unilateral motor preparation. As sequence learning progressed, SICI decreased in the contralateral M1 whilst it increased in the ipsilateral M1. Moreover, these bilateral SICI responses were observed at the onset of motor preparation, suggesting that sequence learning altered baseline SICI levels rather than the SICI decreases occurring during motor preparation per se. Altogether, these results suggest that SICI responses in bilateral M1s reflect two motor processes: an acute decrease of inhibition during motor preparation, and a cooperative but bidirectional shift of baseline inhibition levels as sequence learning progresses.

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Section: Bilateral Decreases Of Sici During Unilateral Motor Preparationcontrasting

confidence: 99%

“…One possibility is that SICI levels acutely decrease to support motor preparation of various tasks [6][7][8] , and tonically shift to support motor sequence learning.…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Bilateral Intracortical Inhibition during Unilateral Motor Preparation and Sequence Learning

Hamel,

Waltzing,

Hinder

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

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Bilateral intracortical inhibition during unilateral motor preparation and sequence learning

Hamel,

Waltzing,

Hinder

et al. 2024

Brain Stimulation

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Effects Of Extrinsic Reward Based Skill Learning On Motor Plasticity

Yadav,

Vassiliadis,

Dubuc

et al. 2024

Preprint

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Human motor skill acquisition is improved by performance feedback and coupling such feedback with extrinsic reward (such as money) can enhance skill learning. However, the neurophysiology underlying such behavioral effect is unclear. To bridge this gap, we assessed the effects of reward on multiple forms of motor plasticity during skill learning. Sixty-five healthy participants divided in three groups performed a pinch-grip skill task with sensory feedback only, sensory and reinforcement feedback or both feedback coupled with an extrinsic monetary reward during skill training. To probe motor plasticity, we applied transcranial magnetic stimulation on the left primary motor cortex at rest before, during and after training in the three groups. We evaluated the amplitude and variability of corticospinal output, GABA-ergic short-intracortical inhibition and use-dependent plasticity before training and at two time points during and after training. At the behavioral level, monetary reward accelerated skill learning. In parallel, corticospinal output became less variable early on during training in the presence of extrinsic reward. Interestingly, this effect was particularly pronounced for participants who were more sensitive to reward, as evaluated in an independent questionnaire. Other measures of motor excitability remained comparable across groups. These findings highlight that a mechanism underlying the benefit of reward on motor skill learning is the fine tuning of early-training resting-state corticospinal variability.SIGNIFICANCE STATEMENTSkill acquisition is enhanced in the presence of reward. Despite its potential clinical relevance for motor rehabilitation, the underlying neurophysiological mechanisms remain largely unexplored. Specifically, whether reward affects the plasticity of motor cortex in the context of skill learning is unclear. We show that reward reduces the variability of corticospinal output at an early stage during training and that this effect correlates with individual sensitivity to reward. Our results suggest that a key mechanism underlying the beneficial effect of reward on motor skill learning may be an increase in the stability of motor output in response to training during early stages of skill learning.

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The intracortical excitability changes underlying the enhancing effects of rewards and punishments on motor performance

Cited by 4 publications

References 90 publications

Bilateral Intracortical Inhibition during Unilateral Motor Preparation and Sequence Learning

Bilateral Intracortical Inhibition during Unilateral Motor Preparation and Sequence Learning

Bilateral intracortical inhibition during unilateral motor preparation and sequence learning

Effects Of Extrinsic Reward Based Skill Learning On Motor Plasticity

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