Effect of Extrinsic Reward on Motor Plasticity during Skill Learning.

IF 2.7 3区 医学 Q3 NEUROSCIENCES eNeuro Pub Date : 2025-04-10 Print Date: 2025-04-01 DOI:10.1523/ENEURO.0410-24.2025
Goldy Yadav, Pierre Vassiliadis, Cecile Dubuc, Friedhelm C Hummel, Gerard Derosiere, Julie Duque
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Abstract

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 into 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 at rest, on the left primary motor cortex before, at an early-training time point, and after training in the three groups and measured motor-evoked potentials from task-relevant muscle of the right arm. This allowed us to evaluate the amplitude and variability of corticospinal output, GABAergic short-intracortical inhibition, and use-dependent plasticity before training and at two additional time points (early and end 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.

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外源奖励对技能学习运动可塑性的影响。
人类运动技能的学习可以通过表现反馈得到改善,而将这种反馈与外在奖励(如金钱)结合起来,可以促进技能的学习。然而,这种行为效应的神经生理学基础尚不清楚。为了填补这一空白,我们评估了奖励对技能学习过程中多种形式的运动可塑性的影响。65 名健康参与者分成三组,分别在仅有感官反馈、感官和强化反馈或同时有反馈和外在货币奖励的情况下进行捏握技能训练。为了探究运动的可塑性,我们在三个组的训练前、训练初期和训练后分别对左侧初级运动皮层进行了经颅磁刺激,并测量了右臂任务相关肌肉的运动诱发电位。这样,我们就能在训练前和另外两个时间点(训练初期和训练末期)评估皮质脊髓输出、GABA能短皮质内抑制和使用依赖性可塑性的幅度和可变性。在行为层面,金钱奖励加速了技能学习。与此同时,在存在外在奖励的情况下,皮质脊髓输出在训练早期的变化较小。有趣的是,根据一份独立问卷的评估,这种效应对于那些对奖励更敏感的参与者尤为明显。其他运动兴奋性测量指标在各组之间仍具有可比性。这些研究结果突出表明,奖励对运动技能学习有益的机制是对早期训练静息状态皮质脊髓变异性的微调。尽管奖励对运动康复具有潜在的临床意义,但其潜在的神经生理学机制在很大程度上仍未得到探索。具体来说,奖励是否会影响运动皮层在技能学习过程中的可塑性尚不清楚。我们的研究表明,在训练的早期阶段,奖励会降低皮质脊髓输出的可变性,而且这种效应与个体对奖励的敏感性相关。我们的研究结果表明,奖励对运动技能学习产生有利影响的一个关键机制可能是,在技能学习的早期阶段,运动输出的稳定性会随着训练的进行而增加。
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来源期刊
eNeuro
eNeuro Neuroscience-General Neuroscience
CiteScore
5.00
自引率
2.90%
发文量
486
审稿时长
16 weeks
期刊介绍: An open-access journal from the Society for Neuroscience, eNeuro publishes high-quality, broad-based, peer-reviewed research focused solely on the field of neuroscience. eNeuro embodies an emerging scientific vision that offers a new experience for authors and readers, all in support of the Society’s mission to advance understanding of the brain and nervous system.
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