Motor learning induces time-dependent plasticity that is observable at the spinal cord level.

Mélanie Henry,Andreas Kramer,Craig Tokuno,Markus Gruber,Louis‐Solal Giboin

doi:10.1113/jp278890

Mélanie Henry, Andreas Kramer + Show 3 more

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https://doi.org/10.1113/jp278890

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Abstract

The spinal cord is an important contributor to motor learning It remains unclear whether short-term spinal cord adaptations are general or task-specific Immediately after task acquisition, neural adaptations were not specific to the trained task (i.e. were general) Twenty-four hours after acquisition, neural adaptations appeared to be task-specific The neural reorganization and generalization of spinal adaptations appears to be time-dependent. Spinal cord plasticity is an important contributor of motor learning in humans, although its mechanisms are still poorly documented. In particular, it remains unclear whether short-term spinal adaptations are general or task-specific. As a marker of neural changes that are observable at spinal level, we measured the Hoffmann reflex (H-reflex) amplitude in the soleus muscle of 18 young healthy human adults before, immediately after (acquisition), and 24 h after (retention) the learning of a skilled task (i.e. one-legged stance on a tilt board). H-reflexes were elicited 46±30ms before touching the tilt board. Additionally, and at the same time points, we measured the H-reflex with the subject sitting at rest and when performing an unskilled and untrained task (i.e. one-legged stance on the floor). After task acquisition, there was a decrease of the H-reflex amplitude measured at rest but not during the skilled or the unskilled task. At retention, there was a decrease of the H-reflex when measured during the skilled task but not during the unskilled task or at rest. Performance increase was not associated with changes in the H-reflex amplitude. After the acquisition of a new skilled task, spinal changes appeared to be general (i.e. observable at rest). However, 24 h after, these changes were task-specific (i.e. observable only during performance of the trained task). These results imply that skill training induces a time-dependent reorganization of the modulation of spinal networks, which possibly reflects a time-dependent optimization of the feedforward motor command.

Highlights

Because the spinal cord is often referred to as the ‘final common path’ (Sherrington, 1906), this would imply that any general change that occurs at the spinal level would require an adaptation of all descending motor commands of previously adopted motor behaviours (Rothwell, 2012; Wolpaw, 2018)
This result indicates that the mean difference of performance between retention and post-acquisition was −0.13 but, because the credible interval contains zero, we cannot support the hypothesis that there was a difference of performance between retention and acquisition
This is supported by the low evidence ratio, indicating that the probability that performance is higher at retention compared to acquisition is 0.22 higher than the probability that the performance was higher at acquisition compared to retention

Summary

Introduction

A multitude of studies demonstrate that neural plasticity associated with motor learning occurs within supraspinal structures, and can be observed at the spinal cord level as well (Carp & Wolpaw, 1994; Feng-Chen & Wolpaw, 1996; Perez et al 2005; Mazzocchio et al 2006; Gruber et al 2007; Meunier et al 2007; Geertsen et al 2008; Vahdat et al 2015; Giboin et al 2019c). This theory states that the substrates of motor learning are distributed and hierarchized within the CNS (i.e. brain plasticity induces and maintains spinal cord plasticity), and that all motor behaviours are continuously maintained and in concurrent negotiation with each other (Wolpaw, 2018) In line with this theory, it has been demonstrated that general changes in the spinal cord, induced by Hoffmann reflex (H-reflex) operant conditioning, could be compensated by other networks at the spinal or supraspinal level to prevent undesired changes in locomotion (Chen et al 2017). This is an important point to consider because many H-reflex experiments in humans have demonstrated rapid changes at the spinal cord level, including immediately after motor skill learning (Perez et al 2005), and even at the very beginning of the motor learning process (Lungu et al 2010)

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