Abstract
The spinal cord participates in the execution of skilled movements by translating high-level cerebral motor representations into musculotopic commands. Yet, the extent to which motor skill acquisition relies on intrinsic spinal cord processes remains unknown. To date, attempts to address this question were limited by difficulties in separating spinal local effects from supraspinal influences through traditional electrophysiological and neuroimaging methods. Here, for the first time, we provide evidence for local learning-induced plasticity in intact human spinal cord through simultaneous functional magnetic resonance imaging of the brain and spinal cord during motor sequence learning. Specifically, we show learning-related modulation of activity in the C6–C8 spinal region, which is independent from that of related supraspinal sensorimotor structures. Moreover, a brain–spinal cord functional connectivity analysis demonstrates that the initial linear relationship between the spinal cord and sensorimotor cortex gradually fades away over the course of motor sequence learning, while the connectivity between spinal activity and cerebellum gains strength. These data suggest that the spinal cord not only constitutes an active functional component of the human motor learning network but also contributes distinctively from the brain to the learning process. The present findings open new avenues for rehabilitation of patients with spinal cord injuries, as they demonstrate that this part of the central nervous system is much more plastic than assumed before. Yet, the neurophysiological mechanisms underlying this intrinsic functional plasticity in the spinal cord warrant further investigations.
Highlights
Results from a plethora of studies clearly indicate that the learning of new motor skills in humans induces functional plasticity in a distributed network of brain areas [1,2,3,4]
The present findings have important clinical implications for rehabilitation of patients with spinal cord injuries, as they demonstrate that this part of the central nervous system is much more plastic than it was assumed before
This suggests that distinct learning mechanisms were involved during the simple sequence (SS) and complex sequence (CS) training conditions, the former being due to a general improvement in motor performance by repeated practice and the latter resulting from sequence-related improvements in motor performance in addition to the nonspecific motor practice effect [18]
Summary
Results from a plethora of studies clearly indicate that the learning of new motor skills in humans induces functional plasticity in a distributed network of brain areas [1,2,3,4]. Human motor learning models usually consider the spinal cord as a passive relay of information from the brain (controller) to the muscles (effectors), with no active learning-related role entrusted to the spinal circuitry [12] This view mainly stems from a computational perspective of motor learning, which assumes that circuits at the spinal cord level, on which cortical plasticity is grounded and stabilized, are hardwired [6]. In an innovative electrophysiological study, Meunier et al [15] showed that homosynaptic depression in soleus muscle (i.e., a measure of local depletion in primary afferent neurotransmitters) significantly changed following adaptation to a complex pattern of changes in resistance during stationary cycling This finding suggests that the pattern of sensory inflow plays an essential role in producing plasticity at the level of spinal cord. One way to overcome this limitation is to record both the brain and spinal cord activities simultaneously in order to assess the extent to which changes in the spinal cord activity correlate with or are statistically independent from the plastic changes that happen at the brain level during motor learning, allowing the identification of intrinsic changes at the spinal cord level
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