Simultaneous Brain–Cervical Cord fMRI Reveals Intrinsic Spinal Cord Plasticity during Motor Sequence Learning

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.

脊髓在执行熟练动作的过程中，通过将高级脑部运动表征转化为肌肉拓扑指令发挥着关键作用。然而，关于运动技能习得在多大程度上依赖于脊髓内在过程的程度，至今尚无定论。迄今为止，由于传统电生理学和神经影像学方法难以将脊髓的局部效应与上位脑部的神经影响区分开来，因此针对这一问题的研究尝试受到了限制。在本研究中，我们首次通过在运动序列学习过程中同步进行大脑和脊髓的功能磁共振成像，提供了关于完整人类脊髓中局部学习诱导的可塑性的证据。具体而言，我们发现与相关上位脑部感觉运动结构的活动调节无关，C6-C8脊髓区域的活动与学习相关。此外，大脑-脊髓功能连接性分析表明，脊髓与感觉运动皮层之间的初始线性关系在运动序列学习过程中逐渐减弱，而脊髓活动与小脑之间的连接性则增强。这些数据表明，脊髓不仅是人类运动学习网络的一个活跃的功能组成部分，而且从大脑中独立贡献于学习过程。当前的发现为脊髓损伤患者的康复开辟了新的途径，因为它们表明这一部分中枢神经系统比之前所认为的更具可塑性。然而，脊髓内源性功能可塑性的神经生理机制仍需进一步研究。