Spinal cord contribution to motor skill learning

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For the last 20 years, psychophysical, multimodal neuroimaging and clinical population studies in my laboratory have increased our knowledge base of the behavioural determinants, neural networks and sleep characteristics mediating the early learning, consolidation, automatization and long-term retention of motor skilled behaviors. My work has allowed to better understand the specialized contribution from the cortico-striatal and cortico-cerebellar systems in motor learning, for example. Yet one important issue that has entirely been overlooked by the neuroscientific community is whether motor skill learning relies on brain plasticity only, or whether this memory process depends on spinal cord activity changes as well. With support from NSERC, we have recently demonstrated that the spinal cord does play a role in motor skill learning. Our results reveal that the learning of a new sequence of movements (MSL) produces a significant reduction of the Hoffman reflex elicited in the forearm1, as well as a specific and localized learning-dependent increase in blood oxygenated level dependent (BOLD) signal in C6-C8 spinal segments of young healthy subjects. Yet despite such advances, several fundamental questions remain regarding the mechanisms of action and brain-spine interaction during motor learning as such changes might also result from descending supraspinal influences. In this grant renewal, we intend to fill out this gap in a unique series of studies aimed at investigating brain-spine interactions in motor learning using a combination of electromyographic (EMG) recordings, magnetic and electrophysiological stimulation, as well as simultaneous tasks-related and resting-state functional magnetic resonance imaging (fMRI) of the brain and cervical spinal cord. The main objectives are: 1) To determine whether the learning-dependent changes that we observed in H-reflex and BOLD signal reflecting spinal cord activity are only found during MSL, or whether it generalizes to other forms of acquisition processes, motor skills and learning stages. 2) To identify the possible neurophysiological mechanisms underlying this learning-dependent spinal change in activity, and how this interacts with brain activity. More specifically, to address the first objective, I propose: a) to test whether the motor memory trace acquired during MSL can also be observed in spinal resting-state activity, b) to study the role of the spinal cord in both early and late learning phases of MSL, c) to determine the extent to which the spinal cord is active when subjects are implicitly learning a new sequence of movements as compared to when they are trained on an explicitly known sequence that only becomes more implicit with practice, and d) to explore whether the spinal cord also plays a role in our ability to adapt to changes in sensorimotor mapping (another form of motor skill called: visuomotor adaptation). Second, to address the second objective, I then plan: a) to assess the extent to which spinal plasticity during MSL relies mostly on habituation, presynaptic, postsynaptic, propriospinal or supraspinal mechanisms or a combination thereof, and b) to uncover the neuronal substrate underlying the mechanism(s) of action responsible for the change in motor learning-dependent activity at the spinal level, and its (their) functional link with brain activity. The experiments above will shed light on whether the spinal cord shows local plasticity during motor learning, what are the conditions and mechanisms under which such phenomena occurs, and how the spinal cord and brain work in concert to acquire and produce skilled motor actions. Insights gained in these studies will then lead to development and assessment of various rehabilitation techniques based on motor learning