Motor learning adaptations at the spinal cord level are task- and time-dependent: Implications for future investigations and treatment interventions.

Abstract

Motor learning is defined as the series of processes by which the performance of a task or skill is learned and refined through plastic reorganization within the nervous system. Although many studies have focused on deciphering the motor learning mechanisms within supraspinal structures, recent investigations have placed greater emphasis on understanding plastic responses at the spinal cord. The findings from these studies appear to suggest that reorganization at the spinal cord level is a unique response to skilled performance tasks as opposed to general motor activities and that the efficacy with which specificity is transferred may rely on a time component influenced by sleep or subsequent training sessions. In a recent study published in The Journal of Physiology, Giboin et al. (2020) further expand the motor learning literature by examining how the skill requirements of a balance task influence plastic changes at the spinal cord immediately and 24 h after practising the skill. Giboin et al. (2020) utilized a series of skill-graded balance performance tasks (i.e. sitting, unilateral standing, tilt board) to examine spinal cord plasticity via the Hoffmann reflex (H-reflex) amplitude relative to the M-wave of the soleus muscle. Eighteen healthy adults (10 women, eight men) underwent two assessment sessions separated by 24 h. During the first session, participants were tasked with learning how to perform a unilateral stance on a tilt board. Prior to practising the tilt board task (pre-acquisition), H-reflex amplitude was measured at rest, when standing unilaterally on the floor, and then when performing the tilt board task. Time to failure for the tilt board task was also assessed as a performance measure. Participants were then given 60 trials to practice the tilt board before H-reflex amplitude and performance were assessed across all three conditions again (post-acquisition). A second testing session, conducted 24 h later, was used to assess skill retention and determine any temporal effects of the skill acquisition (retention). Immediately following the skill acquisition session, H-reflex amplitude was decreased at rest. Interestingly, a similar decrease in H-reflex amplitude was observed during retention, but only during the tilt board task, despite no observed changes in performance from post-acquisition to retention. This provides compelling evidence that the plastic reorganization occurring within the spinal cord structures following skill training is probably both task- and time-dependent. This recent work by Giboin et al. (2020) brings to light several critical points for future investigations and interventions regarding motor learning. The findings of their study suggest that learning occurred at the motor neuron or spinal level as indicated by a down-regulation in H-reflex amplitude, potentially indicating a shift from a feedback-based motor command to feedforward. However, some issues regarding the validity of the H-reflex as a measure of plasticity at the spinal cord level are noted. Specifically, it was addressed that the H-reflex may not necessarily be indicative of plastic changes that occur exclusively at the spinal cord level and may reflect plastic changes that instead occur at supraspinal levels. Although it may be reasonable to hypothesize that changes in H-reflex amplitude observed at rest immediately after task acquisition may represent some short-term changes in plasticity at the spinal level, it may be argued that any conclusions drawn from these findings should be done so with caution. Prior studies have identified some limitations of the H-reflex. One such limitation is that the H-reflex is an electrically induced reflex that does not occur naturally in the human body, making it difficult to draw widely generalizable conclusions regarding dynamic muscle activity. Another limitation identified by prior studies is that the H-reflex may not accurately reflect motor neuron excitability considering synaptic connections between afferent and motor neurons may be subject to presynaptic modification. These limitations point towards the need for future research further investigating the validity of the H-reflex as an independent measure of plasticity at the spinal cord level. The decision by Giboin et al. (2020) to use a Bayesian linear mixed model in this investigation is prudent. When analysing data such as H-reflex amplitude, the inherent between-trial variability can present challenges determining where physiological phenomena actually occur. Linear mixed models will account for the high variability of the H-reflex and a Bayesian analysis will allow greater opportunity to discuss the credibility of results than frequentists statistics. The results of this analysis showed that H-reflex amplitude was higher during pre-acquisition than at retention with a strong evidence ratio during the tilt board task. Pre-acquisition H-reflex amplitude was also higher than post-acquisition but not retention during rest. This is interesting because there was an increase in performance from pre- to post-acquisition for the balance board task, yet no correlations were found between performance increases and changes in the H-reflex amplitude. To attempt to isolate H-reflex adaptations as a result of neural plasticity, Giboin et al. (2020) recorded M-wave and background electromyography (EMG) values. Background EMG values were higher during the floor and tilt board task than at rest, which is expected as a result of the increased muscle activity that occurs during task performance. Overall, the statistical approach used in this intervention was creative and appropriate. Bayesian approaches may prove to be an advantageous means of analysis in the fields of physiology or exercise science. Although no changes in performance on the tilt board task were observed, the decreased H-reflex amplitude during the balance task corresponds to a body of literature suggesting that motor learning and neuromuscular control is task-specific. The importance of task-specificity with respect to balance tasks has previously been emphasized by this group, reporting that slack-line training results in improved task-specific performance and neuromuscular control, without any improvements in general balance performance (Giboin et al. 2018; Ringhof et al. 2019). These findings may be clinically useful, especially in adults and children with neurological pathologies. Task-specific balance exercises, individualized to each patient's needs, may have more positive effects than general balance exercises on activities of daily living for post-stroke adults and children with neurological developmental disorders that affect coordination (Veerbeek et al. 2014). Task-specificity is also relevant in the context of strength-training adaptations and transferability. Among resistance-trained men, unstable variations of the chest-press exercise involving either dumbbells on a bench or a loaded barbell on a swiss ball resulted in greater task-specific strength gains compared to a stable variation of the chest-press using a Smith machine on a bench (Saeterbakken et al. 2016). This is probably because the unstable variations of the chest-press had greater potential for improvement in coordination compared to the fixed-path of a Smith machine. In the orthopaedic rehabilitation setting, one of the goals for common sports injuries, such as lateral ankle sprains, is to improve neuromuscular control of the muscles that help protect the joint. Based on the findings from Saeterbakken et al. (2016), it can be inferred that replicating similar, sport-specific scenarios and positions during rehabilitation with an added element of instability may help to improve neuromuscular control in a variety of unstable contexts. If applied appropriately, this approach may effectively lower the risk for re-injury and promote a safe return to sport. In addition to task-specificity, intensity of the practiced task contributes to motor learning. Although unmeasured, it is not unreasonable to suspect that the rate of perceived exertion was probably higher for the balance task on the tilt board compared to the balance task on the floor. Greater task intensity has been found to be associated with greater changes in neuroplasticity and corticospinal excitability, in agreement with the finding of Giboin et al. (2020) of decreased H-reflex amplitude for the balance tilt board task but not the floor balance task. Although conclusions cannot be drawn as to whether the down-regulated, task-specific H-reflex amplitude is resultant from adaptations at the spinal level or from supraspinal feedforward mechanisms, the findings support the use of task-specificity and intensity for addressing motor learning in both rehabilitation and performance settings. Clinicians who want to induce neuroplastic changes for improved motor learning in various populations (including neurological and orthopaedic) should consider individualizing the parameters that may affect neuroplasticity, including intensity and task-specificity. Although our current understanding of the exact mechanisms responsible for plastic reorganization at the spinal cord level during motor learning remains far from complete, the recent work by Giboin et al. (2020) presents valuable evidence regarding the specific task- and time-dependent nature of these adaptations. Furthermore, their investigation clarifies several avenues through which future studies can expand upon our understanding of spinal cord neuroplasticity at the same time as providing clinicians with several strategies to assist with improving motor performance. None. All authors have contributed towards and approved the final version. Each of the authors agree to be accountable for all aspects of the work. None. We thank Dr Matt S. Stock for his guidance in the preparation of this Journal Club submission.