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An acute session of motor imagery training induces use-dependent plasticity.

ABSTRACT: Motor imagery, defined as the mental representation of an action without movement-related sensory inputs, is a well-known intervention to improve motor performance. In the current study, we tested whether use-dependent plasticity, a mechanism underlying motor learning, could be induced by an acute session of motor imagery. By means of transcranial magnetic stimulation (TMS) over the left primary motor cortex, we evoked isolated thumb movements in the right hand and assessed corticospinal excitability in the flexor and extensor pollicis brevis muscles. We measured the mean TMS-induced movement direction before and after an acute session of motor imagery practice. In a first experiment, participants of the imagery group were instructed to repeatedly imagine their thumb moving in a direction deviated by 90° from the pre-test movement. This group, but not the control group, deviated the post-training TMS-induced movements toward the training target direction (+44°?±?62° and -1°?±?23°, respectively). Interestingly, the deviation magnitude was driven by the corticospinal excitability increase in the agonist muscle. In a second experiment, we found that post-training TMS-induced movements were proportionally deviated toward the trained direction and returned to baseline 30?minutes after the motor imagery training. These findings suggest that motor imagery induces use-dependent plasticity and, this neural process is accompanied by corticospinal excitability increase in the agonist muscle.

SUBMITTER: Ruffino C

PROVIDER: S-EPMC6934610 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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An acute session of motor imagery training induces use-dependent plasticity.

Ruffino Célia C Gaveau Jérémie J Papaxanthis Charalambos C Lebon Florent F

Scientific reports 20191227 1

Motor imagery, defined as the mental representation of an action without movement-related sensory inputs, is a well-known intervention to improve motor performance. In the current study, we tested whether use-dependent plasticity, a mechanism underlying motor learning, could be induced by an acute session of motor imagery. By means of transcranial magnetic stimulation (TMS) over the left primary motor cortex, we evoked isolated thumb movements in the right hand and assessed corticospinal excitab ...[more]

PMID: 31882851

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Project description:Motor behaviors are shaped not only by current sensory signals but also by the history of recent experiences. For instance, repeated movements toward a particular target bias the subsequent movements toward that target direction. This process, called use-dependent plasticity (UDP), is considered a basic and goal-independent way of forming motor memories. Most studies consider movement history as the critical component that leads to UDP (Classen et al., 1998; Verstynen and Sabes, 2011). However, the effects of learning (i.e., improved performance) on UDP during movement repetition have not been investigated. Here, we used transcranial magnetic stimulation in two experiments to assess plasticity changes occurring in the primary motor cortex after individuals repeated reinforced and nonreinforced actions. The first experiment assessed whether learning a skill task modulates UDP. We found that a group that successfully learned the skill task showed greater UDP than a group that did not accumulate learning, but made comparable repeated actions. The second experiment aimed to understand the role of reinforcement learning in UDP while controlling for reward magnitude and action kinematics. We found that providing subjects with a binary reward without visual feedback of the cursor led to increased UDP effects. Subjects in the group that received comparable reward not associated with their actions maintained the previously induced UDP. Our findings illustrate how reinforcing consistent actions strengthens use-dependent memories and provide insight into operant mechanisms that modulate plastic changes in the motor cortex.SIGNIFICANCE STATEMENT Performing consistent motor actions induces use-dependent plastic changes in the motor cortex. This plasticity reflects one of the basic forms of human motor learning. Past studies assumed that this form of learning is exclusively affected by repetition of actions. However, here we showed that success-based reinforcement signals could affect the human use-dependent plasticity (UDP) process. Our results indicate that learning augments and interacts with UDP. This effect is important to the understanding of the interplay between the different forms of motor learning and suggests that reinforcement is not only important to learning new behaviors, but can shape our subsequent behavior via its interaction with UDP.

Project description:BackgroundChronic microglia-mediated inflammation and oxidative stress are well-characterized underlying factors in neurodegenerative disease, whereby reactive inflammatory microglia enhance ROS production and impact neuronal integrity. Recently, it has been shown that during chronic inflammation, neuronal integrity is compromised through targeted disruption of the axon initial segment (AIS), the axonal domain critical for action potential initiation. AIS disruption was associated with contact by reactive inflammatory microglia which wrap around the AIS, increasing association with disease progression. While it is clear that chronic microglial inflammation and enhanced ROS production impact neuronal integrity, little is known about how acute microglial inflammation influences AIS stability. Here, we demonstrate that acute neuroinflammation induces AIS structural plasticity in a ROS-mediated and calpain-dependent manner.MethodsC57BL/6J and NOX2-/- mice were given a single injection of lipopolysaccharide (LPS; 5 mg/kg) or vehicle (0.9% saline, 10 mL/kg) and analyzed at 6 h-2 weeks post-injection. Anti-inflammatory Didox (250 mg/kg) or vehicle (0.9% saline, 10 mL/kg) was administered beginning 24 h post-LPS injection and continued for 5 days; animals were analyzed 1 week post-injection. Microglial inflammation was assessed using immunohistochemistry (IHC) and RT-qPCR, and AIS integrity was quantitatively analyzed using ankyrinG immunolabeling. Data were statistically compared by one-way or two-way ANOVA where mean differences were significant as assessed using Tukey's post hoc analysis.ResultsLPS-induced neuroinflammation, characterized by enhanced microglial inflammation and increased expression of ROS-producing enzymes, altered AIS protein clustering. Importantly, inflammation-induced AIS changes were reversed following resolution of microglial inflammation. Modulation of the inflammatory response using anti-inflammatory Didox, even after significant AIS disruption occurred, increased the rate of AIS recovery. qPCR and IHC analysis revealed that expression of microglial NOX2, a ROS-producing enzyme, was significantly increased correlating with AIS disruption. Furthermore, ablation of NOX2 prevented inflammation-induced AIS plasticity, suggesting that ROS drive AIS structural plasticity.ConclusionsIn the presence of acute microglial inflammation, the AIS undergoes an adaptive change that is capable of spontaneous recovery. Moreover, recovery can be therapeutically accelerated. Together, these findings underscore the dynamic capabilities of this domain in the presence of a pathological insult and provide evidence that the AIS is a viable therapeutic target.

Project description:BackgroundParkinson's disease (PD) causes difficulty with maintaining the speed, size, and vigor of movements, especially when they are internally generated. We previously proposed that the insula is important in motivating intentional movement via its connections with the dorsomedial frontal cortex (dmFC). We demonstrated that subjects with PD can increase the right insula-dmFC functional connectivity using fMRI-based neurofeedback (NF) combined with kinesthetic motor imagery (MI). The current study is a randomized clinical trial testing whether NF-guided kinesthetic MI training can improve motor performance and increase task-based and resting-state right insula-dmFC functional connectivity in subjects with PD.MethodsWe assigned nondemented subjects with mild PD (Hoehn & Yahr stage ≤ 3) to the experimental kinesthetic MI with NF (MI-NF, n = 22) and active control visual imagery (VI, n = 22) groups. Only the MI-NF group received NF-guided MI training (10-12 runs). The NF signal was based on the right insula-dmFC functional connectivity strength. All subjects also practiced their respective imagery tasks at home daily for 4 weeks. Post-training changes in 1) task-based and resting-state right insula-dmFC functional connectivity were the primary imaging outcomes, and 2) MDS-UPDRS motor exam and motor function scores were the primary and secondary clinical outcomes, respectively.ResultsThe MI-NF group was not significantly different from the VI group in any of the primary imaging or clinical outcome measures. The MI-NF group reported subjective improvement in kinesthetic body awareness. There was significant and comparable improvement only in motor function scores in both groups (secondary clinical outcome). This improvement correlated with NF regulation of the right insula-dmFC functional connectivity only in the MI-NF group. Both groups showed specific training effects in whole-brain functional connectivity with distinct neural circuits supporting kinesthetic motor and visual imagery (exploratory imaging outcome).ConclusionsThe functional connectivity-based NF regulation was unsuccessful, however, both kinesthetic MI and VI practice improved motor function in our cohort with mild PD.

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An acute session of motor imagery training induces use-dependent plasticity.

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An acute session of motor imagery training induces use-dependent plasticity.

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