Long-term motor skill training with individually adjusted progressive difficulty enhances learning and promotes corticospinal plasticity.

Motor skill acquisition depends on central nervous plasticity. However, behavioural determinants leading to long lasting corticospinal plasticity and motor expertise remain unexplored. Here we investigate behavioural and electrophysiological effects of individually tailored progressive practice during long-term motor skill training. Two groups of participants practiced a visuomotor task requiring precise control of the right digiti minimi for 6 weeks. One group trained with constant task difficulty, while the other group trained with progressively increasing task difficulty, i.e. continuously adjusted to their individual skill level. Compared to constant practice, progressive practice resulted in a two-fold greater performance at an advanced task level and associated increases in corticospinal excitability. Differences were maintained 8 days later, whereas both groups demonstrated equal retention 14 months later. We demonstrate that progressive practice enhances motor skill learning and promotes corticospinal plasticity. These findings underline the importance of continuously challenging patients and athletes to promote neural plasticity, skilled performance, and recovery.

Long-term progressive motor skill training enhances corticospinal excitability for the ipsilateral hemisphere and motor performance of the untrained hand.

It is well established that unilateral motor practice can lead to increased performance in the opposite non-trained hand. Here, we test the hypothesis that progressively increasing task difficulty during long-term skill training with the dominant right hand increase performance and corticomotor excitability of the left non-trained hand. Subjects practiced a visuomotor tracking task engaging right digit V for 6 weeks with either progressively increasing task difficulty (PT) or no progression (NPT). Corticospinal excitability (CSE) was evaluated from the resting motor threshold (rMT) and recruitment curve parameters following application of transcranial magnetic stimulation (TMS) to the ipsilateral primary motor cortex (iM1) hotspot of the left abductor digiti minimi muscle (ADM). PT led to significant improvements in left-hand motor performance immediately after 6 weeks of training (63 ± 18%, P < 0.001) and 8 days later (76 ± 14%, P < 0.001). In addition, PT led to better task performance compared to NPT (19 ± 15%, P = 0.024 and 27 ± 15%, P = 0.016). Following the initial training session, CSE increased across all subjects. After 6 weeks of training and 8 days later, only PT was accompanied by increased CSE demonstrated by a left and upwards shift in the recruitment curves, e.g. indicated by increased MEPmax (P = 0.012). Eight days after training similar effects were observed, but 14 months later motor performance and CSE were similar between groups. We suggest that progressively adjusting demands for timing and accuracy to individual proficiency promotes motor skill learning and drives the iM1-CSE resulting in enhanced performance of the non-trained hand. The results underline the importance of increasing task difficulty progressively and individually in skill learning and rehabilitation training.

Modulation of proprioceptive feedback during functional electrical stimulation: an fMRI study.

Functional electrical stimulation (FES) is sometimes used as a therapeutic modality in motor rehabilitation to augment voluntary motor drive to effect movement that would otherwise not be possible through voluntary activation alone. Effective motor rehabilitation should require that the central nervous system integrate efferent commands and appropriate afferent information to update the internal models of acquired skills. Here, we investigate whether FES-evoked (FES-ev) and FES-assisted (FES-as) movement are associated with the normal integration of motor commands and sensory feedback in a group of healthy participants during functional magnetic resonance imaging (fMRI). Sensory feedback was removed with a peripheral ischaemic nerve block while the participants performed voluntary (VOL), FES-ev or FES-as movement during fMRI. Before the peripheral nerve block, secondary somatosensory area (S2) activation was greater for the FES-ev and FES-as conditions than for the VOL condition. During the ischaemic nerve block, S2 activation was reduced for the FES-ev condition but not for FES-as and VOL conditions. The nerve block also reduced activation during FES in the primary somatosensory cortex and other motor areas including primary motor cortex, dorsal premotor cortex and supplementary motor area. In contrast, superior parietal lobule (area 7A) and precuneus activation was reduced as a consequence of the ischaemic nerve block in the VOL condition. These data suggest FES-related S2 activation is mainly a sensory phenomenon and does not reflect integration of sensory signals with motor commands.

Interaction of electrical stimulation and voluntary hand movement in SII and the cerebellum during simulated therapeutic functional electrical stimulation in healthy adults.

The therapeutic application of functional electrical stimulation (FES) has shown promising clinical results in the rehabilitation of post-stroke hemiplegia. It appears that the effect is optimal when the patterned electrical stimulation is used in close synchrony with voluntary movement, although the neural mechanisms that underlie the clinical successes reported with therapeutic FES are unknown. One possibility is that therapeutic FES takes advantage of the sensory consequences of an internal model. Here, we investigate fMRI cortical activity when FES is combined with voluntary effort (FESVOL) and we compare this activity to that produced when FES and voluntary activity (VOL) are performed alone. FESVOL revealed greater cerebellar activity compared with FES alone and reduced activity bilaterally in secondary somatosensory areas (SII) compared with VOL alone. Reduced activity was also observed for FESVOL compared with FES alone in the angular gyrus, middle frontal gyrus and inferior frontal gyrus. These findings indicate that during the VOL condition the cerebellum predicts the sensory consequences of the movement and this reduces the subsequent activation in SII. The decreased SII activity may reflect a better match between the internal model and the actual sensory feedback. The greater cerebellar activity coupled with reduced angular gyrus activity in FESVOL compared with FES suggests that the cortex may interpret sensory information during the FES condition as an error-like signal due to the lack of a voluntary component in the movement.

Illusory sensation of movement induced by repetitive transcranial magnetic stimulation.

Human movement sense relies on both somatosensory feedback and on knowledge of the motor commands used to produce the movement. We have induced a movement illusion using repetitive transcranial magnetic stimulation over primary motor cortex and dorsal premotor cortex in the absence of limb movement and its associated somatosensory feedback. Afferent and efferent neural signalling was abolished in the arm with ischemic nerve block, and in the leg with spinal nerve block. Movement sensation was assessed following trains of high-frequency repetitive transcranial magnetic stimulation applied over primary motor cortex, dorsal premotor cortex, and a control area (posterior parietal cortex). Magnetic stimulation over primary motor cortex and dorsal premotor cortex produced a movement sensation that was significantly greater than stimulation over the control region. Movement sensation after dorsal premotor cortex stimulation was less affected by sensory and motor deprivation than was primary motor cortex stimulation. We propose that repetitive transcranial magnetic stimulation over dorsal premotor cortex produces a corollary discharge that is perceived as movement.