Age-dependent modulation of motor network connectivity for skill acquisition, consolidation and interlimb transfer after motor practice.

OBJECTIVE: Age-related differences in neural strategies for motor learning are not fully understood. We determined the effects of age on the relationship between motor network connectivity and motor skill acquisition, consolidation, and interlimb transfer using dynamic imaging of coherent sources. METHODS: Healthy younger (n = 24, 18-24 y) and older (n = 24, 65-87 y) adults unilaterally practiced a visuomotor task and resting-state electroencephalographic data was acquired before and after practice as well as at retention. RESULTS: The results showed that right-hand skill acquisition and consolidation did not differ between age groups. However, age affected the ability to transfer the newly acquired motor skill to the non-practiced limb. Moreover, strengthened left- and right-primary motor cortex-related beta connectivity was negatively and positively associated with right-hand skill acquisition and left-hand skill consolidation in older adults, respectively. CONCLUSION: Age-dependent modulations of bilateral resting-state motor network connectivity indicate age-specific strategies for the acquisition, consolidation, and interlimb transfer of novel motor tasks. SIGNIFICANCE: The present results provide insights into the mechanisms underlying motor learning that are important for the development of interventions for patients with unilateral injuries.

Stress Modulates the Balance between Hippocampal and Motor Networks during Motor Memory Processing.

The functional interaction between hippocampo- and striato-cortical regions during motor sequence learning is essential to trigger optimal memory consolidation. Based on previous evidence from other memory domains that stress alters the balance between these systems, we investigated whether exposure to stress prior to motor learning modulates motor memory processes. Seventy-two healthy young individuals were exposed to a stressful or nonstressful control intervention prior to training on a motor sequence learning task in a magnetic resonance imaging (MRI) scanner. Consolidation was assessed with an MRI retest after a sleep episode. Behavioral results indicate that stress prior to learning did not influence motor performance. At the neural level, stress induced both a larger recruitment of sensorimotor regions and a greater disengagement of hippocampo-cortical networks during training. Brain-behavior regression analyses showed that while this stress-induced shift from (hippocampo-)fronto-parietal to motor networks was beneficial for initial performance, it was detrimental for consolidation. Our results provide the first experimental evidence that stress modulates the neural networks recruited during motor memory processing and therefore effectively unify concepts and mechanisms from diverse memory fields. Critically, our findings suggest that intersubject variability in brain responses to stress determines the impact of stress on motor learning and subsequent consolidation.

Spectral and temporal electroencephalography measures reveal distinct neural networks for the acquisition, consolidation, and interlimb transfer of motor skills in healthy young adults.

OBJECTIVE: Plasticity of the central nervous system likely underlies motor learning. It is however unclear, whether plasticity in cortical motor networks is motor learning stage-, activity-, or connectivity-dependent. METHODS: From electroencephalography (EEG) data, we quantified effective connectivity by the phase slope index (PSI), neuronal activity by event-related desynchronization, and sensorimotor integration by N30 during the stages of visuomotor skill acquisition, consolidation, and interlimb transfer. RESULTS: Although N30 amplitudes and event-related desynchronization in parietal electrodes increased with skill acquisition, changes in PSI correlated most with motor performance in all stages of motor learning. Specifically, changes in PSI between the premotor, supplementary motor, and primary motor cortex (M1) electrodes correlated with skill acquisition, whereas changes in PSI between electrodes representing M1 and the parietal and primary sensory cortex (S1) correlated with skill consolidation. The magnitude of consolidated interlimb transfer correlated with PSI between bilateral M1s and between S1 and M1 in the non-practiced hemisphere. CONCLUSIONS: Spectral and temporal EEG measures but especially PSI correlated with improvements in complex motor behavior and revealed distinct neural networks in the acquisition, consolidation, and interlimb transfer of motor skills. SIGNIFICANCE: A complete understanding of the neuronal mechanisms underlying motor learning can contribute to optimizing rehabilitation protocols.

Direct and crossed effects of somatosensory electrical stimulation on motor learning and neuronal plasticity in humans.

PURPOSE: Sensory input can modify voluntary motor function. We examined whether somatosensory electrical stimulation (SES) added to motor practice (MP) could augment motor learning, interlimb transfer, and whether physiological changes in neuronal excitability underlie these changes. METHODS: Participants (18-30 years, n = 31) received MP, SES, MP + SES, or a control intervention. Visuomotor practice included 300 trials for 25 min with the right-dominant wrist and SES consisted of weak electrical stimulation of the radial and median nerves above the elbow. Single- and double-pulse transcranial magnetic stimulation (TMS) metrics were measured in the intervention and non-intervention extensor carpi radialis. RESULTS: There was 27 % motor learning and 9 % (both p < 0.001) interlimb transfer in all groups but SES added to MP did not augment learning and transfer. Corticospinal excitability increased after MP and SES when measured at rest but it increased after MP and decreased after SES when measured during contraction. No changes occurred in intracortical inhibition and facilitation. MP did not affect the TMS metrics in the transfer hand. In contrast, corticospinal excitability strongly increased after SES with MP + SES showing sharply opposite of these effects. CONCLUSION: Motor practice and SES each can produce motor learning and interlimb transfer and are likely to be mediated by different mechanisms. The results provide insight into the physiological mechanisms underlying the effects of MP and SES on motor learning and cortical plasticity and show that these mechanisms are likely to be different for the trained and stimulated motor cortex and the non-trained and non-stimulated motor cortex.

Neuronal mechanisms of motor learning and motor memory consolidation in healthy old adults.

It is controversial whether or not old adults are capable of learning new motor skills and consolidate the performance gains into motor memory in the offline period. The underlying neuronal mechanisms are equally unclear. We determined the magnitude of motor learning and motor memory consolidation in healthy old adults and examined if specific metrics of neuronal excitability measured by magnetic brain stimulation mediate the practice and retention effects. Eleven healthy old adults practiced a wrist extension-flexion visuomotor skill for 20 min (MP, 71.3 years), while a second group only watched the templates without movements (attentional control, AC, n = 11, 70.5 years). There was 40 % motor learning in MP but none in AC (interaction, p < 0.001) with the skill retained 24 h later in MP and a 16 % improvement in AC. Corticospinal excitability at rest and during task did not change, but when measured during contraction at 20 % of maximal force, it strongly increased in MP and decreased in AC (interaction, p = 0.002). Intracortical inhibition at rest and during the task decreased and facilitation at rest increased in MP, but these metrics changed in the opposite direction in AC. These neuronal changes were especially profound at retention. Healthy old adults can learn a new motor skill and consolidate the learned skill into motor memory, processes that are most likely mediated by disinhibitory mechanisms. These results are relevant for the increasing number of old adults who need to learn and relearn movements during motor rehabilitation.

Direct and crossed effects of somatosensory stimulation on neuronal excitability and motor performance in humans.

This analytic review reports how prolonged periods of somatosensory electric stimulation (SES) with repetitive transcutaneous nerve stimulation can have 'direct' and 'crossed' effects on brain activation, corticospinal excitability, and motor performance. A review of 26 studies involving 315 healthy and 78 stroke and dystonia patients showed that the direct effects of SES increased corticospinal excitability up to 40% (effect size: 0.2 to 6.1) and motor performance up to 14% (effect size: 0.3 to 3.1) but these two features did not correlate. SES did not affect measures of intracortical excitability. Most likely, a long-term potentiation-like mechanism in the excitatory glutamatergic connections between the primary sensory and motor cortices mediates the direct effects of SES on corticospinal excitability and motor performance. We propose two models for the untested hypothesis that adding SES to unilateral motor practice could magnify the magnitude of inter-limb transfer. If tenable, the hypothesis would expand the evolving repertoire of sensory augmentation of cross-education using mirrors and add SES as an alternative to conventional rehabilitation strategies such as constraint-induced movement therapy.