Distinct mechanisms for online and offline motor skill learning across human development.

The human central nervous system (CNS) undergoes tremendous changes from childhood to adulthood and this may affect how individuals at different stages of development learn new skills. Here, we studied motor skill learning in children, adolescents, and young adults to test the prediction that differences in the maturation of different learning mechanisms lead to distinct temporal patterns of motor learning during practice and overnight. We found that overall learning did not differ between children, adolescents, and young adults. However, we demonstrate that adult-like skill learning is characterized by rapid and large improvements in motor performance during practice (i.e., online) that are susceptible to forgetting and decay over time (i.e., offline). On the other hand, child-like learning exhibits slower and less pronounced improvements in performance during practice, but these improvements are robust against forgetting and lead to gains in performance overnight without further practice. The different temporal dynamics of motor skill learning suggest an engagement of distinct learning mechanisms in the human CNS during development. In conclusion, adult-like skill learning mechanisms favor online improvements in motor performance whereas child-like learning mechanisms favors offline behavioral gains. RESEARCH HIGHLIGHTS: Many essential motor skills, like walking, talking, and writing, are acquired during childhood, and it is colloquially thought that children learn better than adults. We investigated dynamics of motor skill learning in children, adolescents, and young adults. Adults displayed substantial improvements during practice that was susceptible to forgetting over time. Children displayed smaller improvements during practice that were resilient against forgetting. The distinct age-related characteristics of these processes of acquisition and consolidation suggest that skill learning relies on different mechanisms in the immature and mature central nervous system.

Directed connectivity between primary and premotor areas underlying ankle force control in young and older adults.

The control of ankle muscle force is an integral component of walking and postural control. Aging impairs the ability to produce force steadily and accurately, which can compromise functional capacity and quality of life. Here, we hypothesized that reduced force control in older adults would be associated with altered cortico-cortical communication within a network comprising the primary motor area (M1), the premotor cortex (PMC), parietal, and prefrontal regions. We examined electroencephalographic (EEG) responses from fifteen younger (20-26 â€‹yr) and fifteen older (65-73 â€‹yr) participants during a unilateral dorsiflexion force-tracing task. Dynamic Causal Modelling (DCM) and Parametric Empirical Bayes (PEB) were used to investigate how directed connectivity between contralateral M1, PMC, parietal, and prefrontal regions was related to age group and precision in force production. DCM and PEB analyses revealed that the strength of connections between PMC and M1 were related to ankle force precision and differed by age group. For young adults, bidirectional PMC-M1 coupling was negatively related to task performance: stronger backward M1-PMC and forward PMC-M1 coupling was associated with worse force precision. The older group exhibited deviations from this pattern. For the PMC to M1 coupling, there were no age-group differences in coupling strength; however, within the older group, stronger coupling was associated with better performance. For the M1 to PMC coupling, older adults followed the same pattern as young adults - with stronger coupling accompanied by worse performance - but coupling strength was lower than in the young group. Our results suggest that bidirectional M1-PMC communication is related to precision in ankle force production and that this relationship changes with aging. We argue that the observed differences reflect compensatory reorganization that counteracts age-related sensorimotor declines and contributes to maintaining performance.

The development of functional and directed corticomuscular connectivity during tonic ankle muscle contraction across childhood and adolescence.

In adults, oscillatory activity in the sensorimotor cortex is coherent with contralateral muscle activity at beta frequencies (15-35 Hz) during tonic contraction. This functional coupling reflects the involvement of the sensorimotor cortex, the corticospinal pathway, and likely also ascending sensory feedback in the task at hand. However, little is known about the developmental trajectory of task-related corticomuscular connectivity relating to the voluntary control of the ankle muscles. To address this, we recorded electroencephalography (EEG) from the vertex (Cz) and electromyography (EMG) from ankle muscles (proximal and distal anterior tibial, TA; soleus, SOL; gastrocnemius medialis, GM) in 33 participants aged 7-23 yr during tonic dorsi- and plantar flexion requiring precise maintenance of a submaximal torque level. Coherence was calculated for Cz-TA, Cz-SOL, TA-TA, and SOL-GM signal pairs. We found strong, positive associations between age and beta band coherence for Cz-TA, Cz-SOL, and TA-TA, suggesting that oscillatory corticomuscular connectivity is strengthened during childhood development and adolescence. Directionality analysis indicated that the primary interaction underlying this age-related increase was in the descending direction. In addition, performance during dorsi- and plantar flexion tasks was positively associated with age, indicating more precise control of the ankle joint in older participants. Performance was also positively associated with beta band coherence, suggesting that participants with greater coherence also exhibited greater precision. We propose that these results indicate an age-related increase in oscillatory corticospinal input to the ankle muscle motoneuron pools during childhood development and adolescence, with possible implications for maturation of precision force control. Within the theoretical framework of predictive coding, we suggest that our results may reflect an age-related increase in reliance on feedforward control as the developing nervous system becomes better at predicting the sensory consequences of movement. These findings may contribute to the development of novel intervention strategies targeting improved sensorimotor control in children and adolescents with central motor disorders.

Oscillatory Corticospinal Activity during Static Contraction of Ankle Muscles Is Reduced in Healthy Old versus Young Adults.

Aging is accompanied by impaired motor function, but age-related changes in neural networks responsible for generating movement are not well understood. We aimed to investigate the functional oscillatory coupling between activity in the sensorimotor cortex and ankle muscles during static contraction. Fifteen young (20-26 yr) and fifteen older (65-73 yr) subjects were instructed to match a target force by performing static ankle dorsi- or plantar flexion, while electroencephalographic (EEG) activity was recorded from the cortex and electromyographic (EMG) activity was recorded from dorsi- (proximal and distal anterior tibia) and plantar (soleus and medial gastrocnemius) flexor muscles. EEG-EMG and EMG-EMG beta band (15-35 Hz) coherence was analyzed as an index of corticospinal activity. Our results demonstrated that beta cortico-, intra-, and intermuscular coherence was reduced in old versus young subjects during static contractions. Old subjects demonstrated significantly greater error than young subjects while matching target forces, but force precision was not related to beta coherence. We interpret this as an age-related decrease in effective oscillatory corticospinal activity during steady-state motor output. Additionally, our data indicate a potential effect of alpha coherence and tremor on performance. These results may be instrumental in developing new interventions to strengthen sensorimotor control in elderly subjects.

Effects of dynamic and isometric motor practice on position control, force control and corticomuscular coherence in preadolescent children.

In this study, we investigated the effects of motor practice with an emphasis on either position or force control on motor performance, motor accuracy and variability in preadolescent children. Furthermore, we investigated corticomuscular coherence and potential changes following motor practice. We designed a setup allowing discrete wrist flexions of the non-dominant hand and tested motor accuracy and variability when the task was to generate specific movement endpoints (15-75 deg) or force levels (5-25% MVC). All participants were tested in both tasks at baseline and post motor practice without augmented feedback on performance. Following baseline assessment, participants (44 children aged 9-11 years) were randomly assigned to either position (PC) or force control (FC) motor practice or a resting control group (CON). The PC and FC groups performed four blocks of 40 trials motor practice with augmented feedback on performance. Following practice, improvements in movement accuracy were significantly greater in the PC group compared to the FC and CON groups (p < 0.001). None of the groups displayed changes in force task performance indicating no benefits of force control motor practice and low transfer between tasks (p-values:0.08-0.45). Corticomuscular coherence (C4-FCR) was demonstrated during the hold phase in both tasks with no difference between tasks. Corticomuscular coherence did not change from baseline to post practice in any group. Our findings demonstrate that preadolescent children improve position control following dynamic accuracy motor practice. Contrary to previous findings in adults, preadolescent children displayed smaller or no improvements in force control following isometric motor practice, low transfer between tasks and no changes in corticomuscular coherence.

Trial-to-trial Variability and Cortical Processing Depend on Recent Outcomes During Human Reinforcement Motor Learning.

The history of our actions and their outcomes represent important information, informing choices and efficiently guiding future behavior. While unsuccessful (S-) outcomes are expected to lead to more explorative motor states and increased behavioral variability, successful (S+) outcomes are expected to reinforce the use of the previous action. Here, we show that humans attribute different values to previous actions during reinforcement motor learning when they experience S- compared to S+ outcomes. Behavioral variability after an S- outcome is influenced more by the previous outcome than after S+ outcomes. Using electroencephalography, we show that theta band oscillations of the prefrontal cortex are most prominent during changes in two consecutive outcomes, potentially reflecting the need for enhanced cognitive control. Our results suggest that S+ experiences 'overwrite' previous motor states to a greater extent than S- experiences and that modulations in neural oscillations in the prefrontal cortex play a potential role in encoding changes in movement variability state during reinforcement motor learning.

Reorganization of functional and directed corticomuscular connectivity during precision grip from childhood to adulthood.

How does the neural control of fine movements develop from childhood to adulthood? Here, we investigated developmental differences in functional corticomuscular connectivity using coherence analyses in 111 individuals from four different age groups covering the age range 8-30 y. EEG and EMG were recorded while participants performed a uni-manual force-tracing task requiring fine control of force in a precision grip with both the dominant and non-dominant hand. Using beamforming methods, we located and reconstructed source activity from EEG data displaying peak coherence with the EMG activity of an intrinsic hand muscle during the task. Coherent cortical sources were found anterior and posterior to the central sulcus in the contralateral hemisphere. Undirected and directed corticomuscular coherence was quantified and compared between age groups. Our results revealed that coherence was greater in adults (20-30 yo) than in children (8-10 yo) and that this difference was driven by greater magnitudes of descending (cortex-to-muscle), rather than ascending (muscle-to-cortex), coherence. We speculate that the age-related differences reflect maturation of corticomuscular networks leading to increased functional connectivity with age. We interpret the greater magnitude of descending oscillatory coupling as reflecting a greater degree of feedforward control in adults compared to children. The findings provide a detailed characterization of differences in functional sensorimotor connectivity for individuals at different stages of typical ontogenetic development that may be related to the maturational refinement of dexterous motor control.

Cortical signatures of precision grip force control in children, adolescents, and adults.

Human dexterous motor control improves from childhood to adulthood, but little is known about the changes in cortico-cortical communication that support such ontogenetic refinement of motor skills. To investigate age-related differences in connectivity between cortical regions involved in dexterous control, we analyzed electroencephalographic data from 88 individuals (range 8-30 years) performing a visually guided precision grip task using dynamic causal modelling and parametric empirical Bayes. Our results demonstrate that bidirectional coupling in a canonical 'grasping network' is associated with precision grip performance across age groups. We further demonstrate greater backward coupling from higher-order to lower-order sensorimotor regions from late adolescence in addition to differential associations between connectivity strength in a premotor-prefrontal network and motor performance for different age groups. We interpret these findings as reflecting greater use of top-down and executive control processes with development. These results expand our understanding of the cortical mechanisms that support dexterous abilities through development.

Acute Exercise Protects Newly Formed Motor Memories Against rTMS-induced Interference Targeting Primary Motor Cortex.

Acute cardiovascular exercise can promote motor memory consolidation following motor practice, and thus long-term retention, but the underlying mechanisms remain sparsely elucidated. Here we test the hypothesis that the positive behavioral effects of acute exercise involve the primary motor cortex and the corticospinal pathway by interfering with motor memory consolidation using non-invasive, low frequency, repetitive transcranial magnetic stimulation (rTMS). Forty-eight able-bodied, young adult male participants (mean age = 24.8 y/o) practiced a visuomotor accuracy task demanding precise and fast pinch force control. Following motor practice, participants either rested or exercised (20 min total: 3 × 3 min at 90% VO2peak) before receiving either sham rTMS or supra-threshold rTMS (115% RMT, 1 Hz) targeting the hand area of the contralateral primary motor cortex for 20 min. Retention was evaluated 24 h following motor practice, and motor memory consolidation was operationalized as overnight changes in motor performance. Low-frequency rTMS resulted in off-line decrements in motor performance compared to sham rTMS, but these were counteracted by a preceding bout of intense exercise. These findings demonstrate that a single session of exercise promotes early motor memory stabilization and protects the primary motor cortex and the corticospinal system against interference.

Corticospinal control of normal and visually guided gait in healthy older and younger adults.

We investigated age-related differences in corticospinal control of muscle activity during normal and visually guided (VG) walking. Young (n = 15, 22.1 ± 1.7 years) and older (n = 15, 68.3 ± 2.7 years) participants performed normal walking and VG walking requiring precise foot placement based on visual cues. Coherence analysis was used to quantify coupling between electroencephalography and electromyography from the anterior tibial muscle (corticomuscular) and between the 2 ends of the anterior tibial muscle (intramuscular) at 15-50 Hz during the swing phase of walking as markers of corticospinal activity. Our results indicated that corticomuscular and intramuscular coherence was lower in older compared to young participants during both tasks. In addition, coherence was generally greater during VG than during normal walking across age groups, although during late swing, older participants drove several of the observed task-related coherence increases. Performance on the VG task was lower in older compared to young participants and was correlated with task-related corticomuscular coherence modulations within the older group. These results suggest age-related differences in the corticospinal control of walking, with possible implications for precision control of foot placement based on visual information.

Using Corticomuscular and Intermuscular Coherence to Assess Cortical Contribution to Ankle Plantar Flexor Activity During Gait.

The present study used coherence and directionality analyses to explore whether the motor cortex contributes to plantar flexor muscle activity during the stance phase and push-off phase during gait. Subjects walked on a treadmill, while EEG over the leg motorcortex area and EMG from the medial gastrocnemius and soleus muscles was recorded. Corticomuscular and intermuscular coherence were calculated from pair-wise recordings. Significant EEG-EMG and EMG-EMG coherence in the beta and gamma frequency bands was found throughout the stance phase with the largest coherence towards push-off. Analysis of directionality revealed that EEG activity preceded EMG activity throughout the stance phase until the time of push-off. These findings suggest that the motor cortex contributes to ankle plantar flexor muscle activity and forward propulsion during gait.