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.