Afferents to Action: Cortical proprioceptive processing assessed with corticokinematic coherence specifically predicts gross motor skills

Abstract

Voluntary motor control is thought to be predicated on the ability to efficiently integrate and process somatosensory afferent information. However, current approaches in the field of motor control have not factored in objective markers of how the brain actually tracks incoming somatosensory information. Here, we asked whether motor performance relates with such markers obtained with an analysis of the coupling between peripheral kinematics and cortical oscillations during continuous movements, best known as corticokinematic coherence (CKC). Motor performance was evaluated by measuring both gross and fine motor skills using the Box and Blocks Test (BBT) and the Purdue Pegboard Test (PPT), respectively, and with a biomechanics measure of coordination. Sixty-one participants completed the BBT, while equipped with electroencephalography and electromyography, and the PPT. We evaluated CKC, from the signals collected during the BBT, as the coherence between movement rhythmicity and brain activity, and coordination as the cross-correlation between muscle activity. CKC at movements first harmonic was positively associated with BBT scores, and showed a relationship with PPT scores, but only in synergy with BBT scores, where participants with lower PPT score had higher CKC than expected based on their BBT score. Coordination was not associated with motor performance and at most, weakly related to CKC. These findings demonstrate that cortical somatosensory processing in the form of strengthened brain-peripheral coupling is specifically associated with better gross motor skills. CKC might be considered as a valuable addition to classical tests of proprioceptive acuity, with important perspectives for future clinical studies and practice. Significance StatementWhether standing upright, jogging, or in Olympic competition, our nervous system not only sends out motor commands prompting muscles to contract, but also receives incoming information to fine-tune motor actions. Though the machinery involved in sensing mechanical changes is well-described, the neural processing of this information is not, making its relevance to motor function unresolved. We found that the coupling strength between peripheral kinematics and cortical activity was related to motor function and at most, only weakly related to conventional muscle-only assessments. We present novel behavioral relevance of this coupling and its specific relationship to gross motor skill. Our study paves the way for including novel brain-centered approaches to complement classical assessment sensorimotor functions in health and disease.