Neural Substrates of Muscle Co-contraction during Dynamic Motor Adaptation

Abstract

As we learn to perform a motor task with novel dynamics, the central nervous system must adapt motor commands and modify sensorimotor transformations. The objective of the current research is to identify the neural mechanisms underlying the adaptive process. It has been shown previously that an increase in muscle co-contraction is frequently associated with the initial phase of adaptation and that co-contraction is gradually reduced as performance improves. Our investigation focused on the neural substrates of muscle co-contraction during the course of motor adaptation using a resting-state fMRI approach in healthy human subjects of both genders. We analyzed the functional connectivity in resting-state networks during three phases of adaptation, corresponding to different muscle co-contraction levels and found that change in the strength of functional connectivity in one brain network was correlated with a metric of co-contraction, and in another with a metric of motor learning. We identified the cerebellum as the key component for regulating muscle co-contraction, especially its connection to the inferior parietal lobule, which was particularly prominent in early stage adaptation. A neural link between cerebellum, superior frontal gyrus and motor cortical regions was associated with reduction of co-contraction during later stages of adaptation. We also found reliable changes in the functional connectivity of a network involving primary motor cortex, superior parietal lobule and cerebellum that were specifically related to the motor learning.

SIGNIFICANCE STATEMENT It is well known that co-contracting muscles is an effective strategy for providing postural stability by modulating mechanical impedance and thereby allowing the central nervous system to compensate for unfamiliar or unexpected physical conditions until motor commands can be appropriately adapted. The present study elucidates the neural substrates underlying the ability to modulate the mechanical impedance of a limb as we learn during motor adaptation. Using resting-state fMRI analysis we demonstrate that a distributed cerebellar-parietal-frontal network functions to regulate muscle co-contraction with the cerebellum as its key component.