Cortical adaptation to muscle fatigue does not alter early proprioceptive processing in primary sensorimotor cortex

Abstract

Muscle fatigue potentially interferes with proprioceptive afference from peripheral "movement sensors"-- the proprioceptors, which may hinder the crucial sensorimotor integration and thus locomotor performance. However, little is known about how muscle fatigue affects cortical processing of proprioceptive afference. Twenty-four healthy volunteers (30.7 {+/-} 6.5 yrs, 13 females) participated in the experiment, which included magnetoencephalography (MEG) recordings during ankle proprioceptive stimulation (2-Hz passive movements), and fatigue tasks comprised of isometric ankle plantar flexion. Corticokinematic coherence (CKC) between foot acceleration and MEG signals was examined before (PRE) and [~]3 min after (POST) the fatigue tasks to quantify the cortical proprioceptive processing. CKC peaked in the gradiometer pairs above the foot region of the primary sensorimotor (SM1) cortex in each participant. CKC strength did not show significant difference between PRE and POST at 2 Hz (0.30 {+/-} 0.12 vs. 0.30 {+/-} 0.14, p = 0.981) or its first harmonic at 4 Hz (0.38 {+/-} 0.14 vs. 0.37 {+/-} 0.13, p = 0.724). However, 4-Hz MEG power was [~]30% lower in POST than in PRE. Surprisingly, fatigue-induced bilateral increase of alpha and beta power was observed in SM1 hand regions during the movement stimulation. Our results indicated that the early processing of proprioceptive afference from the ankle joint was negligibly affected by muscle fatigue, or it recovered rapidly. The effects of muscle fatigue on the proprioceptive processing appear to extend beyond the primary somatotopic regions to bilateral SM1 neuronal networks. This cortical adaptation to muscle fatigue potentially preserves proprioceptive processing by modulating SM1 inhibitory neurons, offering a novel perspective for future research on proprioception.