Population recordings of human motor units often display 'onion skin' discharge patterns -- implications for voluntary motor control

Abstract

Over the past two decades, there has been a radical transformation in our ability to extract useful biological signals from the surface electromyogram (EMG). Advances in EMG electrode design and signal processing techniques have resulted in an extraordinary capacity to identify motor unit spike trains from the surface of a muscle. These EMG grid, or high-density surface EMG (HDsEMG), recordings now provide accurate depictions of as many as 20-30 motor unit spike trains simultaneously during isometric contractions, even at high forces. Such multi-unit recordings often display an unexpected feature known as onion skin behavior, in which multiple motor unit spike trains show essentially parallel and organized increases in discharge rate with increases in voluntary force, such that the earliest recruited units reach the highest discharge rates, while higher threshold units display more modest rate increases. This sequence results in an orderly pattern of discharge resembling the layers of an onion, in which discharge rate trajectories stay largely parallel and rarely cross. Our objective in this review is to explain why this pattern of discharge rates is unexpected, why it does not accurately reflect our current understanding of motoneuron electrophysiology, and why it may potentially lead to unpredicted disruption in muscle force generation. This review is aimed at the practicing clinician, or the clinician scientist. More advanced descriptions of potential electrophysiological mechanisms associated with onion skin characteristics targeting the research scientist will be provided as reference material.