Extrinsic and intrinsic dynamics in movement intermittency

• Published in: eLife Vol. 8
• Main Authors: Susilaradeya, Damar, Xu, Wei, Hall, Thomas M, Galán, Ferran, Alter, Kai, Jackson, Andrew
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 08.04.2019; eLife Sciences Publications, Ltd
• Subjects: Adult; Animals; Control theory; Cortex (motor); Feedback; Female; Human subjects; Humans; Macaca mulatta; Male; Models, Neurological; Motor Activity; motor cortex; Motor Cortex - physiology; Movement; movement intermittency; Nerve Net - physiology; Nervous system; Neuroscience; Noise; optimal feedback control; Oscillations; Research Communication; Rhesus macaque; Sensorimotor system; Sleep; submovements; Velocity; Young Adult; motor cortex; movement intermittency; neuroscience; optimal feedback control; submovements; Rhesus macaque; human
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.40145

What determines how we move in the world? Motor neuroscience often focusses either on intrinsic rhythmical properties of motor circuits or extrinsic sensorimotor feedback loops. Here we show that the interplay of both intrinsic and extrinsic dynamics is required to explain the intermittency observed in continuous tracking movements. Using spatiotemporal perturbations in humans, we demonstrate that apparently discrete submovements made 2–3 times per second reflect constructive interference between motor errors and continuous feedback corrections that are filtered by intrinsic circuitry in the motor system. Local field potentials in monkey motor cortex revealed characteristic signatures of a Kalman filter, giving rise to both low-frequency cortical cycles during movement, and delta oscillations during sleep. We interpret these results within the framework of optimal feedback control, and suggest that the intrinsic rhythmicity of motor cortical networks reflects an internal model of external dynamics, which is used for state estimation during feedback-guided movement. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (<xref ref-type="decision-letter" rid="SA1">see decision letter ).