Graduate School of Frontier Biosciences, Osaka University

Japanese

Error signals in motor cortices drive adaptation in reaching

Journal Neuron 90, 1114-1126 (2016)
Authors Inoue M (1), Uchimura M (2), Kitazawa S (3)

  1. Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, and Osaka University, Yamadaoka 1-4, Suita, Osaka, 565-0871, Japan; Department of Neurophysiology, Juntendo University School of Medicine, Hongo 2-1-1, Bunkyo, Tokyo 113-8421, Japan. Electronic address: msinoue@nict.go.jp.
  2. Dynamic Brain Network Laboratory, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-3, Suita, Osaka 565-0871, Japan.
  3. Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, and Osaka University, Yamadaoka 1-4, Suita, Osaka, 565-0871, Japan; Department of Neurophysiology, Juntendo University School of Medicine, Hongo 2-1-1, Bunkyo, Tokyo 113-8421, Japan; Dynamic Brain Network Laboratory, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-3, Suita, Osaka 565-0871, Japan; Department of Brain Physiology, Graduate School of Medicine, Osaka University, Yamadaoka 1-3, Suita, Osaka 565-0871, Japan. Electronic address: kitazawa@fbs.osaka-u.ac.jp.
Title Error signals in motor cortices drive adaptation in reaching
PubMed 27181058
Laboratory Dynamic Brain Network Laboratory 〈Prof. Kitazawa〉
Abstract

Reaching movements are subject to adaptation in response to errors induced by prisms or external perturbations. Motor cortical circuits have been hypothesized to provide execution errors that drive adaptation, but human imaging studies to date have reported that execution errors are encoded in parietal association areas. Thus, little evidence has been uncovered that supports the motor hypothesis. Here, we show that both primary motor and premotor cortices encode information on end-point errors in reaching. We further show that post-movement microstimulation to these regions caused trial-by-trial increases in errors, which subsided exponentially when the stimulation was terminated. The results indicate for the first time that motor cortical circuits provide error signals that drive trial-by-trial adaptation in reaching movements.

Description

Adaptation in reaching - gradual improvement of motor control in response to a perturbation - is a central issue in motor neuroscience. However, even the cortical origin of errors that drive adaptation has remained elusive. In a new paper published in Neuron, Inoue, Uchimura and Kitazawa have shown that error signals encoded by motor cortical neurons drive adaptation in reaching.

  • The premotor and primary motor cortices encoded visual error in reaching.
  • Stimulation to the motor cortices induced trial-by-trial increases in reach errors.
  • The error increased opposite to the preferred direction of errors at each location.
  • The after-effect of stimulation subsided gradually as in ordinary adaptation.

The neural mechanisms of motor learning and adaptation constitute a central issue in both basic and clinical neuroscience. However, it is surprising that very little is known about the neural mechanisms underlying the motor learning and adaptation of voluntary arm movements. For example, the origin of cortical error signals that drive adaptation in reaching remains an unanswered question. A major theory in motor learning (feedback error learning) proposed by Kawato and Gomi (1992) hypothesized that error signals are provided by premotor circuits, including the motor cortical circuits. However, neuroimaging studies to date have not indicated whether motor cortices encode error signals. Preceding human imaging studies unanimously implicated parietal regions, such as areas 2, 5 and 7, in representing reaching errors.

In the current study, Inoue and colleagues were successful for the first time in inducing trial-by-trial "adaptation" in voluntary arm movements by artificial electrical stimulation of the premotor cortex (PM) or the primary motor cortex (M1). When the stimulation was terminated, the error (after-effect) did not decrease at once but recovered with practice, as observed after typical adaptation. The direction of the increase in the error was opposite to the "preferred" error direction of the neuron recorded in the stimulation site. The results clearly show that the motor cortices submit error signals that drive adaptation in voluntary arm movements, as predicted by the feedback error learning scheme.

The novel technique to artificially "improve" a motor skill by a small amount of stimulation would be applicable to performance enhancement in athletes as well as for restoring motor control in neurological patients.