Mechanisms that allow cortical preparatory activity without inappropriate movement.

Timothy R Darlington,Stephen G Lisberger

doi:10.7554/elife.50962

Abstract

We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEFSEM predicts movement, providing evidence against the 'movement-null' space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEFSEM population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.

Highlights

Preparation is an important component of voluntary movement
We have addressed the general question of how preparatory activity fails to evoke movement in the smooth eye movement region of the frontal eye fields (FEFSEM), a critical node in the neural circuit for smooth pursuit eye movements
We argue that the output of FEFSEM dials up visual-motor gain in preparation for a behaviorally-relevant visual motion of a specific direction and speed, and that the use of FEFSEM output as a sensorimotor gain signal allows preparation to proceed without causing movement

Summary

Introduction

Throughout the motor system, many neurons show modulation of firing rate that occurs during movement preparation that is linked to parameters of the ensuing movement (Dorris et al, 1997; Glimcher and Sparks, 1992; Hanes and Schall, 1996; Munoz and Wurtz, 1995; Tanaka and Fukushima, 1998; Tanji and Evarts, 1976; Weinrich and Wise, 1982; Wurtz and Goldberg, 1972; Churchland et al, 2006a, 2006b; Darlington et al, 2018; Hanes and Schall, 1996; Mahaffy and Krauzlis, 2011; Messier and Kalaska, 2000). The same cells that discharge in relation to the initiation of pursuit show an impressive ramp increase in firing rate during fixation, at a time when there is neither visual motion nor smooth eye movement (Mahaffy and Krauzlis, 2011; Tanaka and Fukushima, 1998). The preparatory activity grows over the hundreds of milliseconds preceding visual motion and the onset of pursuit, and its amplitude encodes expectation of upcoming target speed and combines with visual-motion input in a reliability-weighted manner to determine pursuit-related responses (Darlington et al, 2018)

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