Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets

Abstract
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Abstract

In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally-driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests via subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.

Data availability

Matlab scripts for running the model are provided as supplementary code files. Experimental data are available from the corresponding author (esalinas@wakehealth.edu) upon reasonable request.

Article and author information

Author details

Christopher K Hauser

Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States

Competing interests
No competing interests declared.
Dantong Zhu

Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States

Competing interests
No competing interests declared.
Terrence R Stanford

Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States

Competing interests
No competing interests declared.
Emilio Salinas

Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States

For correspondence
esalinas@wakehealth.edu

Competing interests
Emilio Salinas, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0001-7411-5693

Funding

National Eye Institute (R01EY12389)

Terrence R Stanford

National Science Foundation (Graduate Research Fellowship)

Christopher K Hauser

National Institute of Neurological Disorders and Stroke (Training grant T32NS073553-01)

Christopher K Hauser

National Institute on Drug Abuse (R01DA030750)

Terrence R Stanford
Emilio Salinas

National Eye Institute (R01EY12389-S1)

Terrence R Stanford

National Eye Institute (R01EY021228)

Terrence R Stanford
Emilio Salinas

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Experimental subjects were two adult male rhesus monkeys (Macaca mulatta). All experimental procedures were conducted in accordance with the NIH Guide for the Care and Use of Laboratory Animals, USDA regulations, and the policies set forth by the Institutional Animal Care and Use Committee (IACUC) of Wake Forest School of Medicine under protocols A10-192, A13-088 and A16-192. All surgery was performed under sodium pentobarbital anesthesia, and every effort was made to minimize suffering.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.