Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets
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
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
© 2018, Hauser et al.
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.
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Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.