Mechanisms that allow cortical preparatory activity without inappropriate movement

  1. Timothy R Darlington  Is a corresponding author
  2. Stephen G Lisberger
  1. Duke University School of Medicine, United States

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.

Data availability

Source data have been provided for each figure.

Article and author information

Author details

  1. Timothy R Darlington

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    For correspondence
    trd12@duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5534-7552
  2. Stephen G Lisberger

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7859-4361

Funding

National Institutes of Health (R01-EY027373)

  • Stephen G Lisberger

National Institutes of Health (F30-EY027684)

  • Timothy R Darlington

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

Ethics

Animal experimentation: All procedures received prior approval by Duke's Institutional Animal Care and Use Committee (protocol A085-18-04) and were in compliance with the National Institutes of Health's Guide for the Care and Use of Laboratory Animals.

Copyright

© 2020, Darlington & Lisberger

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.

Metrics

  • 2,117
    views
  • 245
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Timothy R Darlington
  2. Stephen G Lisberger
(2020)
Mechanisms that allow cortical preparatory activity without inappropriate movement
eLife 9:e50962.
https://doi.org/10.7554/eLife.50962

Share this article

https://doi.org/10.7554/eLife.50962

Further reading

    1. Neuroscience
    Paul I Jaffe, Gustavo X Santiago-Reyes ... Russell A Poldrack
    Research Article

    Evidence accumulation models (EAMs) are the dominant framework for modeling response time (RT) data from speeded decision-making tasks. While providing a good quantitative description of RT data in terms of abstract perceptual representations, EAMs do not explain how the visual system extracts these representations in the first place. To address this limitation, we introduce the visual accumulator model (VAM), in which convolutional neural network models of visual processing and traditional EAMs are jointly fitted to trial-level RTs and raw (pixel-space) visual stimuli from individual subjects in a unified Bayesian framework. Models fitted to large-scale cognitive training data from a stylized flanker task captured individual differences in congruency effects, RTs, and accuracy. We find evidence that the selection of task-relevant information occurs through the orthogonalization of relevant and irrelevant representations, demonstrating how our framework can be used to relate visual representations to behavioral outputs. Together, our work provides a probabilistic framework for both constraining neural network models of vision with behavioral data and studying how the visual system extracts representations that guide decisions.

    1. Neuroscience
    Aneri Soni, Michael J Frank
    Research Article

    How and why is working memory (WM) capacity limited? Traditional cognitive accounts focus either on limitations on the number or items that can be stored (slots models), or loss of precision with increasing load (resource models). Here, we show that a neural network model of prefrontal cortex and basal ganglia can learn to reuse the same prefrontal populations to store multiple items, leading to resource-like constraints within a slot-like system, and inducing a trade-off between quantity and precision of information. Such ‘chunking’ strategies are adapted as a function of reinforcement learning and WM task demands, mimicking human performance and normative models. Moreover, adaptive performance requires a dynamic range of dopaminergic signals to adjust striatal gating policies, providing a new interpretation of WM difficulties in patient populations such as Parkinson’s disease, ADHD, and schizophrenia. These simulations also suggest a computational rather than anatomical limit to WM capacity.