Voluntary and involuntary contributions to perceptually guided saccadic choices resolved with millisecond precision

Abstract

In the antisaccade task, which is considered a sensitive assay of cognitive 1 function, a salient visual cue appears and the participant must look away from it. This requires sensory, motor-planning, and cognitive neural mechanisms, but what are their unique contributions to performance, and when exactly are they engaged? Here, by manipulating task urgency, we generate a psychophysical curve that tracks the evolution of the saccadic choice process with millisec ond precision, and resolve the distinct contributions of reflexive (exogenous) and voluntary (endogenous) perceptual mechanisms to antisaccade performance over time. Both progress extremely rapidly, the former driving the eyes toward the cue early on (∼100 ms after cue onset) and the latter directing them away from the cue ∼40 ms later. The behavioral and modeling results provide a detailed, dynamical characterization of attentional and oculomotor capture that is not only qualitatively consistent across participants, but also indicative of their individual perceptual capacities.

Data availability

The psychophysical data are provided in a supplementary data file (Source Data 1). Matlab scripts for running the model are provided in a supplementary source code file (Source code 1).

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7411-5693
  2. Benjamin R Steinberg

    Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  3. Lauren A Sussman

    Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  4. Sophia M Fry

    Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  5. Christopher K Hauser

    Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  6. Denise D Anderson

    Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  7. Terrence R Stanford

    Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.

Funding

National Eye Institute (R01EY025172)

  • Emilio Salinas
  • Terrence R Stanford

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

  • Christopher K Hauser

National Science Foundation (Graduate research fellowship)

  • Christopher K Hauser

Tab Williams Family Endowment

  • Emilio Salinas
  • Terrence R Stanford

National Eye Institute (R01EY021228)

  • Emilio Salinas
  • Terrence R Stanford

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

Ethics

Human subjects: All participants provided informed written consent before the experiment. All experimental procedures were conducted with the approval of the Institutional Review Board (IRB) of Wake Forest School of Medicine.

Reviewing Editor

  1. Daeyeol Lee, Yale School of Medicine, United States

Publication history

  1. Received: February 24, 2019
  2. Accepted: June 20, 2019
  3. Accepted Manuscript published: June 21, 2019 (version 1)
  4. Version of Record published: July 22, 2019 (version 2)

Copyright

© 2019, Salinas 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.

Metrics

  • 1,395
    Page views
  • 231
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Emilio Salinas
  2. Benjamin R Steinberg
  3. Lauren A Sussman
  4. Sophia M Fry
  5. Christopher K Hauser
  6. Denise D Anderson
  7. Terrence R Stanford
(2019)
Voluntary and involuntary contributions to perceptually guided saccadic choices resolved with millisecond precision
eLife 8:e46359.
https://doi.org/10.7554/eLife.46359
  1. Further reading

Further reading

    1. Neuroscience
    Christian H Poth
    Research Advance

    Intelligent behavior requires to act directed by goals despite competing action tendencies triggered by stimuli in the environment. For eye movements, it has recently been discovered that this ability is briefly reduced in urgent situations (Salinas et al., 2019). In a time-window before an urgent response, participants could not help but look at a suddenly appearing visual stimulus, even though their goal was to look away from it. Urgency seemed to provoke a new visual–oculomotor phenomenon: A period in which saccadic eye movements are dominated by external stimuli, and uncontrollable by current goals. This period was assumed to arise from brain mechanisms controlling eye movements and spatial attention, such as those of the frontal eye field. Here, we show that the phenomenon is more general than previously thought. We found that also in well-investigated manual tasks, urgency made goal-conflicting stimulus features dominate behavioral responses. This dominance of behavior followed established trial-to-trial signatures of cognitive control mechanisms that replicate across a variety of tasks. Thus together, these findings reveal that urgency temporarily forces stimulus-driven action by overcoming cognitive control in general, not only at brain mechanisms controlling eye movements.

    1. Developmental Biology
    2. Neuroscience
    Emily L Heckman, Chris Q Doe
    Research Advance Updated

    The organization of neural circuits determines nervous system function. Variability can arise during neural circuit development (e.g. neurite morphology, axon/dendrite position). To ensure robust nervous system function, mechanisms must exist to accommodate variation in neurite positioning during circuit formation. Previously, we developed a model system in the Drosophila ventral nerve cord to conditionally induce positional variability of a proprioceptive sensory axon terminal, and used this model to show that when we altered the presynaptic position of the sensory neuron, its major postsynaptic interneuron partner modified its dendritic arbor to match the presynaptic contact, resulting in functional synaptic input (Sales et al., 2019). Here, we investigate the cellular mechanisms by which the interneuron dendrites detect and match variation in presynaptic partner location and input strength. We manipulate the presynaptic sensory neuron by (a) ablation; (b) silencing or activation; or (c) altering its location in the neuropil. From these experiments we conclude that there are two opposing mechanisms used to establish functional connectivity in the face of presynaptic variability: presynaptic contact stimulates dendrite outgrowth locally, whereas presynaptic activity inhibits postsynaptic dendrite outgrowth globally. These mechanisms are only active during an early larval critical period for structural plasticity. Collectively, our data provide new insights into dendrite development, identifying mechanisms that allow dendrites to flexibly respond to developmental variability in presynaptic location and input strength.