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Rapid stimulus-driven modulation of slow ocular position drifts

  1. Tatiana Malevich
  2. Antimo Buonocore
  3. Ziad M Hafed  Is a corresponding author
  1. Tuebingen University, Germany
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Cite this article as: eLife 2020;9:e57595 doi: 10.7554/eLife.57595

Abstract

The eyes are never still during maintained gaze fixation. When microsaccades are not occurring, ocular position exhibits continuous slow changes, often referred to as drifts. Unlike microsaccades, drifts remain to be viewed as largely random eye movements. Here we found that ocular position drifts can, instead, be very systematically stimulus-driven, and with very short latencies. We used highly precise eye tracking in three well trained macaque monkeys and found that even fleeting (~8 ms duration) stimulus presentations can robustly trigger transient and stimulus-specific modulations of ocular position drifts, and with only approximately 60 ms latency. Such drift responses are binocular, and they are most effectively elicited with large stimuli of low spatial frequency. Intriguingly, the drift responses exhibit some image pattern selectivity, and they are not explained by convergence responses, pupil constrictions, head movements, or starting eye positions. Ocular position drifts have very rapid access to exogenous visual information.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data for figures will be uploaded upon acceptance.

Article and author information

Author details

  1. Tatiana Malevich

    Werner Reichardt Centre for Integrative Neuroscience, Tuebingen University, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Antimo Buonocore

    Werner Reichardt Centre for Integrative Neuroscience, Tuebingen University, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3917-510X
  3. Ziad M Hafed

    Werner Reichardt Centre for Integrative Neuroscience, Tuebingen University, Tuebingen, Germany
    For correspondence
    ziad.m.hafed@cin.uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9968-119X

Funding

Deutsche Forschungsgemeinschaft (HA6749/2-1)

  • Antimo Buonocore
  • Ziad M Hafed

Deutsche Forschungsgemeinschaft (EXC307)

  • Tatiana Malevich
  • Antimo Buonocore
  • Ziad M Hafed

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

Ethics

Animal experimentation: We tracked eye movements in 3 male rhesus macaque monkeys trained on behavioral eye movement tasks under head-stabilized conditions. The experiments were part of a larger neurophysiological investigation in the laboratory. All procedures and behavioral paradigms were approved (CIN3/13 and CIN4/19G) by ethics committees at the Regierungspräsidium Tübingen, and they complied with European Union directives on animal research.

Reviewing Editor

  1. Emilio Salinas, Wake Forest School of Medicine, United States

Publication history

  1. Received: April 5, 2020
  2. Accepted: August 5, 2020
  3. Accepted Manuscript published: August 6, 2020 (version 1)
  4. Version of Record published: August 21, 2020 (version 2)

Copyright

© 2020, Malevich 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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