Superior colliculus drives stimulus-evoked directionally biased saccades and attempted head movements in head-fixed mice

  1. Sebastian H Zahler
  2. David E Taylor
  3. Joey Y Wong
  4. Julia M Adams
  5. Evan H Feinberg  Is a corresponding author
  1. University of California, San Francisco, United States

Abstract

Animals investigate their environments by directing their gaze towards salient stimuli. In the prevailing view, mouse gaze shifts entail head rotations followed by brainstem-mediated eye movements, including saccades to reset the eyes. These 'recentering' saccades are attributed to head movement-related vestibular cues. However, microstimulating mouse superior colliculus (SC) elicits directed head and eye movements resembling SC-dependent sensory-guided gaze shifts in other species, suggesting that mouse gaze shifts may be more flexible than has been recognized. We investigated this possibility by tracking eye and attempted head movements in a head-fixed preparation that eliminates head movement-related sensory cues. We found tactile stimuli evoke directionally biased saccades coincident with attempted head rotations. Differences in saccade endpoints across stimuli are associated with distinct stimulus-dependent relationships between initial eye position and saccade direction and amplitude. Optogenetic perturbations revealed SC drives these gaze shifts. Thus, head-fixed mice make sensory-guided, SC-dependent gaze shifts involving coincident, directionally biased saccades and attempted head movements. Our findings uncover flexibility in mouse gaze shifts and provide a foundation for studying head-eye coupling.

Data availability

Annotated data and model code have been uploaded to a Dryad repository (https://doi.org/10.7272/Q6V69GTV).

The following data sets were generated

Article and author information

Author details

  1. Sebastian H Zahler

    Department of Anatomy, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0089-3593
  2. David E Taylor

    Department of Anatomy, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0476-0299
  3. Joey Y Wong

    Department of Anatomy, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3697-8951
  4. Julia M Adams

    Department of Anatomy, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1402-1040
  5. Evan H Feinberg

    Department of Anatomy, University of California, San Francisco, San Francisco, United States
    For correspondence
    evan.feinberg@ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7040-0980

Funding

National Institute of Mental Health (DP2MH119426)

  • Evan H Feinberg

National Institute of Neurological Disorders and Stroke (R01NS109060)

  • Evan H Feinberg

Simons Foundation Autism Research Initiative (574347)

  • Evan H Feinberg

Esther A. and Joseph Klingenstein Fund

  • Evan H Feinberg

E. Matilda Ziegler Foundation for the Blind

  • Evan H Feinberg

Whitehall Foundation

  • Evan H Feinberg

Brain and Behavior Research Foundation (25337)

  • Evan H Feinberg

Brain and Behavior Research Foundation (27320)

  • Evan H Feinberg

Sandler Foundation

  • Evan H Feinberg

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All animal procedures were approved by the University of California San Francisco Institutional Animal Care and Use Committee (IACUC) (protocol number AN176625), and were conducted in agreement with the Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC).

Reviewing Editor

  1. Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany

Publication history

  1. Preprint posted: February 11, 2021 (view preprint)
  2. Received: August 16, 2021
  3. Accepted: December 27, 2021
  4. Accepted Manuscript published: December 31, 2021 (version 1)
  5. Version of Record published: January 10, 2022 (version 2)

Copyright

© 2021, Zahler 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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  1. Sebastian H Zahler
  2. David E Taylor
  3. Joey Y Wong
  4. Julia M Adams
  5. Evan H Feinberg
(2021)
Superior colliculus drives stimulus-evoked directionally biased saccades and attempted head movements in head-fixed mice
eLife 10:e73081.
https://doi.org/10.7554/eLife.73081

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