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).

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.

Metrics

  • 2,965
    views
  • 386
    downloads
  • 37
    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. 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

Share this article

https://doi.org/10.7554/eLife.73081

Further reading

    1. Immunology and Inflammation
    2. Neuroscience
    Jeremy M Shea, Saul A Villeda
    Research Article

    During aging, microglia – the resident macrophages of the brain – exhibit altered phenotypes and contribute to age-related neuroinflammation. While numerous hallmarks of age-related microglia have been elucidated, the progression from homeostasis to dysfunction during the aging process remains unresolved. To bridge this gap in knowledge, we undertook complementary cellular and molecular analyses of microglia in the mouse hippocampus across the adult lifespan and in the experimental aging model of heterochronic parabiosis. Single-cell RNA-Seq and pseudotime analysis revealed age-related transcriptional heterogeneity in hippocampal microglia and identified intermediate states of microglial aging that also emerge following heterochronic parabiosis. We tested the functionality of intermediate stress response states via TGFβ1 and translational states using pharmacological approaches in vitro to reveal their modulation of the progression to an activated state. Furthermore, we utilized single-cell RNA-Seq in conjunction with in vivo adult microglia-specific Tgfb1 conditional genetic knockout mouse models to demonstrate that microglia advancement through intermediate aging states drives transcriptional inflammatory activation and hippocampal-dependent cognitive decline.

    1. Neuroscience
    William Hockeimer, Ruo-Yah Lai ... James J Knierim
    Research Article

    The hippocampus is believed to encode episodic memory by binding information about the content of experience within a spatiotemporal framework encoding the location and temporal context of that experience. Previous work implies a distinction between positional inputs to the hippocampus from upstream brain regions that provide information about an animal’s location and nonpositional inputs which provide information about the content of experience, both sensory and navigational. Here, we leverage the phenomenon of ‘place field repetition’ to better understand the functional dissociation between positional and nonpositional information encoded in CA1. Rats navigated freely on a novel maze consisting of linear segments arranged in a rectilinear, city-block configuration, which combined elements of open-field foraging and linear-track tasks. Unlike typical results in open-field foraging, place fields were directionally tuned on the maze, even though the animal’s behavior was not constrained to extended, one-dimensional (1D) trajectories. Repeating fields from the same cell tended to have the same directional preference when the fields were aligned along a linear corridor of the maze, but they showed uncorrelated directional preferences when they were unaligned across different corridors. Lastly, individual fields displayed complex time dynamics which resulted in the population activity changing gradually over the course of minutes. These temporal dynamics were evident across repeating fields of the same cell. These results demonstrate that the positional inputs that drive a cell to fire in similar locations across the maze can be behaviorally and temporally dissociated from the nonpositional inputs that alter the firing rates of the cell within its place fields, offering a potential mechanism to increase the flexibility of the system to encode episodic variables within a spatiotemporal framework provided by place cells.