Visual and motor signatures of locomotion dynamically shape apopulation code for feature detection in Drosophila

Abstract

Natural vision is dynamic: as an animal moves, its visual input changes dramatically. How can the visual system reliably extract local features from an input dominated by self-generated signals? In Drosophila, diverse local visual features are represented by a group of projection neurons with distinct tuning properties. Here we describe a connectome-based volumetric imaging strategy to measure visually evoked neural activity across this population. We show that local visual features are jointly represented across the population, and that a shared gain factor improves trial-to-trial coding fidelity. A subset of these neurons, tuned to small objects, is modulated by two independent signals associated with self-movement, a motor-related signal and a visual motion signal associated with rotation of the animal. These two inputs adjust the sensitivity of these feature detectors across the locomotor cycle, selectively reducing their gain during saccades and restoring it during intersaccadic intervals. This work reveals a strategy for reliable feature detection during locomotion.

Data availability

All software and code is available on GitHub. Main analysis, modeling and figure generation code can be found here: https://github.com/mhturner/glom_pop; Visual stimulus code can be found here: https://github.com/ClandininLab/visanalysis and here: https://github.com/ClandininLab/flystim. Extracted ROI responses and associated stimulus metadata, along with raw imaging data, can be found in a Dryad repository here: https://doi.org/10.5061/dryad.h44j0zpp8.

The following data sets were generated

Article and author information

Author details

  1. Maxwell H Turner

    Department of Neurobiology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4164-9995
  2. Avery Krieger

    Department of Neurobiology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Michelle M Pang

    Department of Neurobiology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Thomas R Clandinin

    Department of Neurobiology, Stanford University, Stanford, United States
    For correspondence
    trc@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6277-6849

Funding

National Institutes of Health (F32-MH118707)

  • Maxwell H Turner

National Institutes of Health (K99-EY032549)

  • Maxwell H Turner

National Institutes of Health (R01-EY022638)

  • Thomas R Clandinin

National Institutes of Health (R01NS110060)

  • Thomas R Clandinin

National Science Foundation (GRFP)

  • Avery Krieger

National Defense Science and Engineering Graduate (Fellowship)

  • Michelle M Pang

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

Copyright

© 2022, Turner 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

  • 2,304
    views
  • 264
    downloads
  • 25
    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. Maxwell H Turner
  2. Avery Krieger
  3. Michelle M Pang
  4. Thomas R Clandinin
(2022)
Visual and motor signatures of locomotion dynamically shape apopulation code for feature detection in Drosophila
eLife 11:e82587.
https://doi.org/10.7554/eLife.82587

Share this article

https://doi.org/10.7554/eLife.82587

Further reading

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.