Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

  1. Jennifer Ding
  2. Albert Chen
  3. Janet Chung
  4. Hector Acaron Ledesma
  5. Mofei Wu
  6. David M Berson
  7. Stephanie E Palmer  Is a corresponding author
  8. Wei Wei  Is a corresponding author
  1. The University of Chicago, United States
  2. Harvard University, United States
  3. Brown University, United States

Abstract

Spatially distributed excitation and inhibition collectively shape a visual neuron's receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the role of strong null-direction inhibition of On-Off direction-selective ganglion cells (On-Off DSGCs) on their direction selectivity is well-studied. However, how excitatory inputs influence the On-Off DSGC's visual response is underexplored. Here, we report that On-Off DSGCs have a spatially displaced glutamatergic receptive field along their horizontal preferred-null motion axes. This displaced receptive field contributes to DSGC null-direction spiking during interrupted motion trajectories. Theoretical analyses indicate that population responses during interrupted motion may help populations of On-Off DSGCs signal the spatial location of moving objects in complex, naturalistic visual environments. Our study highlights that the direction-selective circuit exploits separate sets of mechanisms under different stimulus conditions, and these mechanisms may help encode multiple visual features.

Data availability

Data available on Dryad Digital Repository (doi:10.5061/dryad.vq83bk3s8). Source data files have been provided for all main text and supplemental figures.

The following data sets were generated

Article and author information

Author details

  1. Jennifer Ding

    Committee on Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2282-6615
  2. Albert Chen

    Biophysics Graduate Program, Harvard University, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9306-8703
  3. Janet Chung

    Department of Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  4. Hector Acaron Ledesma

    Graduate Program in Biophysical Sciences, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  5. Mofei Wu

    Department of Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  6. David M Berson

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    No competing interests declared.
  7. Stephanie E Palmer

    Organismal Biology and Anatomy, The University of Chicago, Chicago, United States
    For correspondence
    sepalmer@uchicago.edu
    Competing interests
    Stephanie E Palmer, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6211-6293
  8. Wei Wei

    Department of Neurobiology, The University of Chicago, Chicago, United States
    For correspondence
    weiw@uchicago.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7771-5974

Funding

NIH (R01 NS109990)

  • Wei Wei

McKnight Endowment Fund for Neuroscience (McKnight Scholarship Award)

  • Wei Wei

NSF (GRFP DGE-1746045)

  • Jennifer Ding

NIH (F31 EY029156)

  • Hector Acaron Ledesma

NSF (Career Award 1652617)

  • Stephanie E Palmer

Physics of Biological Function (PHY-1734030)

  • Stephanie E Palmer

NIH (RO1 EY012793)

  • David M Berson

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

Ethics

Animal experimentation: All procedures regarding the use of mice were in accordance with the University of Chicago Institutional Animal Care and Use Committee (IACUC) (ACUP protocol 72247) and with the NIH Guide for the Care and Use of Laboratory Animals and the Public Health Service Policy.

Copyright

© 2021, Ding 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

  • 1,139
    views
  • 191
    downloads
  • 4
    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. Jennifer Ding
  2. Albert Chen
  3. Janet Chung
  4. Hector Acaron Ledesma
  5. Mofei Wu
  6. David M Berson
  7. Stephanie E Palmer
  8. Wei Wei
(2021)
Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit
eLife 10:e68181.
https://doi.org/10.7554/eLife.68181

Share this article

https://doi.org/10.7554/eLife.68181

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Tanya Wolff, Mark Eddison ... Gerald M Rubin
    Research Article

    The central complex (CX) plays a key role in many higher-order functions of the insect brain including navigation and activity regulation. Genetic tools for manipulating individual cell types, and knowledge of what neurotransmitters and neuromodulators they express, will be required to gain mechanistic understanding of how these functions are implemented. We generated and characterized split-GAL4 driver lines that express in individual or small subsets of about half of CX cell types. We surveyed neuropeptide and neuropeptide receptor expression in the central brain using fluorescent in situ hybridization. About half of the neuropeptides we examined were expressed in only a few cells, while the rest were expressed in dozens to hundreds of cells. Neuropeptide receptors were expressed more broadly and at lower levels. Using our GAL4 drivers to mark individual cell types, we found that 51 of the 85 CX cell types we examined expressed at least one neuropeptide and 21 expressed multiple neuropeptides. Surprisingly, all co-expressed a small molecule neurotransmitter. Finally, we used our driver lines to identify CX cell types whose activation affects sleep, and identified other central brain cell types that link the circadian clock to the CX. The well-characterized genetic tools and information on neuropeptide and neurotransmitter expression we provide should enhance studies of the CX.

    1. Neuroscience
    François Osiurak, Giovanni Federico ... Mathieu Lesourd
    Research Article

    Our propensity to materiality, which consists in using, making, creating, and passing on technologies, has enabled us to shape the physical world according to our ends. To explain this proclivity, scientists have calibrated their lens to either low-level skills such as motor cognition or high-level skills such as language or social cognition. Yet, little has been said about the intermediate-level cognitive processes that are directly involved in mastering this materiality, that is, technical cognition. We aim to focus on this intermediate level for providing new insights into the neurocognitive bases of human materiality. Here, we show that a technical-reasoning process might be specifically at work in physical problem-solving situations. We found via two distinct neuroimaging studies that the area PF (parietal F) within the left parietal lobe is central for this reasoning process in both tool-use and non-tool-use physical problem-solving and can work along with social-cognitive skills to resolve day-to-day interactions that combine social and physical constraints. Our results demonstrate the existence of a specific cognitive module in the human brain dedicated to materiality, which might be the supporting pillar allowing the accumulation of technical knowledge over generations. Intensifying research on technical cognition could nurture a comprehensive framework that has been missing in fields interested in how early and modern humans have been interacting with the physical world through technology, and how this interaction has shaped our history and culture.