Selectivity to approaching motion in retinal inputs to the dorsal visual pathway

  1. Todd R Appleby
  2. Michael B Manookin  Is a corresponding author
  1. University of Washington, United States

Abstract

A central function of many neural circuits is to rapidly extract salient information from sensory inputs. Detecting approaching motion is an example of a challenging computational task that is important for avoiding threats and navigating through the environment. Here, we report that detection of approaching motion begins at the earliest stages of visual processing in primates. Several ganglion cell types, the retinal output neurons, show selectivity to approaching motion. Synaptic current recordings from these cells further reveal that this preference for approaching motion arises in the interplay between presynaptic excitatory and inhibitory circuit elements. These findings demonstrate how excitatory and inhibitory circuits interact to mediate an ethologically relevant neural function. They further indicate that the elementary computations that detect approaching motion begin early in the visual stream of primates.

Data availability

We have made the population data in the study freely available. Source data files have been provided for Figures 1, 6, and 7.

Article and author information

Author details

  1. Todd R Appleby

    Neuroscience Graduate Program, Department of Ophthalmolgy, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael B Manookin

    Department of Ophthalmology, University of Washington, Seattle, United States
    For correspondence
    manookin@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8116-7619

Funding

National Eye Institute (R01-EY027323)

  • Michael B Manookin

National Eye Institute (R01-EY029247)

  • Michael B Manookin

National Eye Institute (P30-EY001730)

  • Michael B Manookin

National Institutes of Health (P51 OD-010425)

  • Michael B Manookin

Research to Prevent Blindness

  • Michael B Manookin

Alcon Research Institute

  • Michael B Manookin

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

Reviewing Editor

  1. Markus Meister, California Institute of Technology, United States

Ethics

Animal experimentation: All procedures were approved by the University of Washington Institutional Animal Care and Use Committee (IACUC protocol #4277-01).

Version history

  1. Received: August 16, 2019
  2. Accepted: February 18, 2020
  3. Accepted Manuscript published: February 24, 2020 (version 1)
  4. Version of Record published: March 18, 2020 (version 2)

Copyright

© 2020, Appleby & Manookin

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

  • 1,431
    views
  • 222
    downloads
  • 10
    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. Todd R Appleby
  2. Michael B Manookin
(2020)
Selectivity to approaching motion in retinal inputs to the dorsal visual pathway
eLife 9:e51144.
https://doi.org/10.7554/eLife.51144

Share this article

https://doi.org/10.7554/eLife.51144

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Andrea I Luppi, Pedro AM Mediano ... Emmanuel A Stamatakis
    Research Article

    How is the information-processing architecture of the human brain organised, and how does its organisation support consciousness? Here, we combine network science and a rigorous information-theoretic notion of synergy to delineate a ‘synergistic global workspace’, comprising gateway regions that gather synergistic information from specialised modules across the human brain. This information is then integrated within the workspace and widely distributed via broadcaster regions. Through functional MRI analysis, we show that gateway regions of the synergistic workspace correspond to the human brain’s default mode network, whereas broadcasters coincide with the executive control network. We find that loss of consciousness due to general anaesthesia or disorders of consciousness corresponds to diminished ability of the synergistic workspace to integrate information, which is restored upon recovery. Thus, loss of consciousness coincides with a breakdown of information integration within the synergistic workspace of the human brain. This work contributes to conceptual and empirical reconciliation between two prominent scientific theories of consciousness, the Global Neuronal Workspace and Integrated Information Theory, while also advancing our understanding of how the human brain supports consciousness through the synergistic integration of information.

    1. Computational and Systems Biology
    2. Genetics and Genomics
    Ardalan Naseri, Degui Zhi, Shaojie Zhang
    Research Article Updated

    Runs-of-homozygosity (ROH) segments, contiguous homozygous regions in a genome were traditionally linked to families and inbred populations. However, a growing literature suggests that ROHs are ubiquitous in outbred populations. Still, most existing genetic studies of ROH in populations are limited to aggregated ROH content across the genome, which does not offer the resolution for mapping causal loci. This limitation is mainly due to a lack of methods for the efficient identification of shared ROH diplotypes. Here, we present a new method, ROH-DICE (runs-of-homozygous diplotype cluster enumerator), to find large ROH diplotype clusters, sufficiently long ROHs shared by a sufficient number of individuals, in large cohorts. ROH-DICE identified over 1 million ROH diplotypes that span over 100 single nucleotide polymorphisms (SNPs) and are shared by more than 100 UK Biobank participants. Moreover, we found significant associations of clustered ROH diplotypes across the genome with various self-reported diseases, with the strongest associations found between the extended human leukocyte antigen (HLA) region and autoimmune disorders. We found an association between a diplotype covering the homeostatic iron regulator (HFE) gene and hemochromatosis, even though the well-known causal SNP was not directly genotyped or imputed. Using a genome-wide scan, we identified a putative association between carriers of an ROH diplotype in chromosome 4 and an increase in mortality among COVID-19 patients (p-value = 1.82 × 10−11). In summary, our ROH-DICE method, by calling out large ROH diplotypes in a large outbred population, enables further population genetics into the demographic history of large populations. More importantly, our method enables a new genome-wide mapping approach for finding disease-causing loci with multi-marker recessive effects at a population scale.