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.

Ethics

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

Reviewing Editor

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

Publication 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

  • 1,283
    Page views
  • 205
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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

Further reading

    1. Computational and Systems Biology
    Felix Proulx-Giraldeau, Jan M Skotheim, Paul François
    Research Article

    Cell size is controlled to be within a specific range to support physiological function. To control their size, cells use diverse mechanisms ranging from ‘sizers’, in which differences in cell size are compensated for in a single cell division cycle, to ‘adders’, in which a constant amount of cell growth occurs in each cell cycle. This diversity raises the question why a particular cell would implement one rather than another mechanism? To address this question, we performed a series of simulations evolving cell size control networks. The size control mechanism that evolved was influenced by both cell cycle structure and specific selection pressures. Moreover, evolved networks recapitulated known size control properties of naturally occurring networks. If the mechanism is based on a G1 size control and an S/G2/M timer, as found for budding yeast and some human cells, adders likely evolve. But, if the G1 phase is significantly longer than the S/G2/M phase, as is often the case in mammalian cells in vivo, sizers become more likely. Sizers also evolve when the cell cycle structure is inverted so that G1 is a timer, while S/G2/M performs size control, as is the case for the fission yeast S. pombe. For some size control networks, cell size consistently decreases in each cycle until a burst of cell cycle inhibitor drives an extended G1 phase much like the cell division cycle of the green algae Chlamydomonas. That these size control networks evolved such self-organized criticality shows how the evolution of complex systems can drive the emergence of critical processes.

    1. Computational and Systems Biology
    2. Neuroscience
    Kiri Choi, Won Kyu Kim, Changbong Hyeon
    Research Article

    The projection neurons (PNs), reconstructed from electron microscope (EM) images of the Drosophila olfactory system, offer a detailed view of neuronal anatomy, providing glimpses into information flow in the brain. About 150 uPNs constituting 58 glomeruli in the antennal lobe (AL) are bundled together in the axonal extension, routing the olfactory signal received at AL to mushroom body (MB) calyx and lateral horn (LH). Here we quantify the neuronal organization in terms of the inter-PN distances and examine its relationship with the odor types sensed by Drosophila. The homotypic uPNs that constitute glomeruli are tightly bundled and stereotyped in position throughout the neuropils, even though the glomerular PN organization in AL is no longer sustained in the higher brain center. Instead, odor-type dependent clusters consisting of multiple homotypes innervate the MB calyx and LH. Pheromone-encoding and hygro/thermo-sensing homotypes are spatially segregated in MB calyx, whereas two distinct clusters of food-related homotypes are found in LH in addition to the segregation of pheromone-encoding and hygro/thermo-sensing homotypes. We find that there are statistically significant associations between the spatial organization among a group of homotypic uPNs and certain stereotyped olfactory responses. Additionally, the signals from some of the tightly bundled homotypes converge to a specific group of lateral horn neurons (LHNs), which indicates that homotype (or odor type) specific integration of signals occurs at the synaptic interface between PNs and LHNs. Our findings suggest that before neural computation in the inner brain, some of the olfactory information are already encoded in the spatial organization of uPNs, illuminating that a certain degree of labeled-line strategy is at work in the Drosophila olfactory system.