Range, routing and kinetics of rod signaling in primate retina

  1. William N Grimes
  2. Jacob Baudin
  3. Anthony W Azevedo
  4. Fred Rieke  Is a corresponding author
  1. University of Washington, United States

Abstract

Stimulus- or context-dependent routing of neural signals through parallel pathways can permit flexible processing of diverse inputs. For example, work in mouse shows that rod photoreceptor signals are routed through several retinal pathways, each specialized for different light levels. This light-level-dependent routing of rod signals has been invoked to explain several human perceptual results, but it has not been tested in primate retina. Here we show, surprisingly, that rod signals traverse the primate retina almost exclusively through a single pathway - the dedicated rod bipolar pathway. Identical experiments in mouse and primate reveal substantial differences in how rod signals traverse the retina. These results require reevaluating human perceptual results in terms of flexible computation within this single pathway. This includes a prominent speeding of rod signals with light level - which we show is inherited directly from the rod photoreceptors themselves rather than from different pathways with distinct kinetics.

Data availability

We have provided source data for the population analysis for all the main figures (as Excel files) and the raw traces from Figure 2 (Figure 2-source data 2 and Figure 2-source data 3).

Article and author information

Author details

  1. William N Grimes

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  2. Jacob Baudin

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  3. Anthony W Azevedo

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  4. Fred Rieke

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    rieke@u.washington.edu
    Competing interests
    Fred Rieke, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1052-2609

Funding

National Institutes of Health

  • Fred Rieke

Howard Hughes Medical Institute

  • Fred Rieke

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

Reviewing Editor

  1. Daeyeol Lee, Yale School of Medicine, United States

Ethics

Animal experimentation: We obtained primate retinas (Macaca fascicularis, Macaca nemestrina and Macaca mulatta of either sex, ages 3-19 years) through the Tissue Distribution Program of the Regional Primate Research Center. All protocols were approved by the Institutional Animal Care and Use Committee at the University of Washington (protocol 4140-01).

Version history

  1. Received: May 11, 2018
  2. Accepted: September 22, 2018
  3. Accepted Manuscript published: October 9, 2018 (version 1)
  4. Version of Record published: November 5, 2018 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 1,856
    views
  • 333
    downloads
  • 38
    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. William N Grimes
  2. Jacob Baudin
  3. Anthony W Azevedo
  4. Fred Rieke
(2018)
Range, routing and kinetics of rod signaling in primate retina
eLife 7:e38281.
https://doi.org/10.7554/eLife.38281

Share this article

https://doi.org/10.7554/eLife.38281

Further reading

    1. Neuroscience
    Anja T Zai, Anna E Stepien ... Richard HR Hahnloser
    Research Article

    Songbirds’ vocal mastery is impressive, but to what extent is it a result of practice? Can they, based on experienced mismatch with a known target, plan the necessary changes to recover the target in a practice-free manner without intermittently singing? In adult zebra finches, we drive the pitch of a song syllable away from its stable (baseline) variant acquired from a tutor, then we withdraw reinforcement and subsequently deprive them of singing experience by muting or deafening. In this deprived state, birds do not recover their baseline song. However, they revert their songs toward the target by about 1 standard deviation of their recent practice, provided the sensory feedback during the latter signaled a pitch mismatch with the target. Thus, targeted vocal plasticity does not require immediate sensory experience, showing that zebra finches are capable of goal-directed vocal planning.

    1. Neuroscience
    Amanda Chu, Nicholas T Gordon ... Michael A McDannald
    Research Article Updated

    Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that – in addition to jumping, and rearing – is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing – all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveals a fear conditioned cue to orchestrate a temporally organized suite of behaviors.