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.

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).

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

  • 1,925
    views
  • 339
    downloads
  • 43
    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
    Johannes Oppermann, Andrey Rozenberg ... Peter Hegemann
    Tools and Resources

    Channelrhodopsins (ChRs) are light-gated ion channels widely used to optically activate or silence selected electrogenic cells, such as individual brain neurons. Here, we describe identifying and characterizing a set of anion-conducting ChRs (ACRs) from diverse taxa and representing various branches of the ChR phylogenetic tree. The Mantoniella squamata ACR (MsACR1) showed high sensitivity to yellow-green light (λmax at 555 nm) and was further engineered for optogenetic applications. A single amino-acid substitution that mimicked red-light-sensitive rhodopsins like Chrimson shifted the photosensitivity 20 nm toward red light and accelerated photocurrent kinetics. Hence, it was named red and accelerated ACR, raACR. Both wild-type and mutant are capable optical silencers at low light intensities in mouse neurons in vitro and in vivo, while raACR offers a higher temporal resolution.

    1. Neuroscience
    Ilya A Rybak, Natalia A Shevtsova ... Alain Frigon
    Research Article

    Locomotion in mammals is directly controlled by the spinal neuronal network, operating under the control of supraspinal signals and somatosensory feedback that interact with each other. However, the functional architecture of the spinal locomotor network, its operation regimes, and the role of supraspinal and sensory feedback in different locomotor behaviors, including at different speeds, remain unclear. We developed a computational model of spinal locomotor circuits receiving supraspinal drives and limb sensory feedback that could reproduce multiple experimental data obtained in intact and spinal-transected cats during tied-belt and split-belt treadmill locomotion. We provide evidence that the spinal locomotor network operates in different regimes depending on locomotor speed. In an intact system, at slow speeds (<0.4 m/s), the spinal network operates in a non-oscillating state-machine regime and requires sensory feedback or external inputs for phase transitions. Removing sensory feedback related to limb extension prevents locomotor oscillations at slow speeds. With increasing speed and supraspinal drives, the spinal network switches to a flexor-driven oscillatory regime and then to a classical half-center regime. Following spinal transection, the model predicts that the spinal network can only operate in the state-machine regime. Our results suggest that the spinal network operates in different regimes for slow exploratory and fast escape locomotor behaviors, making use of different control mechanisms.