1. Neuroscience
Download icon

Circadian regulation of vertebrate cone photoreceptor function

Research Article
  • Cited 0
  • Views 638
  • Annotations
Cite this article as: eLife 2021;10:e68903 doi: 10.7554/eLife.68903

Abstract

Eukaryotes generally display a circadian rhythm as an adaption to the reoccurring day/night cycle. This is particularly true for visual physiology that is directly affected by changing light conditions. Here we investigate the influence of the circadian rhythm on the expression and function of visual transduction cascade regulators in diurnal zebrafish and nocturnal mice. We focused on regulators of shut-off kinetics such as recoverins, arrestins, opsin kinases, and GTPase-accelerating protein that have direct effects on temporal vision. Transcript as well as protein levels of most analyzed genes show a robust circadian rhythm dependent regulation, which correlates with changes in photoresponse kinetics. Electroretinography demonstrates that photoresponse recovery in zebrafish is delayed in the evening and accelerated in the morning. This physiological rhythmicity is mirrored in visual behaviors, such as optokinetic and optomotor responses. Functional rhythmicity persists in continuous darkness, it is reversed by an inverted light cycle and disrupted by constant light. This is in line with our finding that orthologous gene transcripts from diurnal zebrafish and nocturnal mice are often expressed in an anti-phasic daily rhythm.

Data availability

All data generated and analysed during this study are included in the manuscript and supporting files. The dataset has been uploaded to dryad at http://dx.doi.org/10.5061/dryad.0cfxpnw26

The following data sets were generated

Article and author information

Author details

  1. Jingjing Zang

    Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Matthias Gesemann

    Molecular Life Sciences and Neuroscience Center Zurich, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7635-1235
  3. Jennifer Keim

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Marijana Samardzija

    Lab for Retinal Cell Biology, Department of Ophthalmology, University of Zurich, Schlieren, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Christian Grimm

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9318-4352
  6. Stephan CF Neuhauss

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    For correspondence
    stephan.neuhauss@mls.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9615-480X

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030_200376)

  • Marijana Samardzija

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 animal experiments were carried out in the line with the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research and were approved by the Veterinary Authorities of Kanton Zurich, Switzerland (TV4206)

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Publication history

  1. Received: March 30, 2021
  2. Preprint posted: May 7, 2021 (view preprint)
  3. Accepted: September 20, 2021
  4. Accepted Manuscript published: September 22, 2021 (version 1)
  5. Version of Record published: October 6, 2021 (version 2)

Copyright

© 2021, Zang 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

  • 638
    Page views
  • 163
    Downloads
  • 0
    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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Zhengchao Xu et al.
    Tools and Resources Updated

    The dorsal raphe nucleus (DR) and median raphe nucleus (MR) contain populations of glutamatergic and GABAergic neurons that regulate diverse behavioral functions. However, their whole-brain input-output circuits remain incompletely elucidated. We used viral tracing combined with fluorescence micro-optical sectioning tomography to generate a comprehensive whole-brain atlas of inputs and outputs of glutamatergic and GABAergic neurons in the DR and MR. We found that these neurons received inputs from similar upstream brain regions. The glutamatergic and GABAergic neurons in the same raphe nucleus had divergent projection patterns with differences in critical brain regions. Specifically, MR glutamatergic neurons projected to the lateral habenula through multiple pathways. Correlation and cluster analysis revealed that glutamatergic and GABAergic neurons in the same raphe nucleus received heterogeneous inputs and sent different collateral projections. This connectivity atlas further elucidates the anatomical architecture of the raphe nuclei, which could facilitate better understanding of their behavioral functions.

    1. Neuroscience
    Shankar Ramachandran et al.
    Research Article Updated

    Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here, we show that the Caenorhabditis elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.