Sensitivity and kinetics of signal transmission at the first visual synapse differentially impact visually-guided behavior

  1. Ignacio Sarria
  2. Johan Pahlberg
  3. Yan Cao
  4. Alexander V Kolesnikov
  5. Vladimir J Kefalov
  6. Alapakkam P Sampath
  7. Kirill A Martemyanov  Is a corresponding author
  1. The Scripps Research Institute, United States
  2. University of California, Los Angeles, United States
  3. Washington University in St.Louis, United States

Abstract

In the retina, synaptic transmission between photoreceptors and downstream ON-bipolar neurons (ON-BCs) is mediated by a GPCR pathway, which plays an essential role in vision. However, the mechanisms that control signal transmission at this synapse and its relevance to behavior remain poorly understood. In this study we used a genetic system to titrate the rate of GPCR signaling in ON-BC dendrites by varying the concentration of key RGS proteins and measuring the impact on transmission of signal between photoreceptors and ON-BC neurons using electroretinography and single cell recordings. We found that sensitivity, onset timing, and the maximal amplitude of light-evoked responses in rod- and cone-driven ON-BCs are determined by different RGS concentrations. We further show that changes in RGS concentration differentially impact visually guided-behavior mediated by rod and cone ON pathways. These findings illustrate that neuronal circuit properties can be modulated by adjusting parameters of GPCR-based neurotransmission at individual synapses.

Article and author information

Author details

  1. Ignacio Sarria

    Department of Neuroscience, The Scripps Research Institute, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Johan Pahlberg

    Jules Stein Eye Institute, Department of Ophthalmology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yan Cao

    Department of Neuroscience, The Scripps Research Institute, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexander V Kolesnikov

    Department of Ophthalmology and Visual Sciences, Washington University in St.Louis, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Vladimir J Kefalov

    Department of Ophthalmology and Visual Sciences, Washington University in St.Louis, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alapakkam P Sampath

    Jules Stein Eye Institute, Department of Ophthalmology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Kirill A Martemyanov

    Department of Neuroscience, The Scripps Research Institute, Jupiter, United States
    For correspondence
    kirill@scripps.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Jeremy Nathans, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, United States

Ethics

Animal experimentation: All procedures were carried out in accordance with the National Institute of Health guidelines and were granted formal approval by the Institutional Animal Care and Use Committees of the Scripps Research Institute (IACUC protocol number 14-001), Washington University (IACUC protocol number 20140236), and the University of Southern California (IACUC protocol number 10890).

Version history

  1. Received: January 6, 2015
  2. Accepted: April 11, 2015
  3. Accepted Manuscript published: April 16, 2015 (version 1)
  4. Version of Record published: April 29, 2015 (version 2)

Copyright

© 2015, Sarria 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

  • 1,451
    views
  • 297
    downloads
  • 15
    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. Ignacio Sarria
  2. Johan Pahlberg
  3. Yan Cao
  4. Alexander V Kolesnikov
  5. Vladimir J Kefalov
  6. Alapakkam P Sampath
  7. Kirill A Martemyanov
(2015)
Sensitivity and kinetics of signal transmission at the first visual synapse differentially impact visually-guided behavior
eLife 4:e06358.
https://doi.org/10.7554/eLife.06358

Share this article

https://doi.org/10.7554/eLife.06358

Further reading

    1. Neuroscience
    Ivan Tomić, Paul M Bays
    Research Article

    Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.

    1. Neuroscience
    Emilio Salinas, Bashirul I Sheikh
    Insight

    Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.