1. Neuroscience
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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
Research Article
  • Cited 7
  • Views 1,308
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Cite this article as: eLife 2015;4:e06358 doi: 10.7554/eLife.06358

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.

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).

Reviewing Editor

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

Publication 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.

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Further reading

    1. Neuroscience
    Behrad Noudoost et al.
    Research Article

    Visually guided behavior relies on the integration of sensory input and information held in working memory (WM). Yet it remains unclear how this is accomplished at the level of neural circuits. We studied the direct visual cortical inputs to neurons within a visuomotor area of prefrontal cortex in behaving monkeys. We show that the efficacy of visual input to prefrontal cortex is gated by information held in WM. Surprisingly, visual input to prefrontal neurons was found to target those with both visual and motor properties, rather than preferentially targeting other visual neurons. Furthermore, activity evoked from visual cortex was larger in magnitude, more synchronous, and more rapid, when monkeys remembered locations that matched the location of visual input. These results indicate that WM directly influences the circuitry that transforms visual input into visually guided behavior.

    1. Developmental Biology
    2. Neuroscience
    Jessica Douthit et al.
    Research Article Updated

    As neural circuits form, growing processes select the correct synaptic partners through interactions between cell surface proteins. The presence of such proteins on two neuronal processes may lead to either adhesion or repulsion; however, the consequences of mismatched expression have rarely been explored. Here, we show that the Drosophila CUB-LDL protein Lost and found (Loaf) is required in the UV-sensitive R7 photoreceptor for normal axon targeting only when Loaf is also present in its synaptic partners. Although targeting occurs normally in loaf mutant animals, removing loaf from photoreceptors or expressing it in their postsynaptic neurons Tm5a/b or Dm9 in a loaf mutant causes mistargeting of R7 axons. Loaf localizes primarily to intracellular vesicles including endosomes. We propose that Loaf regulates the trafficking or function of one or more cell surface proteins, and an excess of these proteins on the synaptic partners of R7 prevents the formation of stable connections.