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

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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.

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Ignacio Sarria

Department of Neuroscience, The Scripps Research Institute, Jupiter, United States

Competing interests
The authors declare that no competing interests exist.
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.
Yan Cao

Department of Neuroscience, The Scripps Research Institute, Jupiter, United States

Competing interests
The authors declare that no competing interests exist.
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.
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.
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.
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).

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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.