Cross-synaptic synchrony and transmission of signal and noise across the mouse retina

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Abstract

Cross-synaptic synchrony-correlations in transmitter release across output synapses of a single neuron-is a key determinant of how signal and noise traverse neural circuits. The anatomical connectivity between rod bipolar and A17 amacrine cells in the mammalian retina-specifically that neighboring A17s often receive input from many of the same rod bipolar cells-provides a rare technical opportunity to measure cross-synaptic synchrony under physiological conditions. This approach reveals that synchronization of rod bipolar cell synapses is near perfect in the dark and decreases with increasing light level. Strong synaptic synchronization in the dark minimizes intrinsic synaptic noise and allows rod bipolar cells to faithfully transmit upstream signal and noise to downstream neurons. Desynchronization in steady light lowers the sensitivity of the rod bipolar output to upstream voltage fluctuations. This work reveals how cross-synaptic synchrony shapes retinal responses to physiological light inputs and, more generally, signaling in complex neural networks.

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William N Grimes

Howard Hughes Medical Institute, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.
Mrinalini Hoon

University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.
Kevin L Briggman

National Institute of Neurological Disorders and Stroke, Bethesda, United States

Competing interests
The authors declare that no competing interests exist.
Rachel O Wong

University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.
Fred Rieke

Howard Hughes Medical Institute, University of Washington, Seattle, United States

For correspondence
rieke@u.washington.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: This work was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All procedures followed protocols approved by the Institutional Animal Care and Use Committee (protocol 3030-01) of the University of Washington.

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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.