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Gap junctions set the speed and nucleation rate of stage I retinal waves

Spontaneous waves in the developing retina are essential in the formation of the retinotopic mapping in the visual system. From experiments in rabbits, it is known that the earliest type of retinal waves (stage I) is nucleated spontaneously, propagates at a speed of 451±91 μm/sec and relies on gap j...

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Autores principales: Kähne, Malte, Rüdiger, Sten, Kihara, Alexandre Hiroaki, Lindner, Benjamin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6508742/
https://www.ncbi.nlm.nih.gov/pubmed/31034472
http://dx.doi.org/10.1371/journal.pcbi.1006355
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author Kähne, Malte
Rüdiger, Sten
Kihara, Alexandre Hiroaki
Lindner, Benjamin
author_facet Kähne, Malte
Rüdiger, Sten
Kihara, Alexandre Hiroaki
Lindner, Benjamin
author_sort Kähne, Malte
collection PubMed
description Spontaneous waves in the developing retina are essential in the formation of the retinotopic mapping in the visual system. From experiments in rabbits, it is known that the earliest type of retinal waves (stage I) is nucleated spontaneously, propagates at a speed of 451±91 μm/sec and relies on gap junction coupling between ganglion cells. Because gap junctions (electrical synapses) have short integration times, it has been argued that they cannot set the low speed of stage I retinal waves. Here, we present a theoretical study of a two-dimensional neural network of the ganglion cell layer with gap junction coupling and intrinsic noise. We demonstrate that this model can explain observed nucleation rates as well as the comparatively slow propagation speed of the waves. From the interaction between two coupled neurons, we estimate the wave speed in the model network. Furthermore, using simulations of small networks of neurons (N≤260), we estimate the nucleation rate in the form of an Arrhenius escape rate. These results allow for informed simulations of a realistically sized network, yielding values of the gap junction coupling and the intrinsic noise level that are in a physiologically plausible range.
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spelling pubmed-65087422019-05-23 Gap junctions set the speed and nucleation rate of stage I retinal waves Kähne, Malte Rüdiger, Sten Kihara, Alexandre Hiroaki Lindner, Benjamin PLoS Comput Biol Research Article Spontaneous waves in the developing retina are essential in the formation of the retinotopic mapping in the visual system. From experiments in rabbits, it is known that the earliest type of retinal waves (stage I) is nucleated spontaneously, propagates at a speed of 451±91 μm/sec and relies on gap junction coupling between ganglion cells. Because gap junctions (electrical synapses) have short integration times, it has been argued that they cannot set the low speed of stage I retinal waves. Here, we present a theoretical study of a two-dimensional neural network of the ganglion cell layer with gap junction coupling and intrinsic noise. We demonstrate that this model can explain observed nucleation rates as well as the comparatively slow propagation speed of the waves. From the interaction between two coupled neurons, we estimate the wave speed in the model network. Furthermore, using simulations of small networks of neurons (N≤260), we estimate the nucleation rate in the form of an Arrhenius escape rate. These results allow for informed simulations of a realistically sized network, yielding values of the gap junction coupling and the intrinsic noise level that are in a physiologically plausible range. Public Library of Science 2019-04-29 /pmc/articles/PMC6508742/ /pubmed/31034472 http://dx.doi.org/10.1371/journal.pcbi.1006355 Text en © 2019 Kähne et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Kähne, Malte
Rüdiger, Sten
Kihara, Alexandre Hiroaki
Lindner, Benjamin
Gap junctions set the speed and nucleation rate of stage I retinal waves
title Gap junctions set the speed and nucleation rate of stage I retinal waves
title_full Gap junctions set the speed and nucleation rate of stage I retinal waves
title_fullStr Gap junctions set the speed and nucleation rate of stage I retinal waves
title_full_unstemmed Gap junctions set the speed and nucleation rate of stage I retinal waves
title_short Gap junctions set the speed and nucleation rate of stage I retinal waves
title_sort gap junctions set the speed and nucleation rate of stage i retinal waves
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6508742/
https://www.ncbi.nlm.nih.gov/pubmed/31034472
http://dx.doi.org/10.1371/journal.pcbi.1006355
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