Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.

In the vertebrate retina, horizontal cells generate the inhibitory surround of bipolar cells, an essential step in contrast enhancement. For the last decades, the mechanism involved in this inhibitory synaptic pathway has been a major controversy in retinal research. One hypothesis suggests that con...

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Autores principales:	Lauw J Klaassen, Ziyi Sun, Marvin N Steijaert, Petra Bolte, Iris Fahrenfort, Trijntje Sjoerdsma, Jan Klooster, Yvonne Claassen, Colleen R Shields, Huub M M Ten Eikelder, Ulrike Janssen-Bienhold, Georg Zoidl, Douglas G McMahon, Maarten Kamermans
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/656bfa6183a64e378dc273b850820c43
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spelling	oai:doaj.org-article:656bfa6183a64e378dc273b850820c432021-11-18T05:36:06ZSynaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.1544-91731545-788510.1371/journal.pbio.1001107https://doaj.org/article/656bfa6183a64e378dc273b850820c432011-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21811399/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885In the vertebrate retina, horizontal cells generate the inhibitory surround of bipolar cells, an essential step in contrast enhancement. For the last decades, the mechanism involved in this inhibitory synaptic pathway has been a major controversy in retinal research. One hypothesis suggests that connexin hemichannels mediate this negative feedback signal; another suggests that feedback is mediated by protons. Mutant zebrafish were generated that lack connexin 55.5 hemichannels in horizontal cells. Whole cell voltage clamp recordings were made from isolated horizontal cells and cones in flat mount retinas. Light-induced feedback from horizontal cells to cones was reduced in mutants. A reduction of feedback was also found when horizontal cells were pharmacologically hyperpolarized but was absent when they were pharmacologically depolarized. Hemichannel currents in isolated horizontal cells showed a similar behavior. The hyperpolarization-induced hemichannel current was strongly reduced in the mutants while the depolarization-induced hemichannel current was not. Intracellular recordings were made from horizontal cells. Consistent with impaired feedback in the mutant, spectral opponent responses in horizontal cells were diminished in these animals. A behavioral assay revealed a lower contrast-sensitivity, illustrating the role of the horizontal cell to cone feedback pathway in contrast enhancement. Model simulations showed that the observed modifications of feedback can be accounted for by an ephaptic mechanism. A model for feedback, in which the number of connexin hemichannels is reduced to about 40%, fully predicts the specific asymmetric modification of feedback. To our knowledge, this is the first successful genetic interference in the feedback pathway from horizontal cells to cones. It provides direct evidence for an unconventional role of connexin hemichannels in the inhibitory synapse between horizontal cells and cones. This is an important step in resolving a long-standing debate about the unusual form of (ephaptic) synaptic transmission between horizontal cells and cones in the vertebrate retina.Lauw J KlaassenZiyi SunMarvin N SteijaertPetra BolteIris FahrenfortTrijntje SjoerdsmaJan KloosterYvonne ClaassenColleen R ShieldsHuub M M Ten EikelderUlrike Janssen-BienholdGeorg ZoidlDouglas G McMahonMaarten KamermansPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 9, Iss 7, p e1001107 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Lauw J Klaassen Ziyi Sun Marvin N Steijaert Petra Bolte Iris Fahrenfort Trijntje Sjoerdsma Jan Klooster Yvonne Claassen Colleen R Shields Huub M M Ten Eikelder Ulrike Janssen-Bienhold Georg Zoidl Douglas G McMahon Maarten Kamermans Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
description	In the vertebrate retina, horizontal cells generate the inhibitory surround of bipolar cells, an essential step in contrast enhancement. For the last decades, the mechanism involved in this inhibitory synaptic pathway has been a major controversy in retinal research. One hypothesis suggests that connexin hemichannels mediate this negative feedback signal; another suggests that feedback is mediated by protons. Mutant zebrafish were generated that lack connexin 55.5 hemichannels in horizontal cells. Whole cell voltage clamp recordings were made from isolated horizontal cells and cones in flat mount retinas. Light-induced feedback from horizontal cells to cones was reduced in mutants. A reduction of feedback was also found when horizontal cells were pharmacologically hyperpolarized but was absent when they were pharmacologically depolarized. Hemichannel currents in isolated horizontal cells showed a similar behavior. The hyperpolarization-induced hemichannel current was strongly reduced in the mutants while the depolarization-induced hemichannel current was not. Intracellular recordings were made from horizontal cells. Consistent with impaired feedback in the mutant, spectral opponent responses in horizontal cells were diminished in these animals. A behavioral assay revealed a lower contrast-sensitivity, illustrating the role of the horizontal cell to cone feedback pathway in contrast enhancement. Model simulations showed that the observed modifications of feedback can be accounted for by an ephaptic mechanism. A model for feedback, in which the number of connexin hemichannels is reduced to about 40%, fully predicts the specific asymmetric modification of feedback. To our knowledge, this is the first successful genetic interference in the feedback pathway from horizontal cells to cones. It provides direct evidence for an unconventional role of connexin hemichannels in the inhibitory synapse between horizontal cells and cones. This is an important step in resolving a long-standing debate about the unusual form of (ephaptic) synaptic transmission between horizontal cells and cones in the vertebrate retina.
format	article
author	Lauw J Klaassen Ziyi Sun Marvin N Steijaert Petra Bolte Iris Fahrenfort Trijntje Sjoerdsma Jan Klooster Yvonne Claassen Colleen R Shields Huub M M Ten Eikelder Ulrike Janssen-Bienhold Georg Zoidl Douglas G McMahon Maarten Kamermans
author_facet	Lauw J Klaassen Ziyi Sun Marvin N Steijaert Petra Bolte Iris Fahrenfort Trijntje Sjoerdsma Jan Klooster Yvonne Claassen Colleen R Shields Huub M M Ten Eikelder Ulrike Janssen-Bienhold Georg Zoidl Douglas G McMahon Maarten Kamermans
author_sort	Lauw J Klaassen
title	Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
title_short	Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
title_full	Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
title_fullStr	Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
title_full_unstemmed	Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
title_sort	synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/656bfa6183a64e378dc273b850820c43
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Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels.

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