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Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons

How is binocular motion information integrated in the bilateral network of wide-field motion-sensitive neurons, called lobula plate tangential cells (LPTCs), in the visual system of flies? It is possible to construct an accurate model of this network because a complete picture of synaptic interactio...

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Autores principales: Suzuki, Yoshinori, Morimoto, Takako, Miyakawa, Hiroyoshi, Aonishi, Toru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3900430/
https://www.ncbi.nlm.nih.gov/pubmed/24465711
http://dx.doi.org/10.1371/journal.pone.0085790
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author Suzuki, Yoshinori
Morimoto, Takako
Miyakawa, Hiroyoshi
Aonishi, Toru
author_facet Suzuki, Yoshinori
Morimoto, Takako
Miyakawa, Hiroyoshi
Aonishi, Toru
author_sort Suzuki, Yoshinori
collection PubMed
description How is binocular motion information integrated in the bilateral network of wide-field motion-sensitive neurons, called lobula plate tangential cells (LPTCs), in the visual system of flies? It is possible to construct an accurate model of this network because a complete picture of synaptic interactions has been experimentally identified. We investigated the cooperative behavior of the network of horizontal LPTCs underlying the integration of binocular motion information and the information representation in the bilateral LPTC network through numerical simulations on the network model. First, we qualitatively reproduced rotational motion-sensitive response of the H2 cell previously reported in vivo experiments and ascertained that it could be accounted for by the cooperative behavior of the bilateral network mainly via interhemispheric electrical coupling. We demonstrated that the response properties of single H1 and Hu cells, unlike H2 cells, are not influenced by motion stimuli in the contralateral visual hemi-field, but that the correlations between these cell activities are enhanced by the rotational motion stimulus. We next examined the whole population activity by performing principal component analysis (PCA) on the population activities of simulated LPTCs. We showed that the two orthogonal patterns of correlated population activities given by the first two principal components represent the rotational and translational motions, respectively, and similar to the H2 cell, rotational motion produces a stronger response in the network than does translational motion. Furthermore, we found that these population-coding properties are strongly influenced by the interhemispheric electrical coupling. Finally, to test the generality of our conclusions, we used a more simplified model and verified that the numerical results are not specific to the network model we constructed.
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spelling pubmed-39004302014-01-24 Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons Suzuki, Yoshinori Morimoto, Takako Miyakawa, Hiroyoshi Aonishi, Toru PLoS One Research Article How is binocular motion information integrated in the bilateral network of wide-field motion-sensitive neurons, called lobula plate tangential cells (LPTCs), in the visual system of flies? It is possible to construct an accurate model of this network because a complete picture of synaptic interactions has been experimentally identified. We investigated the cooperative behavior of the network of horizontal LPTCs underlying the integration of binocular motion information and the information representation in the bilateral LPTC network through numerical simulations on the network model. First, we qualitatively reproduced rotational motion-sensitive response of the H2 cell previously reported in vivo experiments and ascertained that it could be accounted for by the cooperative behavior of the bilateral network mainly via interhemispheric electrical coupling. We demonstrated that the response properties of single H1 and Hu cells, unlike H2 cells, are not influenced by motion stimuli in the contralateral visual hemi-field, but that the correlations between these cell activities are enhanced by the rotational motion stimulus. We next examined the whole population activity by performing principal component analysis (PCA) on the population activities of simulated LPTCs. We showed that the two orthogonal patterns of correlated population activities given by the first two principal components represent the rotational and translational motions, respectively, and similar to the H2 cell, rotational motion produces a stronger response in the network than does translational motion. Furthermore, we found that these population-coding properties are strongly influenced by the interhemispheric electrical coupling. Finally, to test the generality of our conclusions, we used a more simplified model and verified that the numerical results are not specific to the network model we constructed. Public Library of Science 2014-01-23 /pmc/articles/PMC3900430/ /pubmed/24465711 http://dx.doi.org/10.1371/journal.pone.0085790 Text en © 2014 Suzuki 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Suzuki, Yoshinori
Morimoto, Takako
Miyakawa, Hiroyoshi
Aonishi, Toru
Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons
title Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons
title_full Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons
title_fullStr Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons
title_full_unstemmed Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons
title_short Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons
title_sort cooperative integration and representation underlying bilateral network of fly motion-sensitive neurons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3900430/
https://www.ncbi.nlm.nih.gov/pubmed/24465711
http://dx.doi.org/10.1371/journal.pone.0085790
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