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Synaptic polarity of the interneuron circuit controlling C. elegans locomotion

Caenorhabditis elegans is the only animal for which a detailed neural connectivity diagram has been constructed. However, synaptic polarities in this diagram, and thus, circuit functions are largely unknown. Here, we deciphered the likely polarities of seven pre-motor neurons implicated in the contr...

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Autores principales: Rakowski, Franciszek, Srinivasan, Jagan, Sternberg, Paul W., Karbowski, Jan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3788333/
https://www.ncbi.nlm.nih.gov/pubmed/24106473
http://dx.doi.org/10.3389/fncom.2013.00128
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author Rakowski, Franciszek
Srinivasan, Jagan
Sternberg, Paul W.
Karbowski, Jan
author_facet Rakowski, Franciszek
Srinivasan, Jagan
Sternberg, Paul W.
Karbowski, Jan
author_sort Rakowski, Franciszek
collection PubMed
description Caenorhabditis elegans is the only animal for which a detailed neural connectivity diagram has been constructed. However, synaptic polarities in this diagram, and thus, circuit functions are largely unknown. Here, we deciphered the likely polarities of seven pre-motor neurons implicated in the control of worm's locomotion, using a combination of experimental and computational tools. We performed single and multiple laser ablations in the locomotor interneuron circuit and recorded times the worms spent in forward and backward locomotion. We constructed a theoretical model of the locomotor circuit and searched its all possible synaptic polarity combinations and sensory input patterns in order to find the best match to the timing data. The optimal solution is when either all or most of the interneurons are inhibitory and forward interneurons receive the strongest input, which suggests that inhibition governs the dynamics of the locomotor interneuron circuit. From the five pre-motor interneurons, only AVB and AVD are equally likely to be excitatory, i.e., they have probably similar number of inhibitory and excitatory connections to distant targets. The method used here has a general character and thus can be also applied to other neural systems consisting of small functional networks.
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spelling pubmed-37883332013-10-08 Synaptic polarity of the interneuron circuit controlling C. elegans locomotion Rakowski, Franciszek Srinivasan, Jagan Sternberg, Paul W. Karbowski, Jan Front Comput Neurosci Neuroscience Caenorhabditis elegans is the only animal for which a detailed neural connectivity diagram has been constructed. However, synaptic polarities in this diagram, and thus, circuit functions are largely unknown. Here, we deciphered the likely polarities of seven pre-motor neurons implicated in the control of worm's locomotion, using a combination of experimental and computational tools. We performed single and multiple laser ablations in the locomotor interneuron circuit and recorded times the worms spent in forward and backward locomotion. We constructed a theoretical model of the locomotor circuit and searched its all possible synaptic polarity combinations and sensory input patterns in order to find the best match to the timing data. The optimal solution is when either all or most of the interneurons are inhibitory and forward interneurons receive the strongest input, which suggests that inhibition governs the dynamics of the locomotor interneuron circuit. From the five pre-motor interneurons, only AVB and AVD are equally likely to be excitatory, i.e., they have probably similar number of inhibitory and excitatory connections to distant targets. The method used here has a general character and thus can be also applied to other neural systems consisting of small functional networks. Frontiers Media S.A. 2013-10-02 /pmc/articles/PMC3788333/ /pubmed/24106473 http://dx.doi.org/10.3389/fncom.2013.00128 Text en Copyright © 2013 Rakowski, Srinivasan, Sternberg and Karbowski. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Rakowski, Franciszek
Srinivasan, Jagan
Sternberg, Paul W.
Karbowski, Jan
Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
title Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
title_full Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
title_fullStr Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
title_full_unstemmed Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
title_short Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
title_sort synaptic polarity of the interneuron circuit controlling c. elegans locomotion
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3788333/
https://www.ncbi.nlm.nih.gov/pubmed/24106473
http://dx.doi.org/10.3389/fncom.2013.00128
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