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The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations

Neurons are characterized by elaborate tree-like dendritic structures that support local computations by integrating multiple inputs from upstream presynaptic neurons. It is less clear whether simple neurons, consisting of a few or even a single neurite, may perform local computations as well. To ad...

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Detalles Bibliográficos
Autores principales: Ruach, Rotem, Ratner, Nir, Emmons, Scott W., Zaslaver, Alon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9934027/
https://www.ncbi.nlm.nih.gov/pubmed/36630454
http://dx.doi.org/10.1073/pnas.2201699120
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author Ruach, Rotem
Ratner, Nir
Emmons, Scott W.
Zaslaver, Alon
author_facet Ruach, Rotem
Ratner, Nir
Emmons, Scott W.
Zaslaver, Alon
author_sort Ruach, Rotem
collection PubMed
description Neurons are characterized by elaborate tree-like dendritic structures that support local computations by integrating multiple inputs from upstream presynaptic neurons. It is less clear whether simple neurons, consisting of a few or even a single neurite, may perform local computations as well. To address this question, we focused on the compact neural network of Caenorhabditis elegans animals for which the full wiring diagram is available, including the coordinates of individual synapses. We find that the positions of the chemical synapses along the neurites are not randomly distributed nor can they be explained by anatomical constraints. Instead, synapses tend to form clusters, an organization that supports local compartmentalized computations. In mutually synapsing neurons, connections of opposite polarity cluster separately, suggesting that positive and negative feedback dynamics may be implemented in discrete compartmentalized regions along neurites. In triple-neuron circuits, the nonrandom synaptic organization may facilitate local functional roles, such as signal integration and coordinated activation of functionally related downstream neurons. These clustered synaptic topologies emerge as a guiding principle in the network, presumably to facilitate distinct parallel functions along a single neurite, which effectively increase the computational capacity of the neural network.
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spelling pubmed-99340272023-07-11 The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations Ruach, Rotem Ratner, Nir Emmons, Scott W. Zaslaver, Alon Proc Natl Acad Sci U S A Biological Sciences Neurons are characterized by elaborate tree-like dendritic structures that support local computations by integrating multiple inputs from upstream presynaptic neurons. It is less clear whether simple neurons, consisting of a few or even a single neurite, may perform local computations as well. To address this question, we focused on the compact neural network of Caenorhabditis elegans animals for which the full wiring diagram is available, including the coordinates of individual synapses. We find that the positions of the chemical synapses along the neurites are not randomly distributed nor can they be explained by anatomical constraints. Instead, synapses tend to form clusters, an organization that supports local compartmentalized computations. In mutually synapsing neurons, connections of opposite polarity cluster separately, suggesting that positive and negative feedback dynamics may be implemented in discrete compartmentalized regions along neurites. In triple-neuron circuits, the nonrandom synaptic organization may facilitate local functional roles, such as signal integration and coordinated activation of functionally related downstream neurons. These clustered synaptic topologies emerge as a guiding principle in the network, presumably to facilitate distinct parallel functions along a single neurite, which effectively increase the computational capacity of the neural network. National Academy of Sciences 2023-01-11 2023-01-17 /pmc/articles/PMC9934027/ /pubmed/36630454 http://dx.doi.org/10.1073/pnas.2201699120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Ruach, Rotem
Ratner, Nir
Emmons, Scott W.
Zaslaver, Alon
The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
title The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
title_full The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
title_fullStr The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
title_full_unstemmed The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
title_short The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
title_sort synaptic organization in the caenorhabditis elegans neural network suggests significant local compartmentalized computations
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9934027/
https://www.ncbi.nlm.nih.gov/pubmed/36630454
http://dx.doi.org/10.1073/pnas.2201699120
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