The hourglass organization of the Caenorhabditis elegans connectome.

We approach the C. elegans connectome as an information processing network that receives input from about 90 sensory neurons, processes that information through a highly recurrent network of about 80 interneurons, and it produces a coordinated output from about 120 motor neurons that control the nem...

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Main Authors: Kaeser M Sabrin, Yongbin Wei, Martijn Pieter van den Heuvel, Constantine Dovrolis
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-02-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1007526
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spelling doaj-46aa3253bd56491b946552b880cb6f792021-04-21T15:14:07ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582020-02-01162e100752610.1371/journal.pcbi.1007526The hourglass organization of the Caenorhabditis elegans connectome.Kaeser M SabrinYongbin WeiMartijn Pieter van den HeuvelConstantine DovrolisWe approach the C. elegans connectome as an information processing network that receives input from about 90 sensory neurons, processes that information through a highly recurrent network of about 80 interneurons, and it produces a coordinated output from about 120 motor neurons that control the nematode's muscles. We focus on the feedforward flow of information from sensory neurons to motor neurons, and apply a recently developed network analysis framework referred to as the "hourglass effect". The analysis reveals that this feedforward flow traverses a small core ("hourglass waist") that consists of 10-15 interneurons. These are mostly the same interneurons that were previously shown (using a different analytical approach) to constitute the "rich-club" of the C. elegans connectome. This result is robust to the methodology that separates the feedforward from the feedback flow of information. The set of core interneurons remains mostly the same when we consider only chemical synapses or the combination of chemical synapses and gap junctions. The hourglass organization of the connectome suggests that C. elegans has some similarities with encoder-decoder artificial neural networks in which the input is first compressed and integrated in a low-dimensional latent space that encodes the given data in a more efficient manner, followed by a decoding network through which intermediate-level sub-functions are combined in different ways to compute the correlated outputs of the network. The core neurons at the hourglass waist represent the information bottleneck of the system, balancing the representation accuracy and compactness (complexity) of the given sensory information.https://doi.org/10.1371/journal.pcbi.1007526
collection DOAJ
language English
format Article
sources DOAJ
author Kaeser M Sabrin
Yongbin Wei
Martijn Pieter van den Heuvel
Constantine Dovrolis
spellingShingle Kaeser M Sabrin
Yongbin Wei
Martijn Pieter van den Heuvel
Constantine Dovrolis
The hourglass organization of the Caenorhabditis elegans connectome.
PLoS Computational Biology
author_facet Kaeser M Sabrin
Yongbin Wei
Martijn Pieter van den Heuvel
Constantine Dovrolis
author_sort Kaeser M Sabrin
title The hourglass organization of the Caenorhabditis elegans connectome.
title_short The hourglass organization of the Caenorhabditis elegans connectome.
title_full The hourglass organization of the Caenorhabditis elegans connectome.
title_fullStr The hourglass organization of the Caenorhabditis elegans connectome.
title_full_unstemmed The hourglass organization of the Caenorhabditis elegans connectome.
title_sort hourglass organization of the caenorhabditis elegans connectome.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2020-02-01
description We approach the C. elegans connectome as an information processing network that receives input from about 90 sensory neurons, processes that information through a highly recurrent network of about 80 interneurons, and it produces a coordinated output from about 120 motor neurons that control the nematode's muscles. We focus on the feedforward flow of information from sensory neurons to motor neurons, and apply a recently developed network analysis framework referred to as the "hourglass effect". The analysis reveals that this feedforward flow traverses a small core ("hourglass waist") that consists of 10-15 interneurons. These are mostly the same interneurons that were previously shown (using a different analytical approach) to constitute the "rich-club" of the C. elegans connectome. This result is robust to the methodology that separates the feedforward from the feedback flow of information. The set of core interneurons remains mostly the same when we consider only chemical synapses or the combination of chemical synapses and gap junctions. The hourglass organization of the connectome suggests that C. elegans has some similarities with encoder-decoder artificial neural networks in which the input is first compressed and integrated in a low-dimensional latent space that encodes the given data in a more efficient manner, followed by a decoding network through which intermediate-level sub-functions are combined in different ways to compute the correlated outputs of the network. The core neurons at the hourglass waist represent the information bottleneck of the system, balancing the representation accuracy and compactness (complexity) of the given sensory information.
url https://doi.org/10.1371/journal.pcbi.1007526
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