The Multilayer Connectome of Caenorhabditis elegans.

Connectomics has focused primarily on the mapping of synaptic links in the brain; yet it is well established that extrasynaptic volume transmission, especially via monoamines and neuropeptides, is also critical to brain function and occurs primarily outside the synaptic connectome. We have mapped th...

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Main Authors: Barry Bentley, Robyn Branicky, Christopher L Barnes, Yee Lian Chew, Eviatar Yemini, Edward T Bullmore, Petra E Vértes, William R Schafer
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-12-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1005283
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spelling doaj-914c7b420618435ea18e9eacc44181cb2021-04-21T15:43:08ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582016-12-011212e100528310.1371/journal.pcbi.1005283The Multilayer Connectome of Caenorhabditis elegans.Barry BentleyRobyn BranickyChristopher L BarnesYee Lian ChewEviatar YeminiEdward T BullmorePetra E VértesWilliam R SchaferConnectomics has focused primarily on the mapping of synaptic links in the brain; yet it is well established that extrasynaptic volume transmission, especially via monoamines and neuropeptides, is also critical to brain function and occurs primarily outside the synaptic connectome. We have mapped the putative monoamine connections, as well as a subset of neuropeptide connections, in C. elegans based on new and published gene expression data. The monoamine and neuropeptide networks exhibit distinct topological properties, with the monoamine network displaying a highly disassortative star-like structure with a rich-club of interconnected broadcasting hubs, and the neuropeptide network showing a more recurrent, highly clustered topology. Despite the low degree of overlap between the extrasynaptic (or wireless) and synaptic (or wired) connectomes, we find highly significant multilink motifs of interaction, pinpointing locations in the network where aminergic and neuropeptide signalling modulate synaptic activity. Thus, the C. elegans connectome can be mapped as a multiplex network with synaptic, gap junction, and neuromodulator layers representing alternative modes of interaction between neurons. This provides a new topological plan for understanding how aminergic and peptidergic modulation of behaviour is achieved by specific motifs and loci of integration between hard-wired synaptic or junctional circuits and extrasynaptic signals wirelessly broadcast from a small number of modulatory neurons.https://doi.org/10.1371/journal.pcbi.1005283
collection DOAJ
language English
format Article
sources DOAJ
author Barry Bentley
Robyn Branicky
Christopher L Barnes
Yee Lian Chew
Eviatar Yemini
Edward T Bullmore
Petra E Vértes
William R Schafer
spellingShingle Barry Bentley
Robyn Branicky
Christopher L Barnes
Yee Lian Chew
Eviatar Yemini
Edward T Bullmore
Petra E Vértes
William R Schafer
The Multilayer Connectome of Caenorhabditis elegans.
PLoS Computational Biology
author_facet Barry Bentley
Robyn Branicky
Christopher L Barnes
Yee Lian Chew
Eviatar Yemini
Edward T Bullmore
Petra E Vértes
William R Schafer
author_sort Barry Bentley
title The Multilayer Connectome of Caenorhabditis elegans.
title_short The Multilayer Connectome of Caenorhabditis elegans.
title_full The Multilayer Connectome of Caenorhabditis elegans.
title_fullStr The Multilayer Connectome of Caenorhabditis elegans.
title_full_unstemmed The Multilayer Connectome of Caenorhabditis elegans.
title_sort multilayer connectome of caenorhabditis elegans.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2016-12-01
description Connectomics has focused primarily on the mapping of synaptic links in the brain; yet it is well established that extrasynaptic volume transmission, especially via monoamines and neuropeptides, is also critical to brain function and occurs primarily outside the synaptic connectome. We have mapped the putative monoamine connections, as well as a subset of neuropeptide connections, in C. elegans based on new and published gene expression data. The monoamine and neuropeptide networks exhibit distinct topological properties, with the monoamine network displaying a highly disassortative star-like structure with a rich-club of interconnected broadcasting hubs, and the neuropeptide network showing a more recurrent, highly clustered topology. Despite the low degree of overlap between the extrasynaptic (or wireless) and synaptic (or wired) connectomes, we find highly significant multilink motifs of interaction, pinpointing locations in the network where aminergic and neuropeptide signalling modulate synaptic activity. Thus, the C. elegans connectome can be mapped as a multiplex network with synaptic, gap junction, and neuromodulator layers representing alternative modes of interaction between neurons. This provides a new topological plan for understanding how aminergic and peptidergic modulation of behaviour is achieved by specific motifs and loci of integration between hard-wired synaptic or junctional circuits and extrasynaptic signals wirelessly broadcast from a small number of modulatory neurons.
url https://doi.org/10.1371/journal.pcbi.1005283
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