Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.

Determining the fundamental architectural design of complex nervous systems will lead to significant medical and technological advances. Yet it remains unclear how nervous systems evolved highly efficient networks with near optimal sharing of pathways that yet produce multiple distinct behaviors to...

Full description

Bibliographic Details
Main Authors: Seongkyun Kim, Hyoungkyu Kim, Jerald D Kralik, Jaeseung Jeong
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-08-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4991803?pdf=render
id doaj-f592e3aff58b4818b0e5e897c1f6e8c7
record_format Article
spelling doaj-f592e3aff58b4818b0e5e897c1f6e8c72020-11-24T21:49:06ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582016-08-01128e100508410.1371/journal.pcbi.1005084Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.Seongkyun KimHyoungkyu KimJerald D KralikJaeseung JeongDetermining the fundamental architectural design of complex nervous systems will lead to significant medical and technological advances. Yet it remains unclear how nervous systems evolved highly efficient networks with near optimal sharing of pathways that yet produce multiple distinct behaviors to reach the organism's goals. To determine this, the nematode roundworm Caenorhabditis elegans is an attractive model system. Progress has been made in delineating the behavioral circuits of the C. elegans, however, many details are unclear, including the specific functions of every neuron and synapse, as well as the extent the behavioral circuits are separate and parallel versus integrative and serial. Network analysis provides a normative approach to help specify the network design. We investigated the vulnerability of the Caenorhabditis elegans connectome by performing computational experiments that (a) "attacked" 279 individual neurons and 2,990 weighted synaptic connections (composed of 6,393 chemical synapses and 890 electrical junctions) and (b) quantified the effects of each removal on global network properties that influence information processing. The analysis identified 12 critical neurons and 29 critical synapses for establishing fundamental network properties. These critical constituents were found to be control elements-i.e., those with the most influence over multiple underlying pathways. Additionally, the critical synapses formed into circuit-level pathways. These emergent pathways provide evidence for (a) the importance of backward locomotion, avoidance behavior, and social feeding behavior to the organism; (b) the potential roles of specific neurons whose functions have been unclear; andhttp://europepmc.org/articles/PMC4991803?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Seongkyun Kim
Hyoungkyu Kim
Jerald D Kralik
Jaeseung Jeong
spellingShingle Seongkyun Kim
Hyoungkyu Kim
Jerald D Kralik
Jaeseung Jeong
Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.
PLoS Computational Biology
author_facet Seongkyun Kim
Hyoungkyu Kim
Jerald D Kralik
Jaeseung Jeong
author_sort Seongkyun Kim
title Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.
title_short Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.
title_full Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.
title_fullStr Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.
title_full_unstemmed Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.
title_sort vulnerability-based critical neurons, synapses, and pathways in the caenorhabditis elegans connectome.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2016-08-01
description Determining the fundamental architectural design of complex nervous systems will lead to significant medical and technological advances. Yet it remains unclear how nervous systems evolved highly efficient networks with near optimal sharing of pathways that yet produce multiple distinct behaviors to reach the organism's goals. To determine this, the nematode roundworm Caenorhabditis elegans is an attractive model system. Progress has been made in delineating the behavioral circuits of the C. elegans, however, many details are unclear, including the specific functions of every neuron and synapse, as well as the extent the behavioral circuits are separate and parallel versus integrative and serial. Network analysis provides a normative approach to help specify the network design. We investigated the vulnerability of the Caenorhabditis elegans connectome by performing computational experiments that (a) "attacked" 279 individual neurons and 2,990 weighted synaptic connections (composed of 6,393 chemical synapses and 890 electrical junctions) and (b) quantified the effects of each removal on global network properties that influence information processing. The analysis identified 12 critical neurons and 29 critical synapses for establishing fundamental network properties. These critical constituents were found to be control elements-i.e., those with the most influence over multiple underlying pathways. Additionally, the critical synapses formed into circuit-level pathways. These emergent pathways provide evidence for (a) the importance of backward locomotion, avoidance behavior, and social feeding behavior to the organism; (b) the potential roles of specific neurons whose functions have been unclear; and
url http://europepmc.org/articles/PMC4991803?pdf=render
work_keys_str_mv AT seongkyunkim vulnerabilitybasedcriticalneuronssynapsesandpathwaysinthecaenorhabditiselegansconnectome
AT hyoungkyukim vulnerabilitybasedcriticalneuronssynapsesandpathwaysinthecaenorhabditiselegansconnectome
AT jeralddkralik vulnerabilitybasedcriticalneuronssynapsesandpathwaysinthecaenorhabditiselegansconnectome
AT jaeseungjeong vulnerabilitybasedcriticalneuronssynapsesandpathwaysinthecaenorhabditiselegansconnectome
_version_ 1725889565625942016