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Optimized connectome architecture for sensory-motor integration

The intricate connectivity patterns of neural circuits support a wide repertoire of communication processes and functional interactions. Here we systematically investigate how neural signaling is constrained by anatomical connectivity in the mesoscale Drosophila (fruit fly) brain network. We use a s...

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Detalles Bibliográficos
Autores principales: Worrell, Jacob C., Rumschlag, Jeffrey, Betzel, Richard F., Sporns, Olaf, Mišić, Bratislav
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6063718/
https://www.ncbi.nlm.nih.gov/pubmed/30090872
http://dx.doi.org/10.1162/NETN_a_00022
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author Worrell, Jacob C.
Rumschlag, Jeffrey
Betzel, Richard F.
Sporns, Olaf
Mišić, Bratislav
author_facet Worrell, Jacob C.
Rumschlag, Jeffrey
Betzel, Richard F.
Sporns, Olaf
Mišić, Bratislav
author_sort Worrell, Jacob C.
collection PubMed
description The intricate connectivity patterns of neural circuits support a wide repertoire of communication processes and functional interactions. Here we systematically investigate how neural signaling is constrained by anatomical connectivity in the mesoscale Drosophila (fruit fly) brain network. We use a spreading model that describes how local perturbations, such as external stimuli, trigger global signaling cascades that spread through the network. Through a series of simple biological scenarios we demonstrate that anatomical embedding potentiates sensory-motor integration. We find that signal spreading is faster from nodes associated with sensory transduction (sensors) to nodes associated with motor output (effectors). Signal propagation was accelerated if sensor nodes were activated simultaneously, suggesting a topologically mediated synergy among sensors. In addition, the organization of the network increases the likelihood of convergence of multiple cascades towards effector nodes, thereby facilitating integration prior to motor output. Moreover, effector nodes tend to coactivate more frequently than other pairs of nodes, suggesting an anatomically enhanced coordination of motor output. Altogether, our results show that the organization of the mesoscale Drosophila connectome imparts privileged, behaviorally relevant communication patterns among sensors and effectors, shaping their capacity to collectively integrate information.
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spelling pubmed-60637182018-08-06 Optimized connectome architecture for sensory-motor integration Worrell, Jacob C. Rumschlag, Jeffrey Betzel, Richard F. Sporns, Olaf Mišić, Bratislav Netw Neurosci Research The intricate connectivity patterns of neural circuits support a wide repertoire of communication processes and functional interactions. Here we systematically investigate how neural signaling is constrained by anatomical connectivity in the mesoscale Drosophila (fruit fly) brain network. We use a spreading model that describes how local perturbations, such as external stimuli, trigger global signaling cascades that spread through the network. Through a series of simple biological scenarios we demonstrate that anatomical embedding potentiates sensory-motor integration. We find that signal spreading is faster from nodes associated with sensory transduction (sensors) to nodes associated with motor output (effectors). Signal propagation was accelerated if sensor nodes were activated simultaneously, suggesting a topologically mediated synergy among sensors. In addition, the organization of the network increases the likelihood of convergence of multiple cascades towards effector nodes, thereby facilitating integration prior to motor output. Moreover, effector nodes tend to coactivate more frequently than other pairs of nodes, suggesting an anatomically enhanced coordination of motor output. Altogether, our results show that the organization of the mesoscale Drosophila connectome imparts privileged, behaviorally relevant communication patterns among sensors and effectors, shaping their capacity to collectively integrate information. MIT Press 2017-12-01 /pmc/articles/PMC6063718/ /pubmed/30090872 http://dx.doi.org/10.1162/NETN_a_00022 Text en © 2017 Massachusetts Institute of Technology http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Worrell, Jacob C.
Rumschlag, Jeffrey
Betzel, Richard F.
Sporns, Olaf
Mišić, Bratislav
Optimized connectome architecture for sensory-motor integration
title Optimized connectome architecture for sensory-motor integration
title_full Optimized connectome architecture for sensory-motor integration
title_fullStr Optimized connectome architecture for sensory-motor integration
title_full_unstemmed Optimized connectome architecture for sensory-motor integration
title_short Optimized connectome architecture for sensory-motor integration
title_sort optimized connectome architecture for sensory-motor integration
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6063718/
https://www.ncbi.nlm.nih.gov/pubmed/30090872
http://dx.doi.org/10.1162/NETN_a_00022
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