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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Main Authors: Jacob C. Worrell, Jeffrey Rumschlag, Richard F. Betzel, Olaf Sporns, Bratislav Mišić
Format: Article
Language:English
Published: The MIT Press 2017-12-01
Series:Network Neuroscience
Subjects:
Online Access:https://www.mitpressjournals.org/doi/pdf/10.1162/NETN_a_00022
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spelling doaj-470d8baa6086433da286b025079eab552020-11-24T22:47:24ZengThe MIT PressNetwork Neuroscience2472-17512017-12-011441543010.1162/NETN_a_00022NETN_a_00022Optimized connectome architecture for sensory-motor integrationJacob C. Worrell0Jeffrey Rumschlag1Richard F. Betzel2Olaf Sporns3Bratislav Mišić4Department of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana, USADepartment of Cell Biology and Neuroscience, University of California Riverside, Riverside, CA, USADepartment of Bioengineering, University of Pennsylvania, Philadelphia, PA, USADepartment of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana, USAMontréal Neurological Institute, McGill University, Montréal, CanadaThe 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. The complex network spanned by neurons and their axonal projections promotes a diverse set of functions. In the present report, we study how the topological organization of the fruit fly brain supports sensory-motor integration. Using a simple communication model, we demonstrate that the topology of this network allows efficient coordination among sensory and motor neurons. Our results suggest that brain network organization may profoundly shape the functional repertoire of this simple organism.https://www.mitpressjournals.org/doi/pdf/10.1162/NETN_a_00022ConnectomeBrainSpreadingDrosophila
collection DOAJ
language English
format Article
sources DOAJ
author Jacob C. Worrell
Jeffrey Rumschlag
Richard F. Betzel
Olaf Sporns
Bratislav Mišić
spellingShingle Jacob C. Worrell
Jeffrey Rumschlag
Richard F. Betzel
Olaf Sporns
Bratislav Mišić
Optimized connectome architecture for sensory-motor integration
Network Neuroscience
Connectome
Brain
Spreading
Drosophila
author_facet Jacob C. Worrell
Jeffrey Rumschlag
Richard F. Betzel
Olaf Sporns
Bratislav Mišić
author_sort Jacob C. Worrell
title Optimized connectome architecture for sensory-motor integration
title_short 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_sort optimized connectome architecture for sensory-motor integration
publisher The MIT Press
series Network Neuroscience
issn 2472-1751
publishDate 2017-12-01
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. The complex network spanned by neurons and their axonal projections promotes a diverse set of functions. In the present report, we study how the topological organization of the fruit fly brain supports sensory-motor integration. Using a simple communication model, we demonstrate that the topology of this network allows efficient coordination among sensory and motor neurons. Our results suggest that brain network organization may profoundly shape the functional repertoire of this simple organism.
topic Connectome
Brain
Spreading
Drosophila
url https://www.mitpressjournals.org/doi/pdf/10.1162/NETN_a_00022
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