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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2017-12-01
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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 |
work_keys_str_mv |
AT jacobcworrell optimizedconnectomearchitectureforsensorymotorintegration AT jeffreyrumschlag optimizedconnectomearchitectureforsensorymotorintegration AT richardfbetzel optimizedconnectomearchitectureforsensorymotorintegration AT olafsporns optimizedconnectomearchitectureforsensorymotorintegration AT bratislavmisic optimizedconnectomearchitectureforsensorymotorintegration |
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1725681739999739904 |