Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns

The neural mechanisms determining the timing of even simple actions, such as when to walk or rest, are largely mysterious. One intriguing, but untested, hypothesis posits a role for ongoing activity fluctuations in neurons of central action selection circuits that drive animal behavior from moment t...

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Main Authors:	Maesani, Andrea, Ramdya, Pavan, Cruchet, Steeve, Gustafson, Kyle, Benton, Richard, Floreano, Dario
Format:	Online
Language:	English
Published:	Public Library of Science 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657918/

id	pubmed-4657918
recordtype	oai_dc
spelling	pubmed-46579182015-12-02 Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns Maesani, Andrea Ramdya, Pavan Cruchet, Steeve Gustafson, Kyle Benton, Richard Floreano, Dario Research Article The neural mechanisms determining the timing of even simple actions, such as when to walk or rest, are largely mysterious. One intriguing, but untested, hypothesis posits a role for ongoing activity fluctuations in neurons of central action selection circuits that drive animal behavior from moment to moment. To examine how fluctuating activity can contribute to action timing, we paired high-resolution measurements of freely walking Drosophila melanogaster with data-driven neural network modeling and dynamical systems analysis. We generated fluctuation-driven network models whose outputs—locomotor bouts—matched those measured from sensory-deprived Drosophila. From these models, we identified those that could also reproduce a second, unrelated dataset: the complex time-course of odor-evoked walking for genetically diverse Drosophila strains. Dynamical models that best reproduced both Drosophila basal and odor-evoked locomotor patterns exhibited specific characteristics. First, ongoing fluctuations were required. In a stochastic resonance-like manner, these fluctuations allowed neural activity to escape stable equilibria and to exceed a threshold for locomotion. Second, odor-induced shifts of equilibria in these models caused a depression in locomotor frequency following olfactory stimulation. Our models predict that activity fluctuations in action selection circuits cause behavioral output to more closely match sensory drive and may therefore enhance navigation in complex sensory environments. Together these data reveal how simple neural dynamics, when coupled with activity fluctuations, can give rise to complex patterns of animal behavior. Public Library of Science 2015-11-23 /pmc/articles/PMC4657918/ /pubmed/26600381 http://dx.doi.org/10.1371/journal.pcbi.1004577 Text en © 2015 Maesani et al http://creativecommons.org/licenses/by/4.0/ 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 author and source are properly credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Maesani, Andrea Ramdya, Pavan Cruchet, Steeve Gustafson, Kyle Benton, Richard Floreano, Dario
spellingShingle	Maesani, Andrea Ramdya, Pavan Cruchet, Steeve Gustafson, Kyle Benton, Richard Floreano, Dario Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns
author_facet	Maesani, Andrea Ramdya, Pavan Cruchet, Steeve Gustafson, Kyle Benton, Richard Floreano, Dario
author_sort	Maesani, Andrea
title	Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns
title_short	Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns
title_full	Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns
title_fullStr	Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns
title_full_unstemmed	Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns
title_sort	fluctuation-driven neural dynamics reproduce drosophila locomotor patterns
description	The neural mechanisms determining the timing of even simple actions, such as when to walk or rest, are largely mysterious. One intriguing, but untested, hypothesis posits a role for ongoing activity fluctuations in neurons of central action selection circuits that drive animal behavior from moment to moment. To examine how fluctuating activity can contribute to action timing, we paired high-resolution measurements of freely walking Drosophila melanogaster with data-driven neural network modeling and dynamical systems analysis. We generated fluctuation-driven network models whose outputs—locomotor bouts—matched those measured from sensory-deprived Drosophila. From these models, we identified those that could also reproduce a second, unrelated dataset: the complex time-course of odor-evoked walking for genetically diverse Drosophila strains. Dynamical models that best reproduced both Drosophila basal and odor-evoked locomotor patterns exhibited specific characteristics. First, ongoing fluctuations were required. In a stochastic resonance-like manner, these fluctuations allowed neural activity to escape stable equilibria and to exceed a threshold for locomotion. Second, odor-induced shifts of equilibria in these models caused a depression in locomotor frequency following olfactory stimulation. Our models predict that activity fluctuations in action selection circuits cause behavioral output to more closely match sensory drive and may therefore enhance navigation in complex sensory environments. Together these data reveal how simple neural dynamics, when coupled with activity fluctuations, can give rise to complex patterns of animal behavior.
publisher	Public Library of Science
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657918/
_version_	1613505383146455040

Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns

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