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...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2015-11-01
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| Series: | PLoS Computational Biology |
| Online Access: | http://europepmc.org/articles/PMC4657918?pdf=render |
| _version_ | 1818287576905154560 |
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| author | Andrea Maesani Pavan Ramdya Steeve Cruchet Kyle Gustafson Richard Benton Dario Floreano |
| author_facet | Andrea Maesani Pavan Ramdya Steeve Cruchet Kyle Gustafson Richard Benton Dario Floreano |
| author_sort | Andrea Maesani |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-13T01:42:41Z |
| format | Article |
| id | doaj.art-11b9717fa6c747a680a3aadd9b33af12 |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-12-13T01:42:41Z |
| publishDate | 2015-11-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-11b9717fa6c747a680a3aadd9b33af122022-12-22T00:03:42ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-11-011111e100457710.1371/journal.pcbi.1004577Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns.Andrea MaesaniPavan RamdyaSteeve CruchetKyle GustafsonRichard BentonDario FloreanoThe 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.http://europepmc.org/articles/PMC4657918?pdf=render |
| spellingShingle | Andrea Maesani Pavan Ramdya Steeve Cruchet Kyle Gustafson Richard Benton Dario Floreano Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns. PLoS Computational Biology |
| title | 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_short | Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns. |
| title_sort | fluctuation driven neural dynamics reproduce drosophila locomotor patterns |
| url | http://europepmc.org/articles/PMC4657918?pdf=render |
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