title: Fluctuation-Driven Neural Dynamics Reproduce Drosophila Locomotor Patterns.
abstract: 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.
authors.affiliation: Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
authors.forename: Andrea
authors.initials: A
authors.lastname: Maesani
authors.affiliation: Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.|Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
authors.forename: Pavan
authors.initials: P
authors.lastname: Ramdya
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
authors.forename: Steeve
authors.initials: S
authors.lastname: Cruchet
authors.affiliation: The Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
authors.forename: Kyle
authors.initials: K
authors.lastname: Gustafson
authors.affiliation: Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
authors.forename: Richard
authors.initials: R
authors.lastname: Benton
authors.affiliation: Institute of Microengineering, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
authors.forename: Dario
authors.initials: D
authors.lastname: Floreano
mesh_terms: D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D016000:Cluster Analysis; D019295:Computational Biology; D004331:Drosophila melanogaster / Q000502:physiology; D008124:Locomotion / Q000502:physiology*; D008959:Models, Neurological; D009474:Neurons / Q000502:physiology*; D055696:Olfactory Perception / Q000502:physiology