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Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila

Censi, Andrea and Straw, Andrew D. and Sayaman, Rosalyn W. and Murray, Richard M. and Dickinson, Michael H. (2013) Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila. PLOS Computational Biology, 9 (2). Art. No. e1002891. ISSN 1553-7358. PMCID PMC3585425.

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As animals move through the world in search of resources, they change course in reaction to both external sensory cues and internally-generated programs. Elucidating the functional logic of complex search algorithms is challenging because the observable actions of the animal cannot be unambiguously assigned to externally- or internally-triggered events. We present a technique that addresses this challenge by assessing quantitatively the contribution of external stimuli and internal processes. We apply this technique to the analysis of rapid turns (“saccades”) of freely flying Drosophila melanogaster. We show that a single scalar feature computed from the visual stimulus experienced by the animal is sufficient to explain a majority (93%) of the turning decisions. We automatically estimate this scalar value from the observable trajectory, without any assumption regarding the sensory processing. A posteriori, we show that the estimated feature field is consistent with previous results measured in other experimental conditions. The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior. We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions. Our results suggest that comparatively few saccades in free-flying conditions are a result of an intrinsic spontaneous process, contrary to previous suggestions. We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens.

Item Type:Article
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URLURL TypeDescription CentralArticle material: Figure S1 material: Text S1
Censi, Andrea0000-0001-5162-0398
Straw, Andrew D.0000-0001-8381-0858
Murray, Richard M.0000-0002-5785-7481
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:© 2013 Censi et al. 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 credited. Received: August 2, 2012; Accepted: December 4, 2012; Published: February 28, 2013. This study was funded by AFOSR (FA9550-06-1-0079 and FA9550-10-1-0086), ARO (DAAD 19-03-D-0004), and NSF (NSF-0931746), DARPA (MSEE). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Kit Longden for insightful comments on a preliminary version of this work. Author Contributions: Conceived and designed the experiments: ADS MHD. Performed the experiments: ADS RWS. Analyzed the data: AC ADS. Wrote the paper: AC ADS RMM MHD. The authors declare that no competing interests exist.
Funding AgencyGrant Number
Air Force Office of Scientific Research (AFOSR)FA9550-06-1-0079
Air Force Office of Scientific Research (AFOSR)FA9550-10-1-0086
Army Research Office (ARO)DAAD 19-03-D-0004
Defense Advanced Research Projects Agency (DARPA)UNSPECIFIED
Issue or Number:2
PubMed Central ID:PMC3585425
Record Number:CaltechAUTHORS:20151124-141949989
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Official Citation:Censi A, Straw AD, Sayaman RW, Murray RM, Dickinson MH (2013) Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila. PLoS Comput Biol 9(2): e1002891. doi:10.1371/journal.pcbi.1002891
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:62390
Deposited By: George Porter
Deposited On:24 Nov 2015 22:48
Last Modified:01 Jul 2020 23:29

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