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Shared generative rules of locomotor behavior in arthropods and vertebrates

Alex Gomez-Marin, Efrat Oron, Anna Gakamsky, Dan Valente, Yoav Benjamini, Ilan Golani
doi: https://doi.org/10.1101/031716
Alex Gomez-Marin
1Champalimaud Neuroscience Programme, Lisbon, Portugal
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  • For correspondence: agomezmarin@gmail.com ilan99@tau.ac.il
Efrat Oron
2Department of Zoology, Faculty of Life Sciences and Sagol School of Neuroscience, Tel Aviv University, Israel
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Anna Gakamsky
2Department of Zoology, Faculty of Life Sciences and Sagol School of Neuroscience, Tel Aviv University, Israel
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Dan Valente
3Cold Spring Harbor laboratory, USA
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Yoav Benjamini
4Department of Statistics and Sagol School of Neuroscience, Tel Aviv University
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Ilan Golani
2Department of Zoology, Faculty of Life Sciences and Sagol School of Neuroscience, Tel Aviv University, Israel
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  • For correspondence: agomezmarin@gmail.com ilan99@tau.ac.il
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Abstract

The discovery of shared behavioral processes across phyla is an essential step in the establishment of a comparative study of behavior. We use immobility as an origin and reference for the measurement of locomotor behavior; speed, direction of walking and direction of facing as the three degrees of freedom shaping fly locomotor behavior; and cocaine as the parameter inducing a progressive transition in and out of immobility. In this way we expose and quantify the generative rules that shape part of fruit fly locomotor behavior, bringing about a gradual buildup of freedom during the transition from immobility to normal behavior and a precisely opposite narrowing down during the transition into immobility. During buildup the fly exhibits enhancement and then reduction to normal values of movement along each degree of freedom: first, body rotation in the horizontal plane, then path curvature and then speed of translation. Transition into immobility unfolds by narrowing down of the repertoire in the opposite sequential order, showing reciprocal relations during both buildup and narrowing down. The same generative rules apply to vertebrate locomotor behavior in a variety of contexts involving transition out and into immobility. Recent claims for deep homology between the arthropod central complex and the vertebrate basal ganglia provide an opportunity to examine whether the generative rules we discovered also share common descent. Neurochemical processes mediating the buildup of locomotor behavior in vertebrates could guide the search for equivalent processes in arthropods. The measurement methodology we use prompts the discovery of candidate behavioral homologies.

Significance Statement Do flies and mice share the same behavior? By defining immobility as an intrinsic reference point for locomotor behavior we show that the rules that generate the transition from immobility to full blown normal behavior, and from full blown behavior to immobility are shared by fruit flies and mice. These rules constitute a much desired aim of evolutionary biology: the discovery of behavioral homologies across distant phyla. The methodology we use facilitates the discovery of cross-phyletic behavioral homologies, shedding light on the problem of the evolution of behavior.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 14, 2015.
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Shared generative rules of locomotor behavior in arthropods and vertebrates
Alex Gomez-Marin, Efrat Oron, Anna Gakamsky, Dan Valente, Yoav Benjamini, Ilan Golani
bioRxiv 031716; doi: https://doi.org/10.1101/031716
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Shared generative rules of locomotor behavior in arthropods and vertebrates
Alex Gomez-Marin, Efrat Oron, Anna Gakamsky, Dan Valente, Yoav Benjamini, Ilan Golani
bioRxiv 031716; doi: https://doi.org/10.1101/031716

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