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On the adaptive behavior of head-fixed flies navigating in two-dimensional, visual virtual reality

Hannah Haberkern, Melanie A. Basnak, View ORCID ProfileBiafra Ahanonu, David Schauder, Jeremy D. Cohen, Mark Bolstad, Christopher Bruns, View ORCID ProfileVivek Jayaraman
doi: https://doi.org/10.1101/462028
Hannah Haberkern
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
2Department of Zoology, Cambridge University, Cambridge, UK
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Melanie A. Basnak
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
3Universidad de Buenos Aires, Buenos Aires, Argentina
4Harvard Medical School, Boston, MA
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Biafra Ahanonu
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
5Massachusetts Institute of Technology, Cambridge, MA, USA
6Stanford University, Stanford, CA
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David Schauder
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Jeremy D. Cohen
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Mark Bolstad
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Christopher Bruns
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Vivek Jayaraman
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Abstract

A navigating animal’s sensory experience is shaped not just by its surroundings, but by its movements within them, which in turn are influenced by its past experiences. Studying the intertwined roles of sensation, experience and directed action in navigation has been made easier by the development of virtual reality (VR) environments for head-fixed animals, which allow for quantitative measurements of behavior in well-controlled sensory conditions. VR has long featured in studies of Drosophila melanogaster, but these experiments have typically relied on one-dimensional (1D) VR, effectively allowing the fly to change only its heading in a visual scene, and not its position. Here we explore how flies navigate in a two-dimensional (2D) visual VR environment that more closely resembles their experience during free behavior. We show that flies’ interaction with landmarks in 2D environments cannot be automatically derived from their behavior in simpler 1D environments. Using a novel paradigm, we then demonstrate that flies in 2D VR adapt their behavior in a visual environment in response to optogenetically delivered appetitive and aversive stimuli. Much like free-walking flies after encounters with food, head-fixed flies respond to optogenetic activation of sugar-sensing neurons by initiating a local search behavior. Finally, by pairing optogenetic activation of heat-sensing cells to the flies’ presence near visual landmarks of specific shapes, we elicit selective learned avoidance of landmarks associated with aversive “virtual heat”. These head-fixed paradigms set the stage for an interrogation of fly brain circuitry underlying flexible navigation in complex visual environments.

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Posted November 04, 2018.
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On the adaptive behavior of head-fixed flies navigating in two-dimensional, visual virtual reality
Hannah Haberkern, Melanie A. Basnak, Biafra Ahanonu, David Schauder, Jeremy D. Cohen, Mark Bolstad, Christopher Bruns, Vivek Jayaraman
bioRxiv 462028; doi: https://doi.org/10.1101/462028
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On the adaptive behavior of head-fixed flies navigating in two-dimensional, visual virtual reality
Hannah Haberkern, Melanie A. Basnak, Biafra Ahanonu, David Schauder, Jeremy D. Cohen, Mark Bolstad, Christopher Bruns, Vivek Jayaraman
bioRxiv 462028; doi: https://doi.org/10.1101/462028

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