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Neural circuit mechanisms for steering control in walking Drosophila

Aleksandr Rayshubskiy, Stephen L. Holtz, Isabel D’Alessandro, Anna A. Li, Quinn X. Vanderbeck, Isabel S. Haber, Peter W. Gibb, Rachel I. Wilson
doi: https://doi.org/10.1101/2020.04.04.024703
Aleksandr Rayshubskiy
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Stephen L. Holtz
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Isabel D’Alessandro
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Anna A. Li
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Quinn X. Vanderbeck
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Isabel S. Haber
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Peter W. Gibb
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Rachel I. Wilson
1Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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  • For correspondence: rachel_wilson@hms.harvard.edu
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Abstract

Navigation can be directed toward distant targets represented within the brain’s spatial maps; alternatively, navigation can be directed toward objects in the local environment. Here we identify neurons in the Drosophila brain that integrate these two types of navigation drives. These neurons send axonal projections to the ventral nerve cord, and their activity predicts and influences steering during walking. Meanwhile, their dendrites integrate steering signals from the compass in the brain’s spatial memory center, as well as stimulus-directed steering signals from multimodal sensory pathways that bypass the compass. Using a computational model, we show how the specific connectivity of this network can generate steering behavior directed toward internal (remembered) goals, and we show how environmental cues can dynamically alter the balance of stimulus- and memory-directed steering. Our results suggest a framework where motor dynamics emerge from the integration of parallel feedback loops that drive steering toward internal versus external goals.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • In this version of the manuscript we made the following changes: (1) Added a computational model that describes the transformation between compass signals and steering drives (Figure 7). (2) The abstract, introduction, and discussion have been re-written. (3) The order of figures has been modified.

Copyright 
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 July 18, 2020.
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Neural circuit mechanisms for steering control in walking Drosophila
Aleksandr Rayshubskiy, Stephen L. Holtz, Isabel D’Alessandro, Anna A. Li, Quinn X. Vanderbeck, Isabel S. Haber, Peter W. Gibb, Rachel I. Wilson
bioRxiv 2020.04.04.024703; doi: https://doi.org/10.1101/2020.04.04.024703
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Neural circuit mechanisms for steering control in walking Drosophila
Aleksandr Rayshubskiy, Stephen L. Holtz, Isabel D’Alessandro, Anna A. Li, Quinn X. Vanderbeck, Isabel S. Haber, Peter W. Gibb, Rachel I. Wilson
bioRxiv 2020.04.04.024703; doi: https://doi.org/10.1101/2020.04.04.024703

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