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Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement

View ORCID ProfileYoshinori Aso, View ORCID ProfileDaichi Yamada, View ORCID ProfileDaniel Bushey, View ORCID ProfileKaren Hibbard, View ORCID ProfileMegan Sammons, View ORCID ProfileHideo Otsuna, View ORCID ProfileYichun Shuai, View ORCID ProfileToshihide Hige
doi: https://doi.org/10.1101/2022.12.21.521497
Yoshinori Aso
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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  • For correspondence: asoy@janelia.hhmi.org hige@email.unc.edu
Daichi Yamada
2Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
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Daniel Bushey
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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Karen Hibbard
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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Megan Sammons
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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Hideo Otsuna
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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Yichun Shuai
1Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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Toshihide Hige
2Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
3Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, United States
4Integrative Program for Biological and Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, United States
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  • For correspondence: asoy@janelia.hhmi.org hige@email.unc.edu
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Summary

How memories are used by the brain to guide future action is poorly understood. In olfactory associative learning in Drosophila, multiple compartments of the mushroom body act in parallel to assign valence to a stimulus. Here, we show that appetitive memories stored in different compartments induce different levels of upwind locomotion. Using a photoactivation screen of a new collection of split-GAL4 drivers and EM connectomics, we identified a cluster of neurons postsynaptic to the mushroom body output neurons (MBONs) that can trigger robust upwind steering. These UpWind Neurons (UpWiNs) integrate inhibitory and excitatory synaptic inputs from MBONs of appetitive and aversive memory compartments, respectively. After training, disinhibition from the appetitive-memory MBONs enhances the response of UpWiNs to reward-predicting odors. Blocking UpWiNs impaired appetitive memory and reduced upwind locomotion during retrieval. Photoactivation of UpWiNs also increased the chance of returning to a location where activation was initiated, suggesting an additional role in olfactory navigation. Thus, our results provide insight into how learned abstract valences are gradually transformed into concrete memory-driven actions through divergent and convergent networks, a neuronal architecture that is commonly found in the vertebrate and invertebrate brains.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • To correct tilted figure 1 and figure 1-figure supplement 1

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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 4.0 International license.
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Posted December 24, 2022.
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Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
Yoshinori Aso, Daichi Yamada, Daniel Bushey, Karen Hibbard, Megan Sammons, Hideo Otsuna, Yichun Shuai, Toshihide Hige
bioRxiv 2022.12.21.521497; doi: https://doi.org/10.1101/2022.12.21.521497
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Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
Yoshinori Aso, Daichi Yamada, Daniel Bushey, Karen Hibbard, Megan Sammons, Hideo Otsuna, Yichun Shuai, Toshihide Hige
bioRxiv 2022.12.21.521497; doi: https://doi.org/10.1101/2022.12.21.521497

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