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Neural circuit basis of aversive odour processing in Drosophila from sensory input to descending output

View ORCID ProfilePaavo Huoviala, View ORCID ProfileMichael-John Dolan, View ORCID ProfileFiona M. Love, Philip Myers, View ORCID ProfileShahar Frechter, Shigehiro Namiki, Lovisa Pettersson, Ruairí J.V. Roberts, Robert Turnbull, View ORCID ProfileZane Mitrevica, Patrick Breads, View ORCID ProfilePhilipp Schlegel, View ORCID ProfileAlexander Shakeel Bates, Tiago Rodrigues, View ORCID ProfileYoshinori Aso, Davi Bock, View ORCID ProfileGerald M. Rubin, View ORCID ProfileMarcus Stensmyr, Gwyneth Card, View ORCID ProfileMarta Costa, View ORCID ProfileGregory S.X.E. Jefferis
doi: https://doi.org/10.1101/394403
Paavo Huoviala
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Michael-John Dolan
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Fiona M. Love
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Philip Myers
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
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Shahar Frechter
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
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Shigehiro Namiki
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Lovisa Pettersson
4Department of Biology, Lund University, 22100 Lund, Sweden
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Ruairí J.V. Roberts
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Robert Turnbull
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Zane Mitrevica
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Patrick Breads
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Philipp Schlegel
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Alexander Shakeel Bates
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
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Tiago Rodrigues
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
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Yoshinori Aso
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Davi Bock
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Gerald M. Rubin
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Marcus Stensmyr
4Department of Biology, Lund University, 22100 Lund, Sweden
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Gwyneth Card
3Janelia Research Campus, Howard Hughes Medical Institute, USA
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Marta Costa
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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Gregory S.X.E. Jefferis
1MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
2Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ UK
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  • For correspondence: jefferis@mrc-lmb.cam.ac.uk
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Abstract

Evolution has shaped nervous systems to produce stereotyped behavioural responses to ethologically relevant stimuli. For example when laying eggs, female Drosophila avoid geosmin, an odorant produced by toxic moulds. Here we identify second, third, and fourth order neurons required for this innate olfactory aversion. Connectomics data place these neurons in a complete synaptic circuit from sensory input to descending output. We find multiple levels of valence-specific convergence, including a novel form of axo-axonic input onto second order neurons conveying another danger signal, the pheromone of parasitoid wasps. However, we also observe extensive divergence: second order geosmin neurons connect with a diverse array of 80 third order cell types. We find a pattern of convergence of aversive odour channels at this level. Crossing one more synaptic layer, we identified descending neurons critical for egg-laying aversion. Our data suggest a transition from a labelled line organisation in the periphery to a highly distributed central brain representation that is then coupled to distinct descending pathways.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Additional data on 3rd and 4th order targets.

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 4.0 International license.
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Posted November 04, 2020.
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Neural circuit basis of aversive odour processing in Drosophila from sensory input to descending output
Paavo Huoviala, Michael-John Dolan, Fiona M. Love, Philip Myers, Shahar Frechter, Shigehiro Namiki, Lovisa Pettersson, Ruairí J.V. Roberts, Robert Turnbull, Zane Mitrevica, Patrick Breads, Philipp Schlegel, Alexander Shakeel Bates, Tiago Rodrigues, Yoshinori Aso, Davi Bock, Gerald M. Rubin, Marcus Stensmyr, Gwyneth Card, Marta Costa, Gregory S.X.E. Jefferis
bioRxiv 394403; doi: https://doi.org/10.1101/394403
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Neural circuit basis of aversive odour processing in Drosophila from sensory input to descending output
Paavo Huoviala, Michael-John Dolan, Fiona M. Love, Philip Myers, Shahar Frechter, Shigehiro Namiki, Lovisa Pettersson, Ruairí J.V. Roberts, Robert Turnbull, Zane Mitrevica, Patrick Breads, Philipp Schlegel, Alexander Shakeel Bates, Tiago Rodrigues, Yoshinori Aso, Davi Bock, Gerald M. Rubin, Marcus Stensmyr, Gwyneth Card, Marta Costa, Gregory S.X.E. Jefferis
bioRxiv 394403; doi: https://doi.org/10.1101/394403

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