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Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adult Drosophila brain

View ORCID ProfileElizabeth C. Marin, View ORCID ProfileRuairí J.V. Roberts, View ORCID ProfileLaurin Büld, View ORCID ProfileMaria Theiss, View ORCID ProfileMarkus W. Pleijzier, View ORCID ProfileTatevik Sarkissian, View ORCID ProfileWillem J. Laursen, View ORCID ProfileRobert Turnbull, View ORCID ProfilePhilipp Schlegel, View ORCID ProfileAlexander S. Bates, View ORCID ProfileFeng Li, View ORCID ProfileMatthias Landgraf, View ORCID ProfileMarta Costa, View ORCID ProfileDavi D. Bock, View ORCID ProfilePaul A. Garrity, View ORCID ProfileGregory S.X.E. Jefferis
doi: https://doi.org/10.1101/2020.01.20.912709
Elizabeth C. Marin
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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  • ORCID record for Elizabeth C. Marin
Ruairí J.V. Roberts
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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  • ORCID record for Ruairí J.V. Roberts
Laurin Büld
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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  • ORCID record for Laurin Büld
Maria Theiss
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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  • ORCID record for Maria Theiss
Markus W. Pleijzier
Division of Neurobiology; MRC Laboratory of Molecular Biology; Cambridge, Cambridgeshire, CB2 0QH; United Kingdom
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  • ORCID record for Markus W. Pleijzier
Tatevik Sarkissian
Department of Biology; Brandeis University; Waltham, MA 02454; USA
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  • ORCID record for Tatevik Sarkissian
Willem J. Laursen
Department of Biology; Brandeis University; Waltham, MA 02454; USA
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  • ORCID record for Willem J. Laursen
Robert Turnbull
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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  • ORCID record for Robert Turnbull
Philipp Schlegel
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United KingdomDivision of Neurobiology; MRC Laboratory of Molecular Biology; Cambridge, Cambridgeshire, CB2 0QH; United Kingdom
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Alexander S. Bates
Division of Neurobiology; MRC Laboratory of Molecular Biology; Cambridge, Cambridgeshire, CB2 0QH; United Kingdom
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Feng Li
Janelia Research Campus; Howard Hughes Medical Institute; Ashburn, VA 20147; USA
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  • ORCID record for Feng Li
Matthias Landgraf
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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Marta Costa
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United Kingdom
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Davi D. Bock
Janelia Research Campus; Howard Hughes Medical Institute; Ashburn, VA 20147; USALarner College of Medicine; University of Vermont; Burlington, VT 05405; USA
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Paul A. Garrity
Department of Biology; Brandeis University; Waltham, MA 02454; USA
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  • ORCID record for Paul A. Garrity
Gregory S.X.E. Jefferis
Department of Zoology; University of Cambridge; Cambridge, CB2 3EJ; United KingdomDivision of Neurobiology; MRC Laboratory of Molecular Biology; Cambridge, Cambridgeshire, CB2 0QH; United Kingdom
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  • For correspondence: jefferis@mrc-lmb.cam.ac.uk
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SUMMARY

Animals exhibit innate and learned preferences for temperature and humidity – conditions critical for their survival and reproduction. Here, we leveraged a whole adult brain electron microscopy volume to study the circuitry associated with antennal thermosensory and hygrosensory neurons, which target specific ventroposterior (VP) glomeruli in the Drosophila melanogaster antennal lobe. We have identified two new VP glomeruli, in addition to the five known ones, and the projection neurons (VP PNs) that relay VP information to higher brain centres, including the mushroom body and lateral horn, seats of learned and innate olfactory behaviours, respectively. Focussing on the mushroom body lateral accessory calyx (lACA), a known thermosensory neuropil, we present a comprehensive connectome by reconstructing neurons downstream of heating- and cooling-responsive VP PNs. We find that a few lACA-associated mushroom body intrinsic neurons (Kenyon cells) solely receive thermosensory inputs, while most receive additional olfactory and thermo- or hygrosensory PN inputs in the main calyx. Unexpectedly, we find several classes of lACA-associated neurons that form a local network with outputs to other brain neuropils, suggesting that the lACA serves as a general hub for thermosensory circuitry. For example, we find DN1 pacemaker neurons that link the lACA to the accessory medulla, likely mediating temperature-based entrainment of the circadian clock. Finally, we survey strongly connected downstream partners of VP PNs across the protocerebrum; these include a descending neuron that receives input mainly from dry-responsive VP PNs, meaning that just two synapses might separate hygrosensory inputs from motor neurons in the nerve cord. (249)

HIGHLIGHTS

  • Two novel thermo/hygrosensory glomeruli in the fly antennal lobe

  • First complete set of thermosensory and hygrosensory projection neurons

  • First connectome for a thermosensory centre, the lateral accessory calyx

  • Novel third order neurons, including a link to the circadian clock

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 4.0 International license.
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Posted January 21, 2020.
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Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adult Drosophila brain
Elizabeth C. Marin, Ruairí J.V. Roberts, Laurin Büld, Maria Theiss, Markus W. Pleijzier, Tatevik Sarkissian, Willem J. Laursen, Robert Turnbull, Philipp Schlegel, Alexander S. Bates, Feng Li, Matthias Landgraf, Marta Costa, Davi D. Bock, Paul A. Garrity, Gregory S.X.E. Jefferis
bioRxiv 2020.01.20.912709; doi: https://doi.org/10.1101/2020.01.20.912709
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Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adult Drosophila brain
Elizabeth C. Marin, Ruairí J.V. Roberts, Laurin Büld, Maria Theiss, Markus W. Pleijzier, Tatevik Sarkissian, Willem J. Laursen, Robert Turnbull, Philipp Schlegel, Alexander S. Bates, Feng Li, Matthias Landgraf, Marta Costa, Davi D. Bock, Paul A. Garrity, Gregory S.X.E. Jefferis
bioRxiv 2020.01.20.912709; doi: https://doi.org/10.1101/2020.01.20.912709

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