The connectome of the adult Drosophila mushroom body provides insights into function

Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently complete...

Full description

Bibliographic Details
Main Authors: Feng Li, Jack W Lindsey, Elizabeth C Marin, Nils Otto, Marisa Dreher, Georgia Dempsey, Ildiko Stark, Alexander S Bates, Markus William Pleijzier, Philipp Schlegel, Aljoscha Nern, Shin-ya Takemura, Nils Eckstein, Tansy Yang, Audrey Francis, Amalia Braun, Ruchi Parekh, Marta Costa, Louis K Scheffer, Yoshinori Aso, Gregory SXE Jefferis, Larry F Abbott, Ashok Litwin-Kumar, Scott Waddell, Gerald M Rubin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/62576
_version_ 1811181024053297152
author Feng Li
Jack W Lindsey
Elizabeth C Marin
Nils Otto
Marisa Dreher
Georgia Dempsey
Ildiko Stark
Alexander S Bates
Markus William Pleijzier
Philipp Schlegel
Aljoscha Nern
Shin-ya Takemura
Nils Eckstein
Tansy Yang
Audrey Francis
Amalia Braun
Ruchi Parekh
Marta Costa
Louis K Scheffer
Yoshinori Aso
Gregory SXE Jefferis
Larry F Abbott
Ashok Litwin-Kumar
Scott Waddell
Gerald M Rubin
author_facet Feng Li
Jack W Lindsey
Elizabeth C Marin
Nils Otto
Marisa Dreher
Georgia Dempsey
Ildiko Stark
Alexander S Bates
Markus William Pleijzier
Philipp Schlegel
Aljoscha Nern
Shin-ya Takemura
Nils Eckstein
Tansy Yang
Audrey Francis
Amalia Braun
Ruchi Parekh
Marta Costa
Louis K Scheffer
Yoshinori Aso
Gregory SXE Jefferis
Larry F Abbott
Ashok Litwin-Kumar
Scott Waddell
Gerald M Rubin
author_sort Feng Li
collection DOAJ
description Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory, and activity regulation. Here, we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.
first_indexed 2024-04-11T09:11:23Z
format Article
id doaj.art-38a0d0540def4718b12444ab842bda3c
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T09:11:23Z
publishDate 2020-12-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-38a0d0540def4718b12444ab842bda3c2022-12-22T04:32:29ZengeLife Sciences Publications LtdeLife2050-084X2020-12-01910.7554/eLife.62576The connectome of the adult Drosophila mushroom body provides insights into functionFeng Li0https://orcid.org/0000-0002-6658-9175Jack W Lindsey1https://orcid.org/0000-0003-0930-7327Elizabeth C Marin2https://orcid.org/0000-0001-6333-0072Nils Otto3https://orcid.org/0000-0001-9713-4088Marisa Dreher4https://orcid.org/0000-0002-0041-9229Georgia Dempsey5https://orcid.org/0000-0002-1854-8336Ildiko Stark6Alexander S Bates7https://orcid.org/0000-0002-1195-0445Markus William Pleijzier8https://orcid.org/0000-0002-7297-4547Philipp Schlegel9https://orcid.org/0000-0002-5633-1314Aljoscha Nern10https://orcid.org/0000-0002-3822-489XShin-ya Takemura11https://orcid.org/0000-0003-2400-6426Nils Eckstein12Tansy Yang13https://orcid.org/0000-0003-1131-0410Audrey Francis14https://orcid.org/0000-0003-1974-7174Amalia Braun15Ruchi Parekh16https://orcid.org/0000-0002-8060-2807Marta Costa17https://orcid.org/0000-0001-5948-3092Louis K Scheffer18https://orcid.org/0000-0002-3289-6564Yoshinori Aso19https://orcid.org/0000-0002-2939-1688Gregory SXE Jefferis20https://orcid.org/0000-0002-0587-9355Larry F Abbott21Ashok Litwin-Kumar22https://orcid.org/0000-0003-2422-6576Scott Waddell23https://orcid.org/0000-0003-4503-6229Gerald M Rubin24https://orcid.org/0000-0001-8762-8703Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDepartment of Neuroscience, Columbia University, Zuckerman Institute, New York, United StatesDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United KingdomDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom; Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United KingdomJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United KingdomDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United KingdomNeurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United KingdomNeurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United KingdomDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom; Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United KingdomJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United KingdomJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United KingdomJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDrosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom; Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United KingdomDepartment of Neuroscience, Columbia University, Zuckerman Institute, New York, United StatesDepartment of Neuroscience, Columbia University, Zuckerman Institute, New York, United StatesCentre for Neural Circuits & Behaviour, University of Oxford, Oxford, United KingdomJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesMaking inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory, and activity regulation. Here, we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.https://elifesciences.org/articles/62576dopaminelearningmemoryneuronal circuitsbehavior
spellingShingle Feng Li
Jack W Lindsey
Elizabeth C Marin
Nils Otto
Marisa Dreher
Georgia Dempsey
Ildiko Stark
Alexander S Bates
Markus William Pleijzier
Philipp Schlegel
Aljoscha Nern
Shin-ya Takemura
Nils Eckstein
Tansy Yang
Audrey Francis
Amalia Braun
Ruchi Parekh
Marta Costa
Louis K Scheffer
Yoshinori Aso
Gregory SXE Jefferis
Larry F Abbott
Ashok Litwin-Kumar
Scott Waddell
Gerald M Rubin
The connectome of the adult Drosophila mushroom body provides insights into function
eLife
dopamine
learning
memory
neuronal circuits
behavior
title The connectome of the adult Drosophila mushroom body provides insights into function
title_full The connectome of the adult Drosophila mushroom body provides insights into function
title_fullStr The connectome of the adult Drosophila mushroom body provides insights into function
title_full_unstemmed The connectome of the adult Drosophila mushroom body provides insights into function
title_short The connectome of the adult Drosophila mushroom body provides insights into function
title_sort connectome of the adult drosophila mushroom body provides insights into function
topic dopamine
learning
memory
neuronal circuits
behavior
url https://elifesciences.org/articles/62576
work_keys_str_mv AT fengli theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT jackwlindsey theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT elizabethcmarin theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT nilsotto theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT marisadreher theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT georgiadempsey theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT ildikostark theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT alexandersbates theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT markuswilliampleijzier theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT philippschlegel theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT aljoschanern theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT shinyatakemura theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT nilseckstein theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT tansyyang theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT audreyfrancis theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT amaliabraun theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT ruchiparekh theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT martacosta theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT louiskscheffer theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT yoshinoriaso theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT gregorysxejefferis theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT larryfabbott theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT ashoklitwinkumar theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT scottwaddell theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT geraldmrubin theconnectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT fengli connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT jackwlindsey connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT elizabethcmarin connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT nilsotto connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT marisadreher connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT georgiadempsey connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT ildikostark connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT alexandersbates connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT markuswilliampleijzier connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT philippschlegel connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT aljoschanern connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT shinyatakemura connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT nilseckstein connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT tansyyang connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT audreyfrancis connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT amaliabraun connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT ruchiparekh connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT martacosta connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT louiskscheffer connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT yoshinoriaso connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT gregorysxejefferis connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT larryfabbott connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT ashoklitwinkumar connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT scottwaddell connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction
AT geraldmrubin connectomeoftheadultdrosophilamushroombodyprovidesinsightsintofunction