The connectome of the adult Drosophila mushroom body provides insights into function
- Howard Hughes Medical Institute, United States
- Columbia University, United States
- University of Cambridge, United Kingdom
- University of Oxford, United Kingdom
- MRC Laboratory of Molecular Biology, United Kingdom
- Cambridge University, United Kingdom
Abstract
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.
Data availability
All the primary data used in this study is freely available through a public server (neuprint.janelia.org). All the underlying data behind that server is open source (CC-BY). There is no institutional resource for hosting connectome data. We commit to keeping this available for at least 10 years, and provide procedures where users can copy any or all of it to their own computer. Login is via any Google account; users who wish to remain anonymous can create a separate account for access purposes only.
Article and author information
Author details
Markus William Pleijzier
Gregory SXE Jefferis
Ashok Litwin-Kumar
Funding
Howard Hughes Medical Institute (internal funding)
- Marisa Dreher
- Aljoscha Nern
- Shin-ya Takemura
- Nils Eckstein
- Audrey Francis
- Ruchi Parekh
- Louis K Scheffer
- Yoshi Aso
- Gerald M Rubin
Wellcome Trust (203261/Z/16/Z)
- Feng Li
- Elizabeth C Marin
- Nils Otto
- Georgia Dempsey
- Ildiko Stark
- Philipp Schlegel
- Tansy Yang
- Amalia Braun
- Marta Costa
- Gregory SXE Jefferis
- Scott Waddell
- Gerald M Rubin
Wellcome Trust (200846/Z/16/Z)
- Scott Waddell
National Science Foundation (NeuroNex DBI-1707398)
- Jack W Lindsey
- Larry F Abbott
- Ashok Litwin-Kumar
Department of Energy (DE-SC0020347)
- Jack W Lindsey
Medical Research Council (MC-U105188491)
- Alexander S Bates
- Markus William Pleijzier
- Philipp Schlegel
- Gregory SXE Jefferis
Simons Foundation (SCGB)
- Jack W Lindsey
- Yoshi Aso
- Larry F Abbott
- Ashok Litwin-Kumar
- Gerald M Rubin
Burroughs Wellcome Fund (1017109)
- Ashok Litwin-Kumar
National Institutes of Health (R01EB029858)
- Ashok Litwin-Kumar
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Leslie C Griffith, Brandeis University, United States
Version history
- Received: August 28, 2020
- Accepted: December 11, 2020
- Accepted Manuscript published: December 14, 2020 (version 1)
- Version of Record published: February 26, 2021 (version 2)
Copyright
© 2020, Li et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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The connectome of the adult Drosophila mushroom body provides insights into function
eLife 9:e62576.
https://doi.org/10.7554/eLife.62576
Further reading
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- Neuroscience
Flexible behaviors over long timescales are thought to engage recurrent neural networks in deep brain regions, which are experimentally challenging to study. In insects, recurrent circuit dynamics in a brain region called the central complex (CX) enable directed locomotion, sleep, and context- and experience-dependent spatial navigation. We describe the first complete electron microscopy-based connectome of the Drosophila CX, including all its neurons and circuits at synaptic resolution. We identified new CX neuron types, novel sensory and motor pathways, and network motifs that likely enable the CX to extract the fly’s head direction, maintain it with attractor dynamics, and combine it with other sensorimotor information to perform vector-based navigational computations. We also identified numerous pathways that may facilitate the selection of CX-driven behavioral patterns by context and internal state. The CX connectome provides a comprehensive blueprint necessary for a detailed understanding of network dynamics underlying sleep, flexible navigation, and state-dependent action selection.
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- Neuroscience
The hemibrain connectome provides large-scale connectivity and morphology information for the majority of the central brain of Drosophila melanogaster. Using this data set, we provide a complete description of the Drosophila olfactory system, covering all first, second and lateral horn-associated third-order neurons. We develop a generally applicable strategy to extract information flow and layered organisation from connectome graphs, mapping olfactory input to descending interneurons. This identifies a range of motifs including highly lateralised circuits in the antennal lobe and patterns of convergence downstream of the mushroom body and lateral horn. Leveraging a second data set we provide a first quantitative assessment of inter- versus intra-individual stereotypy. Comparing neurons across two brains (three hemispheres) reveals striking similarity in neuronal morphology across brains. Connectivity correlates with morphology and neurons of the same morphological type show similar connection variability within the same brain as across two brains.
