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

Author

Jack W Lindsey, Philipp Schlegel, Louis K. Scheffer, Audrey Francis, Marta Costa, Markus William Pleijzier, Feng Li, Nils Otto, Scott Waddell, Shin-ya Takemura, Gregory S.X.E. Jefferis, Ashok Litwin-Kumar, Alexander Shakeel Bates, Amalia Braun, Larry F. Abbott, Georgia Dempsey, Elizabeth C. Marin, Marisa Dreher, Ruchi Parekh, Ildiko Stark, Nils Eckstein, Aljoscha Nern, Tansy Yang, Yoshinori Aso, Gerald M. Rubin, Li, Feng [0000-0002-6658-9175], Lindsey, Jack W [0000-0003-0930-7327], Marin, Elizabeth C [0000-0001-6333-0072], Otto, Nils [0000-0001-9713-4088], Dreher, Marisa [0000-0002-0041-9229], Dempsey, Georgia [0000-0002-1854-8336], Bates, Alexander S [0000-0002-1195-0445], Pleijzier, Markus William [0000-0002-7297-4547], Schlegel, Philipp [0000-0002-5633-1314], Nern, Aljoscha [0000-0002-3822-489X], Takemura, Shin-Ya [0000-0003-2400-6426], Yang, Tansy [0000-0003-1131-0410], Francis, Audrey [0000-0003-1974-7174], Parekh, Ruchi [0000-0002-8060-2807], Costa, Marta [0000-0001-5948-3092], Scheffer, Louis K [0000-0002-3289-6564], Aso, Yoshinori [0000-0002-2939-1688], Jefferis, Gregory Sxe [0000-0002-0587-9355], Litwin-Kumar, Ashok [0000-0003-2422-6576], Waddell, Scott [0000-0003-4503-6229], Rubin, Gerald M [0000-0001-8762-8703], and Apollo - University of Cambridge Repository

Subjects
QH301-705.5, Computer science, Science, Sensory system, neuronal circuits, General Biochemistry, Genetics and Molecular Biology, memory, 03 medical and health sciences, 0302 clinical medicine, Stimulus modality, Connectome, Animals, Experimental work, Biology (General), Mushroom Bodies, 030304 developmental biology, Brain Mapping, 0303 health sciences, learning, D. melanogaster, General Immunology and Microbiology, behavior, General Neuroscience, General Medicine, Drosophila melanogaster, Neuronal circuits, Mushroom bodies, Medicine, Activity regulation, dopamine, Neuroscience, 030217 neurology & neurosurgery, Function (biology), Research Article
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 inDrosophila, 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.

Published
2020
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2. A connectome and analysis of the adult Drosophila central brain

Author

Temour Tokhi, Tom Dolafi, Nneoma Okeoma, Tanya Wolff, Philip M Hubbard, Kazunori Shinomiya, Madelaine K Robertson, Gerald M. Rubin, Gregory S.X.E. Jefferis, Christopher J Knecht, Laramie Leavitt, Alia Suleiman, Satoko Takemura, Christopher Ordish, Jody Clements, Ian A. Meinertzhagen, Alexander Shakeel Bates, Takashi Kawase, Samantha Finley, Nicholas Padilla, Jackie Swift, C. Shan Xu, Stuart Berg, Tyler Paterson, Ashley L Scott, Erika Neace, Shirley Lauchie, Sean M Ryan, Emily M Joyce, Shin-ya Takemura, Tim Blakely, Michael A Cook, Christopher Patrick, Bryon Eubanks, Audrey Francis, Robert Svirskas, William T. Katz, Eric T. Trautman, Caroline Mooney, Ting Zhao, Nicole A Kirk, Megan Sammons, Brandon S Canino, Reed A. George, Louis K. Scheffer, Jolanta A. Borycz, Jon Thomson Rymer, Natasha Cheatham, Dagmar Kainmueller, Gary B. Huang, Khaled Khairy, Nicole Neubarth, Elliott E Phillips, John A. Bogovic, Neha Rampally, Larry Lindsey, Viren Jain, David G. Ackerman, Jane Anne Horne, Kelli Fairbanks, Lowell Umayam, Jens Goldammer, Emily M Phillips, Donald J. Olbris, Feng Li, Emily A Manley, Philipp Schlegel, Hideo Otsuna, Marta Costa, Stephen M. Plaza, Omotara Ogundeyi, Samantha Ballinger, Charli Maldonado, Kelsey Smith, Gary Patrick Hopkins, Vivek Jayaraman, Emily Tenshaw, Julie Kovalyak, Peter H. Li, Tansy Yang, Masayoshi Ito, Miatta Ndama, Claire Smith, Michał Januszewski, Alanna Lohff, SungJin Kim, Anne K Scott, Kei Ito, Iris Talebi, Jeremy Maitlin-Shepard, Nora Forknall, Marisa Dreher, Harald F. Hess, Sari McLin, Patricia K. Rivlin, Dennis A Bailey, Kenneth J. Hayworth, Octave Duclos, Caitlin Ribeiro, John J. Walsh, Zhiyuan Lu, Dorota Tarnogorska, Ruchi Parekh, Aya Shinomiya, Stephan Saalfeld, Margaret A Sobeski, Natalie L Smith, Chelsea X Alvarado, Scheffer, Louis K [0000-0002-3289-6564], Xu, C Shan [0000-0002-8564-7836], Januszewski, Michal [0000-0002-3480-2744], Lu, Zhiyuan [0000-0002-4128-9774], Takemura, Shin-ya [0000-0003-2400-6426], Huang, Gary B [0000-0002-9606-3510], Shinomiya, Kazunori [0000-0003-0262-6421], Maitlin-Shepard, Jeremy [0000-0001-8453-7961], Hubbard, Philip M [0000-0002-6746-5035], Katz, William T [0000-0002-9417-6212], Ackerman, David [0000-0003-0172-6594], Blakely, Tim [0000-0003-0995-5471], Bogovic, John [0000-0002-4829-9457], Kainmueller, Dagmar [0000-0002-9830-2415], Khairy, Khaled A [0000-0002-9274-5928], Li, Peter H [0000-0001-6193-4454], Trautman, Eric T [0000-0001-8588-0569], Bates, Alexander S [0000-0002-1195-0445], Goldammer, Jens [0000-0002-5623-8339], Wolff, Tanya [0000-0002-8681-1749], Svirskas, Robert [0000-0001-8374-6008], Schlegel, Philipp [0000-0002-5633-1314], Knecht, Christopher J [0000-0002-5663-5967], Alvarado, Chelsea X [0000-0002-5973-7512], Bailey, Dennis A [0000-0002-4675-8373], Borycz, Jolanta A [0000-0002-4402-9230], Canino, Brandon S [0000-0002-8454-865X], Cook, Michael [0000-0002-7892-6845], Dreher, Marisa [0000-0002-0041-9229], Eubanks, Bryon [0000-0002-9288-2009], Fairbanks, Kelli [0000-0002-6601-4830], Finley, Samantha [0000-0002-8086-206X], Forknall, Nora [0000-0003-2139-7599], Francis, Audrey [0000-0003-1974-7174], Joyce, Emily M [0000-0001-5794-6321], Kovalyak, Julie [0000-0001-7864-7734], Lauchie, Shirley A [0000-0001-8223-9522], Lohff, Alanna [0000-0002-1242-1836], McLin, Sari [0000-0002-9120-1136], Patrick, Christopher M [0000-0001-8830-1892], Phillips, Elliott E [0000-0002-4918-2058], Phillips, Emily M [0000-0001-7615-301X], Robertson, Madelaine K [0000-0002-1764-0245], Rymer, Jon Thomson [0000-0002-4271-6774], Ryan, Sean M [0000-0002-8879-6108], Sammons, Megan [0000-0003-4516-5928], Shinomiya, Aya [0000-0002-6358-9567], Smith, Natalie L [0000-0002-8271-9873], Swift, Jackie [0000-0003-1321-8183], Takemura, Satoko [0000-0002-2863-0050], Talebi, Iris [0000-0002-0173-8053], Tarnogorska, Dorota [0000-0002-7063-6165], Walsh, John J [0000-0002-7176-4708], Yang, Tansy [0000-0003-1131-0410], Horne, Jane Anne [0000-0001-9673-2692], Parekh, Ruchi [0000-0002-8060-2807], Jayaraman, Vivek [0000-0003-3680-7378], Costa, Marta [0000-0001-5948-3092], Jefferis, Gregory SXE [0000-0002-0587-9355], Ito, Kei [0000-0002-7274-5533], Saalfeld, Stephan [0000-0002-4106-1761], Rubin, Gerald M [0000-0001-8762-8703], Hess, Harald F [0000-0003-3000-1533], Plaza, Stephen M [0000-0001-7425-8555], Apollo - University of Cambridge Repository, Takemura, Shin-Ya [0000-0003-2400-6426], and Jefferis, Gregory Sxe [0000-0002-0587-9355]

Subjects
Male, Computer science, computational biology, 0302 clinical medicine, Drosophila Proteins, Research article, Biology (General), Neurons, Cognitive science, 0303 health sciences, biology, D. melanogaster, General Neuroscience, connectome, Brain, systems biology, graph properties, General Medicine, Human brain, Drosophila melanogaster, medicine.anatomical_structure, Connectome, Medicine, Drosophila, Female, synapse detecton, Insight, Function and Dysfunction of the Nervous System, cell types, Research Article, Computational and Systems Biology, brain regions, Connectomes, QH301-705.5, Ubiquitin-Protein Ligases, Science, connectome reconstuction methods, Small mammal, Central region, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, medicine, Animals, 030304 developmental biology, General Immunology and Microbiology, biology.organism_classification, synapse detection, Synapses, 030217 neurology & neurosurgery, Neuroscience
Abstract

The neural circuits responsible for animal behavior remain largely unknown. We summarize new methods and present the circuitry of a large fraction of the brain of the fruit fly Drosophila melanogaster. Improved methods include new procedures to prepare, image, align, segment, find synapses in, and proofread such large data sets. We define cell types, refine computational compartments, and provide an exhaustive atlas of cell examples and types, many of them novel. We provide detailed circuits consisting of neurons and their chemical synapses for most of the central brain. We make the data public and simplify access, reducing the effort needed to answer circuit questions, and provide procedures linking the neurons defined by our analysis with genetic reagents. Biologically, we examine distributions of connection strengths, neural motifs on different scales, electrical consequences of compartmentalization, and evidence that maximizing packing density is an important criterion in the evolution of the fly’s brain., eLife digest Animal brains of all sizes, from the smallest to the largest, work in broadly similar ways. Studying the brain of any one animal in depth can thus reveal the general principles behind the workings of all brains. The fruit fly Drosophila is a popular choice for such research. With about 100,000 neurons – compared to some 86 billion in humans – the fly brain is small enough to study at the level of individual cells. But it nevertheless supports a range of complex behaviors, including navigation, courtship and learning. Thanks to decades of research, scientists now have a good understanding of which parts of the fruit fly brain support particular behaviors. But exactly how they do this is often unclear. This is because previous studies showing the connections between cells only covered small areas of the brain. This is like trying to understand a novel when all you can see is a few isolated paragraphs. To solve this problem, Scheffer, Xu, Januszewski, Lu, Takemura, Hayworth, Huang, Shinomiya et al. prepared the first complete map of the entire central region of the fruit fly brain. The central brain consists of approximately 25,000 neurons and around 20 million connections. To prepare the map – or connectome – the brain was cut into very thin 8nm slices and photographed with an electron microscope. A three-dimensional map of the neurons and connections in the brain was then reconstructed from these images using machine learning algorithms. Finally, Scheffer et al. used the new connectome to obtain further insights into the circuits that support specific fruit fly behaviors. The central brain connectome is freely available online for anyone to access. When used in combination with existing methods, the map will make it easier to understand how the fly brain works, and how and why it can fail to work correctly. Many of these findings will likely apply to larger brains, including our own. In the long run, studying the fly connectome may therefore lead to a better understanding of the human brain and its disorders. Performing a similar analysis on the brain of a small mammal, by scaling up the methods here, will be a likely next step along this path.

Published
2020

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