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1. A connectome and analysis of the adult Drosophila central brain

Author

Louis K Scheffer, C Shan Xu, Michal Januszewski, Zhiyuan Lu, Shin-ya Takemura, Kenneth J Hayworth, Gary B Huang, Kazunori Shinomiya, Jeremy Maitlin-Shepard, Stuart Berg, Jody Clements, Philip M Hubbard, William T Katz, Lowell Umayam, Ting Zhao, David Ackerman, Tim Blakely, John Bogovic, Tom Dolafi, Dagmar Kainmueller, Takashi Kawase, Khaled A Khairy, Laramie Leavitt, Peter H Li, Larry Lindsey, Nicole Neubarth, Donald J Olbris, Hideo Otsuna, Eric T Trautman, Masayoshi Ito, Alexander S Bates, Jens Goldammer, Tanya Wolff, Robert Svirskas, Philipp Schlegel, Erika Neace, Christopher J Knecht, Chelsea X Alvarado, Dennis A Bailey, Samantha Ballinger, Jolanta A Borycz, Brandon S Canino, Natasha Cheatham, Michael Cook, Marisa Dreher, Octave Duclos, Bryon Eubanks, Kelli Fairbanks, Samantha Finley, Nora Forknall, Audrey Francis, Gary Patrick Hopkins, Emily M Joyce, SungJin Kim, Nicole A Kirk, Julie Kovalyak, Shirley A Lauchie, Alanna Lohff, Charli Maldonado, Emily A Manley, Sari McLin, Caroline Mooney, Miatta Ndama, Omotara Ogundeyi, Nneoma Okeoma, Christopher Ordish, Nicholas Padilla, Christopher M Patrick, Tyler Paterson, Elliott E Phillips, Emily M Phillips, Neha Rampally, Caitlin Ribeiro, Madelaine K Robertson, Jon Thomson Rymer, Sean M Ryan, Megan Sammons, Anne K Scott, Ashley L Scott, Aya Shinomiya, Claire Smith, Kelsey Smith, Natalie L Smith, Margaret A Sobeski, Alia Suleiman, Jackie Swift, Satoko Takemura, Iris Talebi, Dorota Tarnogorska, Emily Tenshaw, Temour Tokhi, John J Walsh, Tansy Yang, Jane Anne Horne, Feng Li, Ruchi Parekh, Patricia K Rivlin, Vivek Jayaraman, Marta Costa, Gregory SXE Jefferis, Kei Ito, Stephan Saalfeld, Reed George, Ian A Meinertzhagen, Gerald M Rubin, Harald F Hess, Viren Jain, and Stephen M Plaza

Subjects
connectome, brain regions, cell types, graph properties, connectome reconstuction methods, synapse detecton, Medicine, Science, Biology (General), QH301-705.5
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.

Published
2020
Full Text
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2. Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain

Author

Kazunori Shinomiya, Gary Huang, Zhiyuan Lu, Toufiq Parag, C Shan Xu, Roxanne Aniceto, Namra Ansari, Natasha Cheatham, Shirley Lauchie, Erika Neace, Omotara Ogundeyi, Christopher Ordish, David Peel, Aya Shinomiya, Claire Smith, Satoko Takemura, Iris Talebi, Patricia K Rivlin, Aljoscha Nern, Louis K Scheffer, Stephen M Plaza, and Ian A Meinertzhagen

Subjects
visual system, motion detection, electron microscopy, connectome, neuroanatomy, optic lobe, Medicine, Science, Biology (General), QH301-705.5
Abstract

Understanding the circuit mechanisms behind motion detection is a long-standing question in visual neuroscience. In Drosophila melanogaster, recently discovered synapse-level connectomes in the optic lobe, particularly in ON-pathway (T4) receptive-field circuits, in concert with physiological studies, suggest a motion model that is increasingly intricate when compared with the ubiquitous Hassenstein-Reichardt model. By contrast, our knowledge of OFF-pathway (T5) has been incomplete. Here, we present a conclusive and comprehensive connectome that, for the first time, integrates detailed connectivity information for inputs to both the T4 and T5 pathways in a single EM dataset covering the entire optic lobe. With novel reconstruction methods using automated synapse prediction suited to such a large connectome, we successfully corroborate previous findings in the T4 pathway and comprehensively identify inputs and receptive fields for T5. Although the two pathways are probably evolutionarily linked and exhibit many similarities, we uncover interesting differences and interactions that may underlie their distinct functional properties.

Published
2019
Full Text
View/download PDF

3. 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

4. Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain

Author

Natasha Cheatham, Iris Talebi, Aya Shinomiya, C. Shan Xu, Claire Smith, Omotara Ogundeyi, David Peel, Kazunori Shinomiya, Shirley Lauchie, Erika Neace, Namra Ansari, Louis K. Scheffer, Roxanne Aniceto, Patricia K. Rivlin, Toufiq Parag, Zhiyuan Lu, Ian A. Meinertzhagen, Gary B. Huang, Aljoscha Nern, Christopher Ordish, Satoko Takemura, and Stephen M. Plaza

Subjects
Computer science, QH301-705.5, neuroanatomy, Science, Models, Neurological, Motion Perception, General Biochemistry, Genetics and Molecular Biology, Motion (physics), Synapse, medicine, motion detection, Image Processing, Computer-Assisted, Animals, Biology (General), Crosses, Genetic, Neurons, optic lobe, General Immunology and Microbiology, biology, electron microscopy, D. melanogaster, General Neuroscience, connectome, Homozygote, Optic Lobe, Nonmammalian, Brain, Motion detection, General Medicine, Dendrites, biology.organism_classification, Lobe, medicine.anatomical_structure, Drosophila melanogaster, Receptive field, Synapses, Connectome, Medicine, visual system, Female, Photoreceptor Cells, Invertebrate, Neuroscience, Neuroanatomy, Research Article
Abstract

Understanding the circuit mechanisms behind motion detection is a long-standing question in visual neuroscience. In Drosophila melanogaster, recently discovered synapse-level connectomes in the optic lobe, particularly in ON-pathway (T4) receptive-field circuits, in concert with physiological studies, suggest a motion model that is increasingly intricate when compared with the ubiquitous Hassenstein-Reichardt model. By contrast, our knowledge of OFF-pathway (T5) has been incomplete. Here, we present a conclusive and comprehensive connectome that, for the first time, integrates detailed connectivity information for inputs to both the T4 and T5 pathways in a single EM dataset covering the entire optic lobe. With novel reconstruction methods using automated synapse prediction suited to such a large connectome, we successfully corroborate previous findings in the T4 pathway and comprehensively identify inputs and receptive fields for T5. Although the two pathways are probably evolutionarily linked and exhibit many similarities, we uncover interesting differences and interactions that may underlie their distinct functional properties.

Published
2019

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