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1. 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

2. The connectome of the adultDrosophilamushroom body: implications for function

Author

Georgia Dempsey, Marta Costa, Philipp Schlegel, Markus William Pleijzier, Feng Li, Ashok Litwin-Kumar, Aljoscha Nern, Yoshinori Aso, Gerald M. Rubin, Jefferis Gsxe, Ruchi Parekh, L. F. Abbott, Ildiko Stark, Alexander Shakeel Bates, Amalia Braun, Elizabeth C. Marin, Audrey Francis, Marisa Dreher, Tansy Yang, Scott Waddell, Louis K. Scheffer, Jack W Lindsey, Satoko Takemura, and Nils Otto

Subjects
Stimulus modality, Neuronal circuits, Computer science, Dopaminergic, Mushroom bodies, Connectome, Sensory system, Neuroscience, Function (biology)
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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3. Author response: A connectome and analysis of the adult Drosophila central brain

Author

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

Subjects
biology, Connectome, Drosophila (subgenus), biology.organism_classification, Neuroscience
Published
2020
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4. Author response: Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain

Author

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

Subjects
Physics, biology, Motion (geometry), Drosophila (subgenus), Edge (geometry), biology.organism_classification, Neuroscience
Published
2018
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5. A connectome of a learning and memory center in the adult Drosophila brain

Author

Christopher Ordish, Toufiq Parag, Shin-ya Takemura, William T. Katz, Roxanne Aniceto, Shirley Lauchie, Stephen M. Plaza, Christopher Sigmund, C. Shan Xu, Satoko Takemura, Stuart Berg, Allan M. Wong, Aya Shinomiya, Donald J. Olbris, Louis K. Scheffer, Lei-Ann Chang, Lowell Umayam, Glenn C. Turner, Omotara Ogundeyi, Harald F. Hess, Ting Zhao, Toshihide Hige, Patricia K. Rivlin, Julie Tran, Zhiyuan Lu, Yoshinori Aso, Gary B. Huang, and Gerald M. Rubin

Subjects
0301 basic medicine, QH301-705.5, Science, En passant, Sensory system, Biology, General Biochemistry, Genetics and Molecular Biology, Synapse, EM reconstruction, 03 medical and health sciences, Memory, dopaminergic neuron, Connectome, Animals, Learning, Biology (General), Mushroom Bodies, D. melanogaster, General Immunology and Microbiology, General Neuroscience, Compartment (ship), Depolarization, General Medicine, memory recall, mushroom body, Associative learning, 030104 developmental biology, Mushroom bodies, Medicine, Drosophila, Neuroscience, Research Article
Abstract

Understanding memory formation, storage and retrieval requires knowledge of the underlying neuronal circuits. In Drosophila, the mushroom body (MB) is the major site of associative learning. We reconstructed the morphologies and synaptic connections of all 983 neurons within the three functional units, or compartments, that compose the adult MB’s α lobe, using a dataset of isotropic 8 nm voxels collected by focused ion-beam milling scanning electron microscopy. We found that Kenyon cells (KCs), whose sparse activity encodes sensory information, each make multiple en passant synapses to MB output neurons (MBONs) in each compartment. Some MBONs have inputs from all KCs, while others differentially sample sensory modalities. Only 6% of KC>MBON synapses receive a direct synapse from a dopaminergic neuron (DAN). We identified two unanticipated classes of synapses, KC>DAN and DAN>MBON. DAN activation produces a slow depolarization of the MBON in these DAN>MBON synapses and can weaken memory recall. DOI: http://dx.doi.org/10.7554/eLife.26975.001

Published
2017
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6. Author response: A connectome of a learning and memory center in the adult Drosophila brain

Author

Toshihide Hige, Christopher Sigmund, Toufiq Parag, Stephen M. Plaza, Aya Shinomiya, C. Shan Xu, Patricia K. Rivlin, Julie Tran, Roxanne Aniceto, Omotara Ogundeyi, Christopher Ordish, Lei-Ann Chang, Harald F. Hess, Louis K. Scheffer, Glenn C. Turner, Lowell Umayam, Gary B. Huang, Gerald M. Rubin, Satoko Takemura, Stuart Berg, Shirley Lauchie, Donald J. Olbris, Zhiyuan Lu, Yoshinori Aso, Shin-ya Takemura, William T. Katz, Allan M. Wong, and Ting Zhao

Subjects
biology, Connectome, Center (algebra and category theory), Drosophila (subgenus), biology.organism_classification, Neuroscience
Published
2017
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7. A visual motion detection circuit suggested by Drosophila connectomics

Author

Zhiyuan Lu, Lei-Ann Chang, Satoko Takemura, Richard D. Fetter, Katerina Blazek, Donald J. Olbris, Christopher Sigmund, Philip Brown Winston, Shin-ya Takemura, William T. Katz, Jane Anne Horne, Arjun Bharioke, Victor Shapiro, Stephen M. Plaza, Patricia K. Rivlin, Mathew A. Saunders, Dmitri B. Chklovskii, Omotara Ogundeyi, Louis K. Scheffer, Shiv Naga Prasad Vitaladevuni, Aljoscha Nern, Ting Zhao, Gerald M. Rubin, and Ian A. Meinertzhagen

Subjects
Connectomics, Retina, Multidisciplinary, Motion Perception, Motion detection, Biology, Models, Biological, Article, Retinal bipolar neuron, Calcium imaging, medicine.anatomical_structure, Models of neural computation, Connectome, medicine, Animals, Drosophila, Female, Visual Pathways, Neuroscience, Medulla
Abstract

Animal behaviour arises from computations in neuronal circuits, but our understanding of these computations has been frustrated by the lack of detailed synaptic connection maps, or connectomes. For example, despite intensive investigations over half a century, the neuronal implementation of local motion detection in the insect visual system remains elusive. Here we develop a semi-automated pipeline using electron microscopy to reconstruct a connectome, containing 379 neurons and 8,637 chemical synaptic contacts, within the Drosophila optic medulla. By matching reconstructed neurons to examples from light microscopy, we assigned neurons to cell types and assembled a connectome of the repeating module of the medulla. Within this module, we identified cell types constituting a motion detection circuit, and showed that the connections onto individual motion-sensitive neurons in this circuit were consistent with their direction selectivity. Our results identify cellular targets for future functional investigations, and demonstrate that connectomes can provide key insights into neuronal computations. Reconstruction of a connectome within the fruitfly visual medulla, containing more than 300 neurons and over 8,000 chemical synapses, reveals a candidate motion detection circuit; such a circuit operates by combining displaced visual inputs, an operation consistent with correlation based motion detection. Three papers in this issue of Nature use the retina as a model for mapping neuronal circuits from the level of individual synaptic contacts to the long-range scale of dendritic interactions. Helmstaedter et al. used electron microscopy to map a mammalian retinal circuit of close to a thousand neurons. The work reveals a new type of retinal bipolar neuron and suggests functional mechanisms for known visual computations. The other two groups study the detection of visual motion in the Drosophila visual system — a classic neural computation model. Takemura et al. used semi-automated electron microscopy to reconstruct the basic connectome (8,637 chemical synapses among 379 neurons) of Drosophila's optic medulla. Their results reveal a candidate motion detection circuit with a wiring plan consistent with direction selectivity. Maisak et al. used calcium imaging to show that T4 and T5 neurons are divided into specific subpopulations responding to motion in four cardinal directions, and are specific to 'ON' versus 'OFF' edges, respectively.

Published
2013
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8. Synaptic circuits and their variations within different columns in the visual system of Drosophila

Author

Ting Zhao, C. Shan Xu, Aya Shinomiya, Omotara Ogundeyi, Roxanne Aniceto, Stephen M. Plaza, Toufiq Parag, Dmitri B. Chklovskii, Shin-ya Takemura, William T. Katz, Juan Nunez-Iglesias, Ian A. Meinertzhagen, Sari McLin, Patricia K. Rivlin, Kelsey Le Lacheur, Shirley Lauchie, Julie Tran, Ashley Nasca, Jane Anne Horne, Christopher Sigmund, Lei Ann Chang, Louis K. Scheffer, Lowell Umayam, Satoko Takemura, Carlie Langille, Donald J. Olbris, Charlotte Weaver, Zhiyuan Lu, and Harald F. Hess

Subjects
Connectomics, Multidisciplinary, Connection (vector bundle), Compound eye, Biology, Biological Sciences, Synapse, medicine.anatomical_structure, Drosophila melanogaster, Postsynaptic potential, Synapses, Neuropil, medicine, Biological neural network, Animals, Neuroscience, Vision, Ocular, Electronic circuit
Abstract

We reconstructed the synaptic circuits of seven columns in the second neuropil or medulla behind the fly's compound eye. These neurons embody some of the most stereotyped circuits in one of the most miniaturized of animal brains. The reconstructions allow us, for the first time to our knowledge, to study variations between circuits in the medulla's neighboring columns. This variation in the number of synapses and the types of their synaptic partners has previously been little addressed because methods that visualize multiple circuits have not resolved detailed connections, and existing connectomic studies, which can see such connections, have not so far examined multiple reconstructions of the same circuit. Here, we address the omission by comparing the circuits common to all seven columns to assess variation in their connection strengths and the resultant rates of several different and distinct types of connection error. Error rates reveal that, overall

Published
2015

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