@article {68225, title = {Neuronal circuits integrating visual motion information in Drosophila melanogaster.}, journal = {Current Biology}, volume = {32}, year = {2022}, month = {2022 Aug 22}, pages = {3529-3544}, abstract = {

The detection of visual motion enables sophisticated animal navigation, and studies on flies have provided profound insights into the cellular and circuit bases of this neural computation. The fly{\textquoteright}s directionally selective T4 and T5 neurons encode ON and OFF motion, respectively. Their axons terminate in one of the four retinotopic layers in the lobula plate, where each layer encodes one of the four directions of motion. Although the input circuitry of the directionally selective neurons has been studied in detail, the synaptic connectivity of circuits integrating T4/T5 motion signals is largely unknown. Here, we report a 3D electron microscopy reconstruction, wherein we comprehensively identified T4/T5{\textquoteright}s synaptic partners in the lobula plate, revealing a diverse set of new cell types and attributing new connectivity patterns to the known cell types. Our reconstruction explains how the ON- and OFF-motion pathways converge. T4 and T5 cells that project to the same layer connect to common synaptic partners and comprise a core motif together with bilayer interneurons, detailing the circuit basis for computing motion opponency. We discovered pathways that likely encode new directions of motion by integrating vertical and horizontal motion signals from upstream T4/T5 neurons. Finally, we identify substantial projections into the lobula, extending the known motion pathways and suggesting that directionally selective signals shape feature detection there. The circuits we describe enrich the anatomical basis for experimental and computations analyses of motion vision and bring us closer to understanding complete sensory-motor pathways.

}, issn = {1879-0445}, doi = {10.1016/j.cub.2022.06.061}, author = {Shinomiya, Kazunori and Nern, Aljoscha and Meinertzhagen, Ian A and Plaza, Stephen M and Reiser, Michael B} } @article {68507, title = {A connectome and analysis of the adult Drosophila central brain.}, journal = {Elife}, volume = {9}, year = {2020}, month = {2020 Sep 07}, 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 . 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{\textquoteright}s brain.

}, keywords = {Animals, Brain, Connectome, Drosophila melanogaster, Female, Male, Neurons, Synapses}, issn = {2050-084X}, doi = {10.7554/eLife.57443}, author = {Scheffer, Louis K and Xu, C Shan and Januszewski, Michal and Lu, Zhiyuan and Takemura, Shin-ya and Hayworth, Kenneth J and Huang, Gary B and Shinomiya, Kazunori and Maitlin-Shepard, Jeremy and Berg, Stuart and Clements, Jody and Hubbard, Philip M and Katz, William T and Umayam, Lowell and Zhao, Ting and Ackerman, David and Blakely, Tim and Bogovic, John and Dolafi, Tom and Kainmueller, Dagmar and Kawase, Takashi and Khairy, Khaled A and Leavitt, Laramie and Li, Peter H and Lindsey, Larry and Neubarth, Nicole and Olbris, Donald J and Otsuna, Hideo and Trautman, Eric T and Ito, Masayoshi and Bates, Alexander S and Goldammer, Jens and Wolff, Tanya and Svirskas, Robert and Schlegel, Philipp and Neace, Erika and Knecht, Christopher J and Alvarado, Chelsea X and Bailey, Dennis A and Ballinger, Samantha and Borycz, Jolanta A and Canino, Brandon S and Cheatham, Natasha and Cook, Michael and Dreher, Marisa and Duclos, Octave and Eubanks, Bryon and Fairbanks, Kelli and Finley, Samantha and Forknall, Nora and Francis, Audrey and Hopkins, Gary Patrick and Joyce, Emily M and Kim, SungJin and Kirk, Nicole A and Kovalyak, Julie and Lauchie, Shirley A and Lohff, Alanna and Maldonado, Charli and Manley, Emily A and McLin, Sari and Mooney, Caroline and Ndama, Miatta and Ogundeyi, Omotara and Okeoma, Nneoma and Ordish, Christopher and Padilla, Nicholas and Patrick, Christopher M and Paterson, Tyler and Phillips, Elliott E and Phillips, Emily M and Rampally, Neha and Ribeiro, Caitlin and Robertson, Madelaine K and Rymer, Jon Thomson and Ryan, Sean M and Sammons, Megan and Scott, Anne K and Scott, Ashley L and Shinomiya, Aya and Smith, Claire and Smith, Kelsey and Smith, Natalie L and Sobeski, Margaret A and Suleiman, Alia and Swift, Jackie and Takemura, Satoko and Talebi, Iris and Tarnogorska, Dorota and Tenshaw, Emily and Tokhi, Temour and Walsh, John J and Yang, Tansy and Horne, Jane Anne and Li, Feng and Parekh, Ruchi and Rivlin, Patricia K and Jayaraman, Vivek and Costa, Marta and Jefferis, Gregory Sxe and Ito, Kei and Saalfeld, Stephan and George, Reed and Meinertzhagen, Ian A and Rubin, Gerald M and Hess, Harald F and Jain, Viren and Plaza, Stephen M} } @article {51252, title = {Comparisons between the ON- and OFF-edge motion pathways in the brain.}, journal = {eLife}, volume = {8}, year = {2019}, month = {2019 Jan 09}, abstract = {

Understanding the circuit mechanisms behind motion detection is a long-standing question in visual neuroscience. In , recent synapse-level connectomes in the optic lobe, particularly in ON-pathway (T4) receptive-field circuits, in concert with physiological studies, suggest an increasingly intricate motion model compared with the ubiquitous Hassenstein-Reichardt model, while 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 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. While the two pathways are likely evolutionarily linked and indeed exhibit many similarities, we uncover interesting differences and interactions that may underlie their distinct functional properties.

}, issn = {2050-084X}, doi = {10.7554/eLife.40025}, author = {Shinomiya, Kazunori and Huang, Gary and Lu, Zhiyuan and Parag, Toufiq and Xu, C Shan and Aniceto, Roxanne and Ansari, Namra and Cheatham, Natasha and Lauchie, Shirley and Neace, Erika and Ogundeyi, Omotara and Ordish, Christopher and Peel, David and Shinomiya, Aya and Smith, Claire and Takemura, Satoko and Talebi, Iris and Rivlin, Patricia K and Nern, Aljoscha and Scheffer, Louis K and Plaza, Stephen M and Meinertzhagen, Ian A} } @article {65206, title = {The organization of the second optic chiasm of the optic lobe.}, journal = {Frontiers in Neural Circuits}, volume = {13}, year = {2019}, month = {2019 Oct 11}, pages = {65}, abstract = {

Visual pathways from the compound eye of an insect relay to four neuropils, successively the lamina, medulla, lobula, and lobula plate in the underlying optic lobe. Among these neuropils, the medulla, lobula, and lobula plate are interconnected by the complex second optic chiasm, through which the anteroposterior axis undergoes an inversion between the medulla and lobula. Given their complex structure, the projection patterns through the second optic chiasm have so far lacked critical analysis. By densely reconstructing axon trajectories using a volumetric scanning electron microscopy (SEM) technique, we reveal the three-dimensional structure of the second optic chiasm of , which comprises interleaving bundles and sheets of axons insulated from each other by glial sheaths. These axon bundles invert their horizontal sequence in passing between the medulla and lobula. Axons connecting the medulla and lobula plate are also bundled together with them but do not decussate the sequence of their horizontal positions. They interleave with sheets of projection neuron axons between the lobula and lobula plate, which also lack decussations. We estimate that approximately 19,500 cells per hemisphere, about two thirds of the optic lobe neurons, contribute to the second chiasm, most being Tm cells, with an estimated additional 2,780 T4 and T5 cells each. The chiasm mostly comprises axons and cell body fibers, but also a few synaptic elements. Based on our anatomical findings, we propose that a chiasmal structure between the neuropils is potentially advantageous for processing complex visual information in parallel. The EM reconstruction shows not only the structure of the chiasm in the adult brain, the previously unreported main topic of our study, but also suggest that the projection patterns of the neurons comprising the chiasm may be determined by the proliferation centers from which the neurons develop. Such a complex wiring pattern could, we suggest, only have arisen in several evolutionary steps.

}, issn = {1662-5110}, doi = {10.3389/fncir.2019.00065}, author = {Shinomiya, Kazunori and Horne, Jane Anne and McLin, Sari and Wiederman, Meagan and Nern, Aljoscha and Plaza, Stephen M and Meinertzhagen, Ian A} } @inbook {48701, title = {Recent progress in the 3D reconstruction of Drosophila neural circuits.}, booktitle = {Decoding Neural Circuit Structure and Function}, year = {2017}, pages = {63-89}, publisher = {Springer}, organization = {Springer}, abstract = {

The brain of fruit fly Drosophila melanogaster has been used as a model system for functional analysis of neuronal circuits, including connectomics research, due to its modest size (~700\ μm) and availability of abundant molecular genetics tools for visualizing neurons. Three-dimensional (3D) reconstruction of high-resolution images of neurons or circuits visualized with appropriate methods is a critical step for obtaining information such as morphology and connectivity patterns of neuronal circuits. In this chapter, we introduce methods for generating 3D reconstructed images with data acquired from confocal laser scanning microscopy (CLSM) or electron microscopy (EM) to analyze neuronal circuits found in the central nervous system (CNS) of the fruit fly. Comparisons of different algorithms and strategies for reconstructing neuronal circuits, using actual studies as references, will be discussed within this chapter.

}, doi = {10.1007/978-3-319-57363-2_3}, author = {Shinomiya, Kazunori and Ito, Masayoshi} } @article {46940, title = {A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system.}, journal = {Frontiers in Neural Circuits}, volume = {9}, year = {2015}, month = {2015}, pages = {33}, abstract = {

Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate (LOP), that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the LOP. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: (1) the morphology of their dendritic arbors; (2) their four morphological and functional subtypes; (3) their cholinergic profile in Drosophila; (4) their input from the pathways of L3 cells in the first neuropil, or lamina (LA), and by one of a pair of LA cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and (5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO). Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.

}, issn = {1662-5110}, doi = {10.3389/fncir.2015.00033}, author = {Shinomiya, Kazunori and Takemura, Shin-ya and Rivlin, Patricia K and Plaza, Stephen M and Scheffer, Louis K and Meinertzhagen, Ian A} } @article {6884, title = {A systematic nomenclature for the insect brain.}, journal = {Neuron}, volume = {81}, year = {2014}, month = {2014 Feb 19}, pages = {755-65}, abstract = {

Despite the importance of the insect nervous system for functional and developmental neuroscience, descriptions of insect brains have suffered from a lack of uniform nomenclature. Ambiguous definitions of brain regions and fiber bundles have contributed to the variation of names used to describe the same structure. The lack of clearly determined neuropil boundaries has made it difficult to document precise locations of neuronal projections for connectomics study. To address such issues, a consortium of\ neurobiologists studying arthropod brains, the Insect Brain Name Working Group, has established the present hierarchical nomenclature system, using the brain of Drosophila melanogaster as the reference framework, while taking the brains of other taxa into careful consideration for maximum consistency and expandability. The following summarizes the consortium{\textquoteright}s nomenclature system and highlights examples of existing ambiguities and remedies for them. This nomenclature is intended to serve as a\ standard of reference for the study of the brain of Drosophila and other insects.

}, issn = {1097-4199}, doi = {10.1016/j.neuron.2013.12.017}, author = {Ito, Kei and Shinomiya, Kazunori and Ito, Masayoshi and Armstrong, J Douglas and Boyan, George and Hartenstein, Volker and Harzsch, Steffen and Heisenberg, Martin and Homberg, Uwe and Jenett, Arnim and Keshishian, Haig and Restifo, Linda L and R{\"o}ssler, Wolfgang and Simpson, Julie H and Strausfeld, Nicholas J and Strauss, Roland and Vosshall, Leslie B} }