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130 Publications

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    05/18/22 | A functionally ordered visual feature map in the Drosophila brain.
    Klapoetke NC, Nern A, Rogers EM, Rubin GM, Reiser MB, Card GM
    Neuron. 2022 May 18;110(10):1700. doi: 10.1016/j.neuron.2022.02.013

    Topographic maps, the systematic spatial ordering of neurons by response tuning, are common across species. In Drosophila, the lobula columnar (LC) neuron types project from the optic lobe to the central brain, where each forms a glomerulus in a distinct position. However, the advantages of this glomerular arrangement are unclear. Here, we examine the functional and spatial relationships of 10 glomeruli using single-neuron calcium imaging. We discover novel detectors for objects smaller than the lens resolution (LC18) and for complex line motion (LC25). We find that glomeruli are spatially clustered by selectivity for looming versus drifting object motion and ordered by size tuning to form a topographic visual feature map. Furthermore, connectome analysis shows that downstream neurons integrate from sparse subsets of possible glomeruli combinations, which are biased for glomeruli encoding similar features. LC neurons are thus an explicit example of distinct feature detectors topographically organized to facilitate downstream circuit integration.

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    12/16/21 | Synaptic targets of photoreceptors specialized to detect color and skylight polarization in .
    Kind E, Longden KD, Nern A, Zhao A, Sancer G, Flynn MA, Laughland CW, Gezahegn B, Ludwig HD, Thomson AG, Obrusnik T, Alarcón PG, Dionne H, Bock DD, Rubin GM, Reiser MB, Wernet MF
    eLife. 2021 Dec 16;10:. doi: 10.7554/eLife.71858

    Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

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    12/14/20 | The connectome of the adult mushroom body provides insights into function.
    Li F, Lindsey JW, Marin EC, Otto N, Dreher M, Dempsey G, Stark I, Bates AS, Pleijzier MW, Schlegel P, Nern A, Takemura S, Eckstein N, Yang T, Francis A, Braun A, Parekh R, Costa M, Scheffer LK, Aso Y, Jefferis GS, Abbott LF, Litwin-Kumar A, Waddell S, Rubin GM
    eLife. 2020 Dec 14;9:. doi: 10.7554/eLife.62576

    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 , 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.

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    10/26/21 | A connectome of the central complex reveals network motifs suitable for flexible navigation and context-dependent action selection.
    Hulse BK, Haberkern H, Franconville R, Turner-Evans DB, Takemura S, Wolff T, Noorman M, Dreher M, Dan C, Parekh R, Hermundstad AM, Rubin GM, Jayaraman V
    eLife. 2021 Oct 26;10:. doi: 10.7554/eLife.66039

    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 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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    05/28/21 | Information flow, cell types and stereotypy in a full olfactory connectome.
    Schlegel P, Bates AS, Stürner T, Jagannathan SR, Drummond N, Hsu J, Serratosa Capdevila L, Javier A, Marin EC, Barth-Maron A, Tamimi IF, Li F, Rubin GM, Plaza SM, Costa M, Jefferis GS
    eLife. 2021 May 25;10:. doi: 10.7554/eLife.66018

    The connectome provides large scale connectivity and morphology information for the majority of the central brain of . Using this data set, we provide a complete description of the 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.

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    11/18/20 | Spatial readout of visual looming in the central brain of Drosophila.
    Morimoto MM, Nern A, Zhao A, Rogers EM, Wong A, Isaacson MD, Bock D, Rubin GM, Reiser MB
    eLife. 2020 Nov 18;9:. doi: 10.7554/eLife.57685

    Visual systems can exploit spatial correlations in the visual scene by using retinotopy. However, retinotopy is often lost, such as when visual pathways are integrated with other sensory modalities. How is spatial information processed outside of strictly visual brain areas? Here, we focused on visual looming responsive LC6 cells in , a population whose dendrites collectively cover the visual field, but whose axons form a single glomerulus-a structure without obvious retinotopic organization-in the central brain. We identified multiple cell types downstream of LC6 in the glomerulus and found that they more strongly respond to looming in different portions of the visual field, unexpectedly preserving spatial information. Through EM reconstruction of all LC6 synaptic inputs to the glomerulus, we found that LC6 and downstream cell types form circuits within the glomerulus that enable spatial readout of visual features and contralateral suppression-mechanisms that transform visual information for behavioral control.

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    11/03/20 | Cell types and neuronal circuitry underlying female aggression in Drosophila.
    Schretter CE, Aso Y, Robie AA, Dreher M, Dolan M, Chen N, Ito M, Yang T, Parekh R, Branson KM, Rubin GM
    eLife. 2020 Nov 03;9:. doi: 10.7554/eLife.58942

    Aggressive social interactions are used to compete for limited resources and are regulated by complex sensory cues and the organism's internal state. While both sexes exhibit aggression, its neuronal underpinnings are understudied in females. Here, we identify a population of sexually dimorphic aIPg neurons in the adult central brain whose optogenetic activation increased, and genetic inactivation reduced, female aggression. Analysis of GAL4 lines identified in an unbiased screen for increased female chasing behavior revealed the involvement of another sexually dimorphic neuron, pC1d, and implicated aIPg and pC1d neurons as core nodes regulating female aggression. Connectomic analysis demonstrated that aIPg neurons and pC1d are interconnected and suggest that aIPg neurons may exert part of their effect by gating the flow of visual information to descending neurons. Our work reveals important regulatory components of the neuronal circuitry that underlies female aggressive social interactions and provides tools for their manipulation.

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    10/14/20 | The neuroanatomical ultrastructure and function of a biological ring attractor.
    Turner-Evans DB, Jensen KT, Ali S, Paterson T, Sheridan A, Ray RP, Wolff T, Lauritzen JS, Rubin GM, Bock DD, Jayaraman V
    Neuron. 2020 Oct 14;108(1):145-63. doi: 10.1016/j.neuron.2020.08.006

    Neural representations of head direction (HD) have been discovered in many species. Theoretical work has proposed that the dynamics associated with these representations are generated, maintained, and updated by recurrent network structures called ring attractors. We evaluated this theorized structure-function relationship by performing electron-microscopy-based circuit reconstruction and RNA profiling of identified cell types in the HD system of Drosophila melanogaster. We identified motifs that have been hypothesized to maintain the HD representation in darkness, update it when the animal turns, and tether it to visual cues. Functional studies provided support for the proposed roles of individual excitatory or inhibitory circuit elements in shaping activity. We also discovered recurrent connections between neuronal arbors with mixed pre- and postsynaptic specializations. Our results confirm that the Drosophila HD network contains the core components of a ring attractor while also revealing unpredicted structural features that might enhance the network's computational power.

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    Rubin LabSvoboda Lab
    09/17/20 | The mind of a mouse.
    Abbott LF, Bock DD, Callaway EM, Denk W, Dulac C, Fairhall AL, Fiete I, Harris KM, Helmstaedter M, Jain V, Kasthuri N, LeCun Y, Lichtman JW, Littlewood PB, Luo L, Maunsell JH, Reid RC, Rosen BR, Rubin GM, Sejnowski TJ, Seung HS, Svoboda K, Tank DW, Tsao D, Van Essen DC
    Cell. 2020 Sep 17;182(6):1372-1376. doi: 10.1016/j.cell.2020.08.010

    Large scientific projects in genomics and astronomy are influential not because they answer any single question but because they enable investigation of continuously arising new questions from the same data-rich sources. Advances in automated mapping of the brain's synaptic connections (connectomics) suggest that the complicated circuits underlying brain function are ripe for analysis. We discuss benefits of mapping a mouse brain at the level of synapses.

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    09/07/20 | A connectome and analysis of the adult central brain.
    Scheffer LK, Xu CS, Januszewski M, Lu Z, Takemura S, Hayworth KJ, Huang GB, Shinomiya K, Maitlin-Shepard J, Berg S, Clements J, Hubbard PM, Katz WT, Umayam L, Zhao T, Ackerman D, Blakely T, Bogovic J, Dolafi T, Kainmueller D, Kawase T, Khairy KA, Leavitt L, Li PH, Lindsey L, Neubarth N, Olbris DJ, Otsuna H, Trautman ET, Ito M, Bates AS, Goldammer J, Wolff T, Svirskas R, Schlegel P, Neace E, Knecht CJ, Alvarado CX, Bailey DA, Ballinger S, Borycz JA, Canino BS, Cheatham N, Cook M, Dreher M, Duclos O, Eubanks B, Fairbanks K, Finley S, Forknall N, Francis A, Hopkins GP, Joyce EM, Kim S, Kirk NA, Kovalyak J, Lauchie SA, Lohff A, Maldonado C, Manley EA, McLin S, Mooney C, Ndama M, Ogundeyi O, Okeoma N, Ordish C, Padilla N, Patrick CM, Paterson T, Phillips EE, Phillips EM, Rampally N, Ribeiro C, Robertson MK, Rymer JT, Ryan SM, Sammons M, Scott AK, Scott AL, Shinomiya A, Smith C, Smith K, Smith NL, Sobeski MA, Suleiman A, Swift J, Takemura S, Talebi I, Tarnogorska D, Tenshaw E, Tokhi T, Walsh JJ, Yang T, Horne JA, Li F, Parekh R, Rivlin PK, Jayaraman V, Costa M, Jefferis GS, Ito K, Saalfeld S, George R, Meinertzhagen IA, Rubin GM, Hess HF, Jain V, Plaza SM
    Elife. 2020 Sep 07;9:. doi: 10.7554/eLife.57443

    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's brain.

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