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7 Janelia Publications

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    10/17/23 | A comprehensive neuroanatomical survey of the Drosophila Lobula Plate Tangential Neurons with predictions for their optic flow sensitivity.
    Arthur Zhao , Aljoscha Nern , Sanna Koskela , Marisa Dreher , Mert Erginkaya , Connor W Laughland , Henrique DF Ludwig , Alex G Thomson , Judith Hoeller , Ruchi Parekh , Sandro Romani , Davi D Bock , Eugenia Chiappe , Michael B Reiser
    bioRxiv. 2023 Oct 17:. doi: 10.1101/2023.10.16.562634

    Flying insects exhibit remarkable navigational abilities controlled by their compact nervous systems. Optic flow, the pattern of changes in the visual scene induced by locomotion, is a crucial sensory cue for robust self-motion estimation, especially during rapid flight. Neurons that respond to specific, large-field optic flow patterns have been studied for decades, primarily in large flies, such as houseflies, blowflies, and hover flies. The best-known optic-flow sensitive neurons are the large tangential cells of the dipteran lobula plate, whose visual-motion responses, and to a lesser extent, their morphology, have been explored using single-neuron neurophysiology. Most of these studies have focused on the large, Horizontal and Vertical System neurons, yet the lobula plate houses a much larger set of 'optic-flow' sensitive neurons, many of which have been challenging to unambiguously identify or to reliably target for functional studies. Here we report the comprehensive reconstruction and identification of the Lobula Plate Tangential Neurons in an Electron Microscopy (EM) volume of a whole Drosophila brain. This catalog of 58 LPT neurons (per brain hemisphere) contains many neurons that are described here for the first time and provides a basis for systematic investigation of the circuitry linking self-motion to locomotion control. Leveraging computational anatomy methods, we estimated the visual motion receptive fields of these neurons and compared their tuning to the visual consequence of body rotations and translational movements. We also matched these neurons, in most cases on a one-for-one basis, to stochastically labeled cells in genetic driver lines, to the mirror-symmetric neurons in the same EM brain volume, and to neurons in an additional EM data set. Using cell matches across data sets, we analyzed the integration of optic flow patterns by neurons downstream of the LPTs and find that most central brain neurons establish sharper selectivity for global optic flow patterns than their input neurons. Furthermore, we found that self-motion information extracted from optic flow is processed in distinct regions of the central brain, pointing to diverse foci for the generation of visual behaviors.

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    09/18/23 | Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
    Yoshinori Aso , Daichi Yamada , Daniel Bushey , Karen Hibbard , Megan Sammons , Hideo Otsuna , Yichun Shuai , Toshihide Hige
    eLife. 2023 Sep 18:. doi: 10.7554/eLife.85756

    How memories are used by the brain to guide future action is poorly understood. In olfactory associative learning in Drosophila, multiple compartments of the mushroom body act in parallel to assign valence to a stimulus. Here, we show that appetitive memories stored in different compartments induce different levels of upwind locomotion. Using a photoactivation screen of a new collection of split-GAL4 drivers and EM connectomics, we identified a cluster of neurons postsynaptic to the mushroom body output neurons (MBONs) that can trigger robust upwind steering. These UpWind Neurons (UpWiNs) integrate inhibitory and excitatory synaptic inputs from MBONs of appetitive and aversive memory compartments, respectively. After training, disinhibition from the appetitive-memory MBONs enhances the response of UpWiNs to reward-predicting odors. Blocking UpWiNs impaired appetitive memory and reduced upwind locomotion during retrieval. Photoactivation of UpWiNs also increased the chance of returning to a location where activation was initiated, suggesting an additional role in olfactory navigation. Thus, our results provide insight into how learned abstract valences are gradually transformed into concrete memory-driven actions through divergent and convergent networks, a neuronal architecture that is commonly found in the vertebrate and invertebrate brains.

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    09/07/23 | Combinatorial circuit dynamics orchestrate flexible motor patterns in Drosophila.
    Hiroshi M. Shiozaki , Kaiyu Wang , Joshua L. Lillvis , Min Xu , Barry J. Dickson , David L. Stern
    bioRxiv. 2023 Sep 07:. doi: 10.1101/2022.12.14.520499

    Motor systems flexibly implement diverse motor programs to pattern behavioral sequences, yet their neural underpinnings remain unclear. Here, we investigated the neural circuit mechanisms of flexible courtship behavior in Drosophila. Courting males alternately produce two types of courtship song. By recording calcium signals in the ventral nerve cord (VNC) in behaving flies, we found that different songs are produced by activating overlapping neural populations with distinct motor functions in a combinatorial manner. Recordings from the brain suggest that song is driven by two descending pathways – one defines when to sing and the other specifies what song to sing. Connectomic analysis reveals that these “when” and “what” descending pathways provide structured input to VNC neurons with different motor functions. These results suggest that dynamic changes in the activation patterns of descending pathways drive different combinations of motor modules, thereby flexibly switching between different motor actions.

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    09/01/23 | The Neural Basis of Drosophila Courtship Song
    Joshua L. Lillvis , Kaiyu Wang , Hiroshi M. Shiozaki , Min Xu , David L. Stern , Barry J. Dickson
    bioRxiv. 2023 Sep 01:. doi: 10.1101/2023.08.30.555537

    Animal sounds are produced by patterned vibrations of specific organs, but the neural circuits that drive these vibrations are not well defined in any animal. Here we provide a functional and synaptic map of most of the neurons in the Drosophila male ventral nerve cord (the analog of the vertebrate spinal cord) that drive complex, patterned song during courtship. Male Drosophila vibrate their wings toward females during courtship to produce two distinct song modes – pulse and sine song – with characteristic features that signal species identity and male quality. We identified song-producing neural circuits by optogenetically activating and inhibiting identified cell types in the ventral nerve cord (VNC) and by tracing their patterns of synaptic connectivity in the male VNC connectome. The core song circuit consists of at least eight cell types organized into overlapping circuits, where all neurons are required for pulse song and a subset are required for sine song. The pulse and sine circuits each include a feed-forward pathway from brain descending neurons to wing motor neurons, with extensive reciprocal and feed-back connections. We also identify specific neurons that shape the individual features of each song mode. These results reveal commonalities amongst diverse animals in the neural mechanisms that generate diverse motor patterns from a single set of muscles.

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    06/09/23 | Organization of an Ascending Circuit that Conveys Flight Motor State
    Han S. J. Cheong , Kaitlyn N. Boone , Marryn M. Bennett , Farzaan Salman , Jacob D. Ralston , Kaleb Hatch , Raven F. Allen , Alec M. Phelps , Andrew P. Cook , Jasper S. Phelps , Mert Erginkaya , Wei-Chung A. Lee , Gwyneth M. Card , Kevin C. Daly , Andrew M. Dacks
    bioRxiv. 2023 Jun 09:. doi: 10.1101/2023.06.07.544074

    Natural behaviors are a coordinated symphony of motor acts which drive self-induced or reafferent sensory activation. Single sensors only signal presence and magnitude of a sensory cue; they cannot disambiguate exafferent (externally-induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to make appropriate decisions and initiate adaptive behavioral outcomes. This is mediated by predictive motor signaling mechanisms, which emanate from motor control pathways to sensory processing pathways, but how predictive motor signaling circuits function at the cellular and synaptic level is poorly understood. We use a variety of techniques, including connectomics from both male and female electron microscopy volumes, transcriptomics, neuroanatomical, physiological and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs), which putatively provide predictive motor signals to several sensory and motor neuropil. Both AHN pairs receive input primarily from an overlapping population of descending neurons, many of which drive wing motor output. The two AHN pairs target almost exclusively non-overlapping downstream neural networks including those that process visual, auditory and mechanosensory information as well as networks coordinating wing, haltere, and leg motor output. These results support the conclusion that the AHN pairs multi-task, integrating a large amount of common input, then tile their output in the brain, providing predictive motor signals to non-overlapping sensory networks affecting motor control both directly and indirectly.

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    06/01/23 | Single-cell type analysis of wing premotor circuits in the ventral nerve cord of Drosophila melanogaster
    Erica Ehrhardt , Samuel C Whitehead , Shigehiro Namiki , Ryo Minegishi , Igor Siwanowicz , Kai Feng , Hideo Otsuna , FlyLight Project Team , Geoffrey W Meissner , David Stern , Jim Truman , David Shepherd , Michael H. Dickinson , Kei Ito , Barry J Dickson , Itai Cohen , Gwyneth M Card , Wyatt Korff
    bioRxiv. 2023 Jun 01:. doi: 10.1101/2023.05.31.542897

    To perform most behaviors, animals must send commands from higher-order processing centers in the brain to premotor circuits that reside in ganglia distinct from the brain, such as the mammalian spinal cord or insect ventral nerve cord. How these circuits are functionally organized to generate the great diversity of animal behavior remains unclear. An important first step in unraveling the organization of premotor circuits is to identify their constituent cell types and create tools to monitor and manipulate these with high specificity to assess their function. This is possible in the tractable ventral nerve cord of the fly. To generate such a toolkit, we used a combinatorial genetic technique (split-GAL4) to create 195 sparse driver lines targeting 198 individual cell types in the ventral nerve cord. These included wing and haltere motoneurons, modulatory neurons, and interneurons. Using a combination of behavioral, developmental, and anatomical analyses, we systematically characterized the cell types targeted in our collection. Taken together, the resources and results presented here form a powerful toolkit for future investigations of neural circuits and connectivity of premotor circuits while linking them to behavioral outputs.

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    02/23/23 | A searchable image resource of Drosophila GAL4-driver expression patterns with single neuron resolution.
    Meissner GW, Nern A, Dorman Z, Depasquale GM, Forster K, Gibney T, Hausenfluck JH, He Y, Iyer NA, Jeter J, Johnson L, Johnston RM, Lee K, Melton B, Yarbrough B, Zugates CT, Clements J, Goina C, Otsuna H, Rokicki K, Svirskas RR, Aso Y, Card GM, Dickson BJ, Ehrhardt E, Goldammer J, Ito M, Kainmueller D, Korff W, Mais L, minegishi r, Namiki S, Rubin GM, Sterne GR, Wolff T, Malkesman O
    eLife. 2023 Feb 23;12:. doi: 10.7554/eLife.80660

    Precise, repeatable genetic access to specific neurons via GAL4/UAS and related methods is a key advantage of Drosophila neuroscience. Neuronal targeting is typically documented using light microscopy of full GAL4 expression patterns, which generally lack the single-cell resolution required for reliable cell type identification. Here we use stochastic GAL4 labeling with the MultiColor FlpOut approach to generate cellular resolution confocal images at large scale. We are releasing aligned images of 74,000 such adult central nervous systems. An anticipated use of this resource is to bridge the gap between neurons identified by electron or light microscopy. Identifying individual neurons that make up each GAL4 expression pattern improves the prediction of split-GAL4 combinations targeting particular neurons. To this end we have made the images searchable on the NeuronBridge website. We demonstrate the potential of NeuronBridge to rapidly and effectively identify neuron matches based on morphology across imaging modalities and datasets.

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