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9 Publications

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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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    03/14/22 | A population of descending neurons that regulates the flight motor of Drosophila.
    Namiki S, Ros IG, Morrow C, Rowell WJ, Card GM, Korff W, Dickinson MH
    Current Biology. 2022 Mar 14;32(5):1189-1196. doi: 10.1016/j.cub.2022.01.008

    Similar to many insect species, Drosophila melanogaster is capable of maintaining a stable flight trajectory for periods lasting up to several hours. Because aerodynamic torque is roughly proportional to the fifth power of wing length, even small asymmetries in wing size require the maintenance of subtle bilateral differences in flapping motion to maintain a stable path. Flies can even fly straight after losing half of a wing, a feat they accomplish via very large, sustained kinematic changes to both the damaged and intact wings. Thus, the neural network responsible for stable flight must be capable of sustaining fine-scaled control over wing motion across a large dynamic range. In this study, we describe an unusual type of descending neuron (DNg02) that projects directly from visual output regions of the brain to the dorsal flight neuropil of the ventral nerve cord. Unlike many descending neurons, which exist as single bilateral pairs with unique morphology, there is a population of at least 15 DNg02 cell pairs with nearly identical shape. By optogenetically activating different numbers of DNg02 cells, we demonstrate that these neurons regulate wingbeat amplitude over a wide dynamic range via a population code. Using two-photon functional imaging, we show that DNg02 cells are responsive to visual motion during flight in a manner that would make them well suited to continuously regulate bilateral changes in wing kinematics. Collectively, we have identified a critical set of descending neurons that provides the sensitivity and dynamic range required for flight control.

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    11/17/20 | Multi-regional circuits underlying visually guided decision-making in Drosophila.
    Cheong H, Siwanowicz I, Card GM
    Current Opinion in Neurobiology. 2020 Nov 17;65:77-87. doi: 10.1016/j.conb.2020.10.010

    Visually guided decision-making requires integration of information from distributed brain areas, necessitating a brain-wide approach to examine its neural mechanisms. New tools in Drosophila melanogaster enable circuits spanning the brain to be charted with single cell-type resolution. Here, we highlight recent advances uncovering the computations and circuits that transform and integrate visual information across the brain to make behavioral choices. Visual information flows from the optic lobes to three primary central brain regions: a sensorimotor mapping area and two 'higher' centers for memory or spatial orientation. Rapid decision-making during predator evasion emerges from the spike timing dynamics in parallel sensorimotor cascades. Goal-directed decisions may occur through memory, navigation and valence processing in the central complex and mushroom bodies.

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    09/09/20 | A systematic nomenclature for the Drosophila ventral nerve cord.
    Court R, Namiki S, Armstrong JD, Borner J, Card G, Costa M, Dickinson M, Duch C, Korff W, Mann R, Merritt D, Murphey RK, Seeds AM, Shirangi T, Simpson JH, Truman JW, Tuthill JC, Williams DW, Shepherd D
    Neuron. 2020 Sep 14;107(6):1071-79. doi: 10.1016/j.neuron.2020.08.005

    Drosophila melanogaster is an established model for neuroscience research with relevance in biology and medicine. Until recently, research on the Drosophila brain was hindered by the lack of a complete and uniform nomenclature. Recognizing this, Ito et al. (2014) produced an authoritative nomenclature for the adult insect brain, using Drosophila as the reference. Here, we extend this nomenclature to the adult thoracic and abdominal neuromeres, the ventral nerve cord (VNC), to provide an anatomical description of this major component of the Drosophila nervous system. The VNC is the locus for the reception and integration of sensory information and involved in generating most of the locomotor actions that underlie fly behaviors. The aim is to create a nomenclature, definitions, and spatial boundaries for the Drosophila VNC that are consistent with other insects. The work establishes an anatomical framework that provides a powerful tool for analyzing the functional organization of the VNC.

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    09/12/18 | Speed dependent descending control of freezing behavior in Drosophila melanogaster.
    Zacarias R, Namiki S, Card GM, Vasconcelos ML, Moita MA
    Nature Communications. 2018 Sep 12;9(1):3697. doi: 10.1038/s41467-018-05875-1

    The most fundamental choice an animal has to make when it detects a threat is whether to freeze, reducing its chances of being noticed, or to flee to safety. Here we show that Drosophila melanogaster exposed to looming stimuli in a confined arena either freeze or flee. The probability of freezing versus fleeing is modulated by the fly's walking speed at the time of threat, demonstrating that freeze/flee decisions depend on behavioral state. We describe a pair of descending neurons crucially implicated in freezing. Genetic silencing of DNp09 descending neurons disrupts freezing yet does not prevent fleeing. Optogenetic activation of both DNp09 neurons induces running and freezing in a state-dependent manner. Our findings establish walking speed as a key factor in defensive response choices and reveal a pair of descending neurons as a critical component in the circuitry mediating selection and execution of freezing or fleeing behaviors.

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    12/09/17 | Optogenetic dissection of descending behavioral control in Drosophila.
    Cande J, Namiki S, Qiu J, Korff W, Card GM, Shaevitz JW, Stern DL, Berman GJ
    eLife. 2018:e34275. doi: 10.7554/eLife.34275

    In most animals, the brain makes behavioral decisions that are transmitted by descending neurons to the nerve cord circuitry that produces behaviors. In insects, only a few descending neurons have been associated with specific behaviors. To explore how descending neurons control an insect's movements, we developed a novel method to systematically assay the behavioral effects of activating individual neurons on freely behaving terrestrial D. melanogaster. We calculated a two-dimensional representation of the entire behavior space explored by these flies and we associated descending neurons with specific behaviors by identifying regions of this space that were visited with increased frequency during optogenetic activation. Applying this approach across a large collection of descending neurons, we found that (1) activation of most of the descending neurons drove stereotyped behaviors, (2) in many cases multiple descending neurons activated similar behaviors, and (3) optogenetically-activated behaviors were often dependent on the behavioral state prior to activation.

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    06/26/18 | The functional organization of descending sensory-motor pathways in Drosophila.
    Namiki S, Dickinson MH, Wong AM, Korff W, Card GM
    eLife. 2018 Jun 26:e34272. doi: 10.7554/eLife.34272

    In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in Drosophila melanogaster and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all Drosophila DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly's capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.

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    04/26/17 | A systematic nomenclature for the Drosophila ventral nervous system.
    Court RC, Armstrong JD, Borner J, Card GM, Costa M, Dickinson MH, Duch C, Korff W, Mann RS, Merritt D, Murphey RK, Namiki S, Seeds AM, Shepherd D, Shirangi TR, Simpson JH, Truman JW, Tuthill JC, Williams DW
    bioRxiv. 2017 Apr 26:. doi: 10.1101/122952

    Insect nervous systems are proven and powerful model systems for neuroscience research with wide relevance in biology and medicine. However, descriptions of insect brains have suffered from a lack of a complete and uniform nomenclature. Recognising this problem the Insect Brain Name Working Group produced the first agreed hierarchical nomenclature system for the adult insect brain, using Drosophila melanogaster as the reference framework, with other insect taxa considered to ensure greater consistency and expandability (Ito et al., 2014). Ito et al. (2014) purposely focused on the gnathal regions that account for approximately 50% of the adult CNS. We extend this nomenclature system to the sub-gnathal regions of the adult Drosophila nervous system to provide a nomenclature of the so-called ventral nervous system (VNS), which includes the thoracic and abdominal neuromeres that was not included in the original work and contains the neurons that play critical roles underpinning most fly behaviours.

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