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30 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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    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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    03/11/22 | Context-dependent control of behavior in Drosophila.
    Oram TB, Card GM
    Current Opinion in Neurobiology. 2022 Mar 11;73:102523. doi: 10.1016/j.conb.2022.02.003

    The representation of contextual information peripheral to a salient stimulus is central to an animal's ability to correctly interpret and flexibly respond to that stimulus. While the computations and circuits underlying the context-dependent modulation of stimulus-response pairings have typically been studied in vertebrates, the genetic tractability, numeric simplification, and well-characterized connectivity patterns of the Drosophila melanogaster brain have facilitated circuit-level insights into contextual processing. Recent studies in flies reveal the neuronal mechanisms that create flexible context-dependent behavioral responses to sensory events in conditions of predation threat, feeding regulation, and social interaction.

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    12/06/21 | Functional architecture of neural circuits for leg proprioception in Drosophila.
    Chen C, Agrawal S, Mark B, Mamiya A, Sustar A, Phelps JS, Lee WA, Dickson BJ, Card GM, Tuthill JC
    Current Biology. 2021 Dec 06;31(23):5163. doi: 10.1016/j.cub.2021.09.035

    To effectively control their bodies, animals rely on feedback from proprioceptive mechanosensory neurons. In the Drosophila leg, different proprioceptor subtypes monitor joint position, movement direction, and vibration. Here, we investigate how these diverse sensory signals are integrated by central proprioceptive circuits. We find that signals for leg joint position and directional movement converge in second-order neurons, revealing pathways for local feedback control of leg posture. Distinct populations of second-order neurons integrate tibia vibration signals across pairs of legs, suggesting a role in detecting external substrate vibration. In each pathway, the flow of sensory information is dynamically gated and sculpted by inhibition. Overall, our results reveal parallel pathways for processing of internal and external mechanosensory signals, which we propose mediate feedback control of leg movement and vibration sensing, respectively. The existence of a functional connectivity map also provides a resource for interpreting connectomic reconstruction of neural circuits for leg proprioception.

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    12/01/20 | Multi-regional circuits underlying visually guided decision-making in Drosophila.
    Cheong HS, Siwanowicz I, Card GM
    Current Opinion in Neurobiology. 2020 Dec 01;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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    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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    08/01/20 | Wiring patterns from auditory sensory neurons to the escape and song-relay pathways in fruit flies.
    Kim H, Horigome M, Ishikawa Y, Li F, Lauritzen JS, Card G, Bock DD, Kamikouchi A
    Journal of Comparative Neurology. 2020 Aug 01;528(12):2068. doi: 10.1002/cne.24877

    Many animals rely on acoustic cues to decide what action to take next. Unraveling the wiring patterns of the auditory neural pathways is prerequisite for understanding such information processing. Here we reconstructed the first step of the auditory neural pathway in the fruit fly brain, from primary to secondary auditory neurons, at the resolution of transmission electron microscopy. By tracing axons of two major subgroups of auditory sensory neurons in fruit flies, low-frequency tuned Johnston's organ (JO)-B neurons and high-frequency tuned JO-A neurons, we observed extensive connections from JO-B neurons to the main second-order neurons in both the song-relay and escape pathways. In contrast, JO-A neurons connected strongly to a neuron in the escape pathway. Our findings suggest that heterogeneous JO neuronal populations could be recruited to modify escape behavior whereas only specific JO neurons contribute to courtship behavior. We also found that all JO neurons have postsynaptic sites at their axons. Presynaptic modulation at the output sites of JO neurons could affect information processing of the auditory neural pathway in flies. This article is protected by copyright. All rights reserved.

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    03/27/20 | Unc-4 acts to promote neuronal identity and development of the take-off circuit in the Drosophila CNS.
    Lacin H, Williamson WR, Card GM, Skeath JB, Truman JW
    eLife. 2020 Mar 27;9:. doi: 10.7554/eLife.55007
    07/01/19 | State-dependent decoupling of sensory and motor circuits underlies behavioral flexibility in Drosophila.
    Ache JM, Namiki S, Lee A, Branson K, Card GM
    Nature Neuroscience. 2019 Jul 01;22(7):1132-1139. doi: 10.1038/s41593-019-0413-4

    An approaching predator and self-motion toward an object can generate similar looming patterns on the retina, but these situations demand different rapid responses. How central circuits flexibly process visual cues to activate appropriate, fast motor pathways remains unclear. Here we identify two descending neuron (DN) types that control landing and contribute to visuomotor flexibility in Drosophila. For each, silencing impairs visually evoked landing, activation drives landing, and spike rate determines leg extension amplitude. Critically, visual responses of both DNs are severely attenuated during non-flight periods, effectively decoupling visual stimuli from the landing motor pathway when landing is inappropriate. The flight-dependence mechanism differs between DN types. Octopamine exposure mimics flight effects in one, whereas the other probably receives neuronal feedback from flight motor circuits. Thus, this sensorimotor flexibility arises from distinct mechanisms for gating action-specific descending pathways, such that sensory and motor networks are coupled or decoupled according to the behavioral state.

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