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25 Janelia Publications

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    12/02/20 | Distributed control of motor circuits for backward walking in Drosophila.
    Feng K, Sen R, minegishi r, Dübbert M, Bockemühl T, Büschges A, Dickson BJ
    Nature Communications. 2020 Dec 02;11(1):6166. doi: 10.1038/s41467-020-19936-x

    How do descending inputs from the brain control leg motor circuits to change how an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response. The Drosophila Moonwalker Descending Neurons (MDNs), which alter leg motor circuit dynamics so that the fly walks backwards, exemplify the command-type mechanism. Here, we identify several dozen MDN target neurons within the leg motor circuits, and show that two of them mediate distinct and highly-specific changes in leg muscle activity during backward walking: LBL40 neurons provide the hindleg power stroke during stance phase; LUL130 neurons lift the legs at the end of stance to initiate swing. Through these two effector neurons, MDN directly controls both the stance and swing phases of the backward stepping cycle. These findings suggest that command-type descending neurons can also operate through the distributed control of local motor circuits.

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    11/25/20 | Neural circuit mechanisms of sexual receptivity in Drosophila females.
    Wang K, Wang F, Forknall N, Yang T, Patrick C, Parekh R, Dickson BJ
    Nature. 2020 Nov 25:. doi: 10.1038/s41586-020-2972-7

    Choosing a mate is one of the most consequential decisions a female will make during her lifetime. A female fly signals her willingness to mate by opening her vaginal plates, allowing a courting male to copulate. Vaginal plate opening (VPO) occurs in response to the male courtship song and is dependent on the mating status of the female. How these exteroceptive (song) and interoceptive (mating status) inputs are integrated to regulate VPO remains unknown. Here we characterize the neural circuitry that implements mating decisions in the brain of female Drosophila melanogaster. We show that VPO is controlled by a pair of female-specific descending neurons (vpoDNs). The vpoDNs receive excitatory input from auditory neurons (vpoENs), which are tuned to specific features of the D. melanogaster song, and from pC1 neurons, which encode the mating status of the female. The song responses of vpoDNs, but not vpoENs, are attenuated upon mating, accounting for the reduced receptivity of mated females. This modulation is mediated by pC1 neurons. The vpoDNs thus directly integrate the external and internal signals that control the mating decisions of Drosophila females.

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    10/05/20 | Circuit and behavioral mechanisms of sexual rejection by drosophila females.
    Wang F, Wang K, Forknall N, Parekh R, Dickson BJ
    Current Biology. 2020 Oct 05;30(19):. doi: 10.1016/j.cub.2020.07.083

    The mating decisions of Drosophila melanogaster females are primarily revealed through either of two discrete actions: opening of the vaginal plates to allow copulation, or extrusion of the ovipositor to reject the male. Both actions are triggered by the male courtship song, and both are dependent upon the female's mating status. Virgin females are more likely to open their vaginal plates in response to song; mated females are more likely to extrude their ovipositor. Here, we examine the neural cause and behavioral consequence of ovipositor extrusion. We show that the DNp13 descending neurons act as command-type neurons for ovipositor extrusion, and that ovipositor extrusion is an effective deterrent only when performed by females that have previously mated. The DNp13 neurons respond to male song via direct synaptic input from the pC2l auditory neurons. Mating status does not modulate the song responses of DNp13 neurons, but rather how effectively they can engage the motor circuits for ovipositor extrusion. We present evidence that mating status information is mediated by ppk sensory neurons in the uterus, which are activated upon ovulation. Vaginal plate opening and ovipositor extrusion are thus controlled by anatomically and functionally distinct circuits, highlighting the diversity of neural decision-making circuits even in the context of closely related behaviors with shared exteroceptive and interoceptive inputs.

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    06/25/20 | Controlling motor neurons of every muscle for fly proboscis reaching.
    McKellar CE, Siwanowicz I, Dickson BJ, Simpson JH
    eLife. 2020 Jun 25;9:. doi: 10.7554/eLife.54978

    We describe the anatomy of all the primary motor neurons in the fly proboscis and characterize their contributions to its diverse reaching movements. Pairing this behavior with the wealth of genetic tools offers the possibility to study motor control at single-neuron resolution, and soon throughout entire circuits. As an entry to these circuits, we provide detailed anatomy of proboscis motor neurons, muscles, and joints. We create a collection of fly strains to individually manipulate every proboscis muscle through control of its motor neurons, the first such collection for an appendage. We generate a model of the action of each proboscis joint, and find that only a small number of motor neurons are needed to produce proboscis reaching. Comprehensive control of each motor element in this numerically simple system paves the way for future study of both reflexive and flexible movements of this appendage.

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    03/02/20 | Neural circuitry linking mating and egg laying in Drosophila females.
    Wang F, Wang K, Forknall N, Patrick C, Yang T, Parekh R, Bock D, Dickson BJ
    Nature. 2020 Mar 02;579(7797):101-105. doi: 10.1038/s41586-020-2055-9

    Mating and egg laying are tightly cooordinated events in the reproductive life of all oviparous females. Oviposition is typically rare in virgin females but is initiated after copulation. Here we identify the neural circuitry that links egg laying to mating status in Drosophila melanogaster. Activation of female-specific oviposition descending neurons (oviDNs) is necessary and sufficient for egg laying, and is equally potent in virgin and mated females. After mating, sex peptide-a protein from the male seminal fluid-triggers many behavioural and physiological changes in the female, including the onset of egg laying. Sex peptide is detected by sensory neurons in the uterus, and silences these neurons and their postsynaptic ascending neurons in the abdominal ganglion. We show that these abdominal ganglion neurons directly activate the female-specific pC1 neurons. GABAergic (γ-aminobutyric-acid-releasing) oviposition inhibitory neurons (oviINs) mediate feed-forward inhibition from pC1 neurons to both oviDNs and their major excitatory input, the oviposition excitatory neurons (oviENs). By attenuating the abdominal ganglion inputs to pC1 neurons and oviINs, sex peptide disinhibits oviDNs to enable egg laying after mating. This circuitry thus coordinates the two key events in female reproduction: mating and egg laying.

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    11/22/19 | TwoLumps ascending neurons mediate touch-evoked reversal of walking direction in Drosophila.
    Sen R, Wang K, Dickson BJ
    Current Biology. 2019 Nov 22;29(24):4337-44. doi: 10.1016/j.cub.2019.11.004

    External cues, including touch, enable walking animals to flexibly maneuver around obstacles and extricate themselves from dead-ends (for reviews, see [1-3]). In a screen for neurons that enable Drosophila melanogaster to retreat when it encounters a dead-end, we identified a pair of ascending neurons, the TwoLumps Ascending (TLA) neurons. Silencing TLA activity impairs backward locomotion, whereas optogenetic activation triggers backward walking. TLA-induced reversal is mediated in part by the Moonwalker Descending Neurons (MDNs) [4], which receive excitatory input from the TLAs. Silencing the TLAs decreases the extent to which freely walking flies back up upon encountering a physical barrier in the dark, and TLAs show calcium responses to optogenetic activation of neurons expressing the mechanosensory channel NOMPC. We infer that TLAs convey feedforward mechanosensory stimuli to transiently activate MDNs in response to anterior body touch.

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    07/06/19 | Cellular level analysis of the locomotor neural circuits in Drosophila melanogaster.
    minegishi r, Feng K, Dickson B
    Biomimetic and Biohybrid Systems. 2019 Jul 6:334-7
    03/12/19 | Split-QF system for fine-tuned transgene expression in Drosophila.
    Riabinina O, Vernon SW, Dickson BJ, Baines RA
    Genetics. 2019 Mar 12;212(1):53-63. doi: 10.1534/genetics.119.302034

    The Q-system is a binary expression system that works well across species. Here we report the development and demonstrate applications of a split-QF system that drives strong expression in , is repressible by QS and inducible by a small non-toxic molecule quinic acid. The split-QF system is fully compatible with existing split-GAL4 and split-LexA lines, thus greatly expanding the range of possible advanced intersectional experiments and anatomical, physiological and behavioural assays in and in other organisms.

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    03/08/19 | Neural evolution of context-dependent fly song.
    Ding Y, Lillvis JL, Cande J, Berman GJ, Arthur BJ, Long X, Xu M, Dickson BJ, Stern DL
    Current Biology : CB. 2019 Mar 08;29(7):1089-99. doi: 10.1016/j.cub.2019.02.019

    It is unclear where in the nervous system evolutionary changes tend to occur. To localize the source of neural evolution that has generated divergent behaviors, we developed a new approach to label and functionally manipulate homologous neurons across Drosophila species. We examined homologous descending neurons that drive courtship song in two species that sing divergent song types and localized relevant evolutionary changes in circuit function downstream of the intrinsic physiology of these descending neurons. This evolutionary change causes different species to produce divergent motor patterns in similar social contexts. Artificial stimulation of these descending neurons drives multiple song types, suggesting that multifunctional properties of song circuits may facilitate rapid evolution of song types.

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    01/07/19 | Threshold-based ordering of sequential actions during Drosophila courtship.
    McKellar CE, Lillvis JL, Bath DE, Fitzgerald JE, Cannon JG, Simpson JH, Dickson BJ
    Current Biology : CB. 2019 Jan 07;29(3):426-34. doi: 10.1016/j.cub.2018.12.019

    Goal-directed animal behaviors are typically composed of sequences of motor actions whose order and timing are critical for a successful outcome. Although numerous theoretical models for sequential action generation have been proposed, few have been supported by the identification of control neurons sufficient to elicit a sequence. Here, we identify a pair of descending neurons that coordinate a stereotyped sequence of engagement actions during Drosophila melanogaster male courtship behavior. These actions are initiated sequentially but persist cumulatively, a feature not explained by existing models of sequential behaviors. We find evidence consistent with a ramp-to-threshold mechanism, in which increasing neuronal activity elicits each action independently at successively higher activity thresholds.

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