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8 Janelia Publications

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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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    06/01/23 | 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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    03/31/23 | Ascending neurons convey behavioral state to integrative sensory and action selection centers in the brain
    Chin-Lin Chen , Florian Aymanns , Ryo Minegishi , Victor D. V. Matsuda , Nicolas Talabot , Semih Günel , Barry J. Dickson , Pavan Ramdya
    Nature Neuroscience. 2023 Mar 31:. doi: 10.1038/s41593-023-01281-z

    Knowledge of one’s own behavioral state—whether one is walking, grooming, or resting—is critical for contextualizing sensory cues including interpreting visual motion and tracking odor sources. Additionally, awareness of one’s own posture is important to avoid initiating destabilizing or physically impossible actions. Ascending neurons (ANs), interneurons in the vertebrate spinal cord or insect ventral nerve cord (VNC) that project to the brain, may provide such high-fidelity behavioral state signals. However, little is known about what ANs encode and where they convey signals in any brain. To address this gap, we performed a large-scale functional screen of AN movement encoding, brain targeting, and motor system patterning in the adult fly, Drosophila melanogaster. Using a new library of AN sparse driver lines, we measured the functional properties of 247 genetically-identifiable ANs by performing two-photon microscopy recordings of neural activity in tethered, behaving flies. Quantitative, deep network-based neural and behavioral analyses revealed that ANs nearly exclusively encode high-level behaviors—primarily walking as well as resting and grooming—rather than low-level joint or limb movements. ANs that convey self-motion—resting, walking, and responses to gust-like puff stimuli—project to the brain’s anterior ventrolateral protocerebrum (AVLP), a multimodal, integrative sensory hub, while those that encode discrete actions—eye grooming, turning, and proboscis extension—project to the brain’s gnathal ganglion (GNG), a locus for action selection. The structure and polarity of AN projections within the VNC are predictive of their functional encoding and imply that ANs participate in motor computations while also relaying state signals to the brain. Illustrative of this are ANs that temporally integrate proboscis extensions over tens-of-seconds, likely through recurrent interconnectivity. Thus, in line with long-held theoretical predictions, ascending populations convey high-level behavioral state signals almost exclusively to brain regions implicated in sensory feature contextualization and action selection.

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    12/15/22 | Neural coding of distinct motor patterns during Drosophila courtship song
    Hiroshi M. Shiozaki , Kaiyu Wang , Joshua L. Lillvis , Min Xu , Barry J. Dickson , David L. Stern
    bioRxiv. 2022 Dec 15:. doi: 10.1101/2022.12.14.520499

    Animals flexibly switch between different actions by changing neural activity patterns for motor control. Courting Drosophila melanogaster males produce two different acoustic signals, pulse and sine song, each of which can be promoted by artificial activation of distinct neurons. However, how the activity of these neurons implements flexible song production is unknown. Here, we developed an assay to record neuronal calcium signals in the ventral nerve cord, which contains the song motor circuit, in singing flies. We found that sine-promoting neurons, but not pulse-promoting neurons, show strong activation during sine song. In contrast, both pulse- and sine-promoting neurons are active during pulse song. Furthermore, population calcium imaging in the song circuit suggests that sine song involves activation of a subset of neurons that are also active during pulse song. Thus, differential activation of overlapping, rather than distinct, neural populations underlies flexible motor actions during acoustic communication in D. melanogaster.

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    01/01/21 | Neural circuit mechanisms of sexual receptivity in Drosophila females.
    Wang K, Wang F, Forknall N, Yang T, Patrick C, Parekh R, Dickson BJ
    Nature. 2021 Jan 01;589(7843):577-81. 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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    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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