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9 Janelia Publications

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    11/03/20 | Cell types and neuronal circuitry underlying female aggression in .
    Schretter CE, Aso Y, Robie AA, Dreher M, Dolan M, Chen N, Ito M, Yang T, Parekh R, Branson KM, Rubin GM
    eLife. 2020 Nov 03;9:. doi: 10.7554/eLife.58942

    Aggressive social interactions are used to compete for limited resources and are regulated by complex sensory cues and the organism's internal state. While both sexes exhibit aggression, its neuronal underpinnings are understudied in females. Here, we identify a population of sexually dimorphic aIPg neurons in the adult central brain whose optogenetic activation increased, and genetic inactivation reduced, female aggression. Analysis of GAL4 lines identified in an unbiased screen for increased female chasing behavior revealed the involvement of another sexually dimorphic neuron, pC1d, and implicated aIPg and pC1d neurons as core nodes regulating female aggression. Connectomic analysis demonstrated that aIPg neurons and pC1d are interconnected and suggest that aIPg neurons may exert part of their effect by gating the flow of visual information to descending neurons. Our work reveals important regulatory components of the neuronal circuitry that underlies female aggressive social interactions and provides tools for their manipulation.

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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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    11/14/19 | Nitric oxide acts as a cotransmitter in a subset of dopaminergic neurons to diversify memory dynamics.
    Aso Y, Ray RP, Long X, Bushey D, Cichewicz K, Ngo T, Sharp B, Christoforou C, Hu A, Lemire AL, Tillberg P, Hirsh J, Litwin-Kumar A, Rubin GM
    eLife. 2019 Nov 14;8:. doi: 10.7554/eLife.49257

    Animals employ diverse learning rules and synaptic plasticity dynamics to record temporal and statistical information about the world. However, the molecular mechanisms underlying this diversity are poorly understood. The anatomically defined compartments of the insect mushroom body function as parallel units of associative learning, with different learning rates, memory decay dynamics and flexibility (Aso & Rubin 2016). Here we show that nitric oxide (NO) acts as a neurotransmitter in a subset of dopaminergic neurons in . NO's effects develop more slowly than those of dopamine and depend on soluble guanylate cyclase in postsynaptic Kenyon cells. NO acts antagonistically to dopamine; it shortens memory retention and facilitates the rapid updating of memories. The interplay of NO and dopamine enables memories stored in local domains along Kenyon cell axons to be specialized for predicting the value of odors based only on recent events. Our results provide key mechanistic insights into how diverse memory dynamics are established in parallel memory systems.

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    10/15/19 | The yellow gene influences Drosophila male mating success through sex comb melanization.
    Massey JH, Chung D, Siwanowicz I, Stern DL, Wittkopp PJ
    eLife. 2019 Oct 15;8:. doi: 10.7554/eLife.49388

    males perform a series of courtship behaviors that, when successful, result in copulation with a female. For over a century, mutations in the gene, named for its effects on pigmentation, have been known to reduce male mating success. Prior work has suggested that influences mating behavior through effects on wing extension, song, and/or courtship vigor. Here, we rule out these explanations, as well as effects on the nervous system more generally, and find instead that the effects of on male mating success are mediated by its effects on pigmentation of male-specific leg structures called sex combs. Loss of expression in these modified bristles reduces their melanization, which changes their structure and causes difficulty grasping females prior to copulation. These data illustrate why the mechanical properties of anatomy, not just neural circuitry, must be considered to fully understand the development and evolution of behavior.

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    05/21/19 | Neurogenetic dissection of the lateral horn reveals major outputs, diverse behavioural functions, and interactions with the mushroom body.
    Dolan M, Frechter S, Bates AS, Dan C, Huoviala P, Roberts RJ, Schlegel P, Dhawan S, Tabano R, Dionne H, Christoforou C, Close K, Sutcliffe B, Giuliani B, Li F, Costa M, Ihrke G, Meissner GW, Bock DD, Aso Y, Rubin GM, Jefferis GS
    Elife. 2019 May 21;8:. doi: 10.7554/eLife.43079

    Animals exhibit innate behaviours to a variety of sensory stimuli including olfactory cues. In , one higher olfactory centre, the lateral horn (LH), is implicated in innate behaviour. However, our structural and functional understanding of the LH is scant, in large part due to a lack of sparse neurogenetic tools for this region. We generate a collection of split-GAL4 driver lines providing genetic access to 82 LH cell types. We use these to create an anatomical and neurotransmitter map of the LH and link this to EM connectomics data. We find ~30% of LH projections converge with outputs from the mushroom body, site of olfactory learning and memory. Using optogenetic activation, we identify LH cell types that drive changes in valence behavior or specific locomotor programs. In summary, we have generated a resource for manipulating and mapping LH neurons, providing new insights into the circuit basis of innate and learned olfactory behavior.

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    01/09/19 | Comparisons between the ON- and OFF-edge motion pathways in the brain.
    Shinomiya K, Huang G, Lu Z, Parag T, Xu CS, Aniceto R, Ansari N, Cheatham N, Lauchie S, Neace E, Ogundeyi O, Ordish C, Peel D, Shinomiya A, Smith C, Takemura S, Talebi I, Rivlin PK, Nern A, Scheffer LK, Plaza SM, Meinertzhagen IA
    eLife. 2019 Jan 09;8:. doi: 10.7554/eLife.40025

    Understanding the circuit mechanisms behind motion detection is a long-standing question in visual neuroscience. In , recent synapse-level connectomes in the optic lobe, particularly in ON-pathway (T4) receptive-field circuits, in concert with physiological studies, suggest an increasingly intricate motion model compared with the ubiquitous Hassenstein-Reichardt model, while our knowledge of OFF-pathway (T5) has been incomplete. Here we present a conclusive and comprehensive connectome that for the first time integrates detailed connectivity information for inputs to both T4 and T5 pathways in a single EM dataset covering the entire optic lobe. With novel reconstruction methods using automated synapse prediction suited to such a large connectome, we successfully corroborate previous findings in the T4 pathway and comprehensively identify inputs and receptive fields for T5. While the two pathways are likely evolutionarily linked and indeed exhibit many similarities, we uncover interesting differences and interactions that may underlie their distinct functional properties.

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    04/10/17 | Stem cell-intrinsic, seven-up-triggered temporal factor gradients diversify intermediate neural progenitors.
    Ren Q, Yang C, Liu Z, Sugino K, Mok K, He Y, Ito M, Nern A, Otsuna H, Lee T
    Current Biology : CB. 2017 Apr 10;27(9):1303-13. doi: 10.1016/j.cub.2017.03.047

    Building a sizable, complex brain requires both cellular expansion and diversification. One mechanism to achieve these goals is production of multiple transiently amplifying intermediate neural progenitors (INPs) from a single neural stem cell. Like mammalian neural stem cells, Drosophila type II neuroblasts utilize INPs to produce neurons and glia. Within a given lineage, the consecutively born INPs produce morphologically distinct progeny, presumably due to differential inheritance of temporal factors. To uncover the underlying temporal fating mechanisms, we profiled type II neuroblasts' transcriptome across time. Our results reveal opposing temporal gradients of Imp and Syp RNA-binding proteins (descending and ascending, respectively). Maintaining high Imp throughout serial INP production expands the number of neurons and glia with early temporal fate at the expense of cells with late fate. Conversely, precocious upregulation of Syp reduces the number of cells with early fate. Furthermore, we reveal that the transcription factor Seven-up initiates progression of the Imp/Syp gradients. Interestingly, neuroblasts that maintain initial Imp/Syp levels can still yield progeny with a small range of early fates. We therefore propose that the Seven-up-initiated Imp/Syp gradients create coarse temporal windows within type II neuroblasts to pattern INPs, which subsequently undergo fine-tuned subtemporal patterning.

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    11/16/15 | Propagation of homeostatic sleep signals by segregated synaptic microcircuits of the Drosophila mushroom body.
    Sitaraman D, Aso Y, Jin X, Chen N, Felix M, Rubin GM, Nitabach MN
    Current Biology : CB. 2015 Nov 16;25(22):2915-27. doi: 10.1016/j.cub.2015.09.017

    The Drosophila mushroom body (MB) is a key associative memory center that has also been implicated in the control of sleep. However, the identity of MB neurons underlying homeostatic sleep regulation, as well as the types of sleep signals generated by specific classes of MB neurons, has remained poorly understood. We recently identified two MB output neuron (MBON) classes whose axons convey sleep control signals from the MB to converge in the same downstream target region: a cholinergic sleep-promoting MBON class and a glutamatergic wake-promoting MBON class. Here, we deploy a combination of neurogenetic, behavioral, and physiological approaches to identify and mechanistically dissect sleep-controlling circuits of the MB. Our studies reveal the existence of two segregated excitatory synaptic microcircuits that propagate homeostatic sleep information from different populations of intrinsic MB "Kenyon cells" (KCs) to specific sleep-regulating MBONs: sleep-promoting KCs increase sleep by preferentially activating the cholinergic MBONs, while wake-promoting KCs decrease sleep by preferentially activating the glutamatergic MBONs. Importantly, activity of the sleep-promoting MB microcircuit is increased by sleep deprivation and is necessary for homeostatic rebound sleep (i.e., the increased sleep that occurs after, and in compensation for, sleep lost during deprivation). These studies reveal for the first time specific functional connections between subsets of KCs and particular MBONs and establish the identity of synaptic microcircuits underlying transmission of homeostatic sleep signals in the MB.

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