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9 Janelia Publications

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    03/20/24 | Motor neurons generate pose-targeted movements via proprioceptive sculpting.
    Gorko B, Siwanowicz I, Close K, Christoforou C, Hibbard KL, Kabra M, Lee A, Park J, Li SY, Chen AB, Namiki S, Chen C, Tuthill JC, Bock DD, Rouault H, Branson K, Ihrke G, Huston SJ
    Nature. 2024 Mar 20:. doi: 10.1038/s41586-024-07222-5

    Motor neurons are the final common pathway through which the brain controls movement of the body, forming the basic elements from which all movement is composed. Yet how a single motor neuron contributes to control during natural movement remains unclear. Here we anatomically and functionally characterize the individual roles of the motor neurons that control head movement in the fly, Drosophila melanogaster. Counterintuitively, we find that activity in a single motor neuron rotates the head in different directions, depending on the starting posture of the head, such that the head converges towards a pose determined by the identity of the stimulated motor neuron. A feedback model predicts that this convergent behaviour results from motor neuron drive interacting with proprioceptive feedback. We identify and genetically suppress a single class of proprioceptive neuron that changes the motor neuron-induced convergence as predicted by the feedback model. These data suggest a framework for how the brain controls movements: instead of directly generating movement in a given direction by activating a fixed set of motor neurons, the brain controls movements by adding bias to a continuing proprioceptive-motor loop.

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    09/18/23 | Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
    Yoshinori Aso , Daichi Yamada , Daniel Bushey , Karen Hibbard , Megan Sammons , Hideo Otsuna , Yichun Shuai , Toshihide Hige
    eLife. 2023 Sep 18:. doi: 10.7554/eLife.85756

    How memories are used by the brain to guide future action is poorly understood. In olfactory associative learning in Drosophila, multiple compartments of the mushroom body act in parallel to assign valence to a stimulus. Here, we show that appetitive memories stored in different compartments induce different levels of upwind locomotion. Using a photoactivation screen of a new collection of split-GAL4 drivers and EM connectomics, we identified a cluster of neurons postsynaptic to the mushroom body output neurons (MBONs) that can trigger robust upwind steering. These UpWind Neurons (UpWiNs) integrate inhibitory and excitatory synaptic inputs from MBONs of appetitive and aversive memory compartments, respectively. After training, disinhibition from the appetitive-memory MBONs enhances the response of UpWiNs to reward-predicting odors. Blocking UpWiNs impaired appetitive memory and reduced upwind locomotion during retrieval. Photoactivation of UpWiNs also increased the chance of returning to a location where activation was initiated, suggesting an additional role in olfactory navigation. Thus, our results provide insight into how learned abstract valences are gradually transformed into concrete memory-driven actions through divergent and convergent networks, a neuronal architecture that is commonly found in the vertebrate and invertebrate brains.

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    06/15/23 | Flexible specificity of memory in Drosophila depends on a comparison between choices
    Mehrab N Modi , Adithya Rajagopalan , Hervé Rouault , Yoshinori Aso , Glenn C Turner
    eLife. 2023 Jun 15:. doi: 10.7554/eLife.80923

    Memory guides behavior across widely varying environments and must therefore be both sufficiently specific and general. A memory too specific will be useless in even a slightly different environment, while an overly general memory may lead to suboptimal choices. Animals successfully learn to both distinguish between very similar stimuli and generalize across cues. Rather than forming memories that strike a balance between specificity and generality, Drosophila can flexibly categorize a given stimulus into different groups depending on the options available. We asked how this flexibility manifests itself in the well-characterized learning and memory pathways of the fruit fly. We show that flexible categorization in neuronal activity as well as behavior depends on the order and identity of the perceived stimuli. Our results identify the neural correlates of flexible stimulus-categorization in the fruit fly.

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    02/23/23 | A searchable image resource of Drosophila GAL4-driver expression patterns with single neuron resolution.
    Meissner GW, Nern A, Dorman Z, Depasquale GM, Forster K, Gibney T, Hausenfluck JH, He Y, Iyer NA, Jeter J, Johnson L, Johnston RM, Lee K, Melton B, Yarbrough B, Zugates CT, Clements J, Goina C, Otsuna H, Rokicki K, Svirskas RR, Aso Y, Card GM, Dickson BJ, Ehrhardt E, Goldammer J, Ito M, Kainmueller D, Korff W, Mais L, minegishi r, Namiki S, Rubin GM, Sterne GR, Wolff T, Malkesman O
    eLife. 2023 Feb 23;12:. doi: 10.7554/eLife.80660

    Precise, repeatable genetic access to specific neurons via GAL4/UAS and related methods is a key advantage of Drosophila neuroscience. Neuronal targeting is typically documented using light microscopy of full GAL4 expression patterns, which generally lack the single-cell resolution required for reliable cell type identification. Here we use stochastic GAL4 labeling with the MultiColor FlpOut approach to generate cellular resolution confocal images at large scale. We are releasing aligned images of 74,000 such adult central nervous systems. An anticipated use of this resource is to bridge the gap between neurons identified by electron or light microscopy. Identifying individual neurons that make up each GAL4 expression pattern improves the prediction of split-GAL4 combinations targeting particular neurons. To this end we have made the images searchable on the NeuronBridge website. We demonstrate the potential of NeuronBridge to rapidly and effectively identify neuron matches based on morphology across imaging modalities and datasets.

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    05/26/22 | One engram two readouts: stimulus dynamics switch a learned behavior in Drosophila
    Mehrab N Modi , Adithya Rajagopalan , Hervé Rouault , Yoshinori Aso , Glenn C Turner
    bioRxiv. 2022 May 26:. doi: 10.1101/2022.05.24.492551

    Memory guides the choices an animal makes across widely varying conditions in dynamic environments. Consequently, the most adaptive choice depends on the options available. How can a single memory support optimal behavior across different sets of choice options? We address this using olfactory learning in Drosophila. Even when we restrict an odor-punishment association to a single set of synapses using optogenetics, we find that flies still show choice behavior that depends on the options it encounters. Here we show that how the odor choices are presented to the animal influences memory recall itself. Presenting two similar odors in sequence enabled flies to not only discriminate them behaviorally but also at the level of neural activity. However, when the same odors were encountered as solitary stimuli, no such differences were detectable. These results show that memory recall is not simply a comparison to a static learned template, but can be adaptively modulated by stimulus dynamics.

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    11/03/20 | Cell types and neuronal circuitry underlying female aggression in Drosophila.
    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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    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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    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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    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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