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7 Janelia Publications

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    09/16/23 | Driver lines for studying associative learning in Drosophila
    Yichun Shuai , Megan Sammons , Gabriella Sterne , Karen Hibbard , He Yang , Ching-Po Yang , Claire Managan , Igor Siwanowicz , Tzumin Lee , Gerald M. Rubin , Glenn Turner , Yoshinori Aso
    bioRxiv. 2023 Sep 16:. doi: 10.1101/2023.09.15.557808

    The mushroom body (MB) is the center for associative learning in insects. In Drosophila, intersectional split-GAL4 drivers and electron microscopy (EM) connectomes have laid the foundation for precise interrogation of the MB neural circuits. However, many cell types upstream and downstream of the MB remained to be investigated due to lack of driver lines. Here we describe a new collection of over 800 split-GAL4 and split-LexA drivers that cover approximately 300 cell types, including sugar sensory neurons, putative nociceptive ascending neurons, olfactory and thermo-/hygro-sensory projection neurons, interneurons connected with the MB-extrinsic neurons, and various other cell types. We characterized activation phenotypes for a subset of these lines and identified the sugar sensory neuron line most suitable for reward substitution. Leveraging the thousands of confocal microscopy images associated with the collection, we analyzed neuronal morphological stereotypy and discovered that one set of mushroom body output neurons, MBON08/MBON09, exhibits striking individuality and asymmetry across animals. In conjunction with the EM connectome maps, the driver lines reported here offer a powerful resource for functional dissection of neural circuits for associative learning in adult Drosophila.

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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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    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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    07/18/17 | A connectome of a learning and memory center in the adult Drosophila brain.
    Takemura S, Aso Y, Hige T, Wong AM, Lu Z, Xu CS, Rivlin PK, Hess HF, Zhao T, Parag T, Berg S, Huang G, Katz WT, Olbris DJ, Plaza SM, Umayam LA, Aniceto R, Chang L, Lauchie S, et al
    eLife. 2017 Jul 18;6:e26975. doi: 10.7554/eLife.26975

    Understanding memory formation, storage and retrieval requires knowledge of the underlying neuronal circuits. In Drosophila, the mushroom body (MB) is the major site of associative learning. We reconstructed the morphologies and synaptic connections of all 983 neurons within the three functional units, or compartments, that compose the adult MB’s α lobe, using a dataset of isotropic 8-nm voxels collected by focused ion-beam milling scanning electron microscopy. We found that Kenyon cells (KCs), whose sparse activity encodes sensory information, each make multiple en passant synapses to MB output neurons (MBONs) in each compartment. Some MBONs have inputs from all KCs, while others differentially sample sensory modalities. Only six percent of KC>MBON synapses receive a direct synapse from a dopaminergic neuron (DAN). We identified two unanticipated classes of synapses, KC>DAN and DAN>MBON. DAN activation produces a slow depolarization of the MBON in these DAN>MBON synapses and can weaken memory recall.

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    04/15/16 | Direct neural pathways convey distinct visual information to Drosophila mushroom bodies.
    Vogt K, Aso Y, Hige T, Knapek S, Ichinose T, Friedrich AB, Turner GC, Rubin GM, Tanimoto H
    eLife. 2016 Apr 15;5:e14009. doi: 10.7554/eLife.14009

    Previously, we identified that visual and olfactory associative memories of Drosophila share the mushroom body (MB) circuits (Vogt et al. 2014). Despite well-characterized odor representations in the Drosophila MB, the MB circuit for visual information is totally unknown. Here we show that a small subset of MB Kenyon cells (KCs) selectively responds to visual but not olfactory stimulation. The dendrites of these atypical KCs form a ventral accessory calyx (vAC), distinct from the main calyx that receives olfactory input. We identified two types of visual projection neurons (VPNs) directly connecting the optic lobes and the vAC. Strikingly, these VPNs are differentially required for visual memories of color and brightness. The segregation of visual and olfactory domains in the MB allows independent processing of distinct sensory memories and may be a conserved form of sensory representations among insects.

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    12/02/15 | Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila
    Hige T, Aso Y, Modi M, Rubin GM, Turner GC
    Neuron. 2015 Dec 2;88(5):985-98. doi: 10.1016/j.neuron.2015.11.003

    Although associative learning has been localized to specific brain areas in many animals, identifying the underlying synaptic processes in vivo has been difficult. Here, we provide the first demonstration of long-term synaptic plasticity at the output site of the Drosophila mushroom body. Pairing an odor with activation of specific dopamine neurons induces both learning and odor-specific synaptic depression. The plasticity induction strictly depends on the temporal order of the two stimuli, replicating the logical requirement for associative learning. Furthermore, we reveal that dopamine action is confined to and distinct across different anatomical compartments of the mushroom body lobes. Finally, we find that overlap between sparse representations of different odors defines both stimulus specificity of the plasticity and generalizability of associative memories across odors. Thus, the plasticity we find here not only manifests important features of associative learning but also provides general insights into how a sparse sensory code is read out.

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    10/08/15 | Plasticity-driven individualization of olfactory coding in mushroom body output neurons.
    Hige T, Aso Y, Rubin GM, Turner GC
    Nature. 2015 Oct 8;526(7572):258-62. doi: 10.1038/nature15396

    Although all sensory circuits ascend to higher brain areas where stimuli are represented in sparse, stimulus-specific activity patterns, relatively little is known about sensory coding on the descending side of neural circuits, as a network converges. In insects, mushroom bodies have been an important model system for studying sparse coding in the olfactory system, where this format is important for accurate memory formation. In Drosophila, it has recently been shown that the 2,000 Kenyon cells of the mushroom body converge onto a population of only 34 mushroom body output neurons (MBONs), which fall into 21 anatomically distinct cell types. Here we provide the first, to our knowledge, comprehensive view of olfactory representations at the fourth layer of the circuit, where we find a clear transition in the principles of sensory coding. We show that MBON tuning curves are highly correlated with one another. This is in sharp contrast to the process of progressive decorrelation of tuning in the earlier layers of the circuit. Instead, at the population level, odour representations are reformatted so that positive and negative correlations arise between representations of different odours. At the single-cell level, we show that uniquely identifiable MBONs display profoundly different tuning across different animals, but that tuning of the same neuron across the two hemispheres of an individual fly was nearly identical. Thus, individualized coordination of tuning arises at this level of the olfactory circuit. Furthermore, we find that this individualization is an active process that requires a learning-related gene, rutabaga. Ultimately, neural circuits have to flexibly map highly stimulus-specific information in sparse layers onto a limited number of different motor outputs. The reformatting of sensory representations we observe here may mark the beginning of this sensory-motor transition in the olfactory system.

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