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5 Janelia Publications

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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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    05/05/17 | What can tiny mushrooms in fruit flies tell us about learning and memory?
    Hige T
    Neuroscience Research. 2017 May 05:. doi: 10.1016/j.neures.2017.05.002

    Nervous systems have evolved to translate external stimuli into appropriate behavioral responses. In an ever-changing environment, flexible adjustment of behavioral choice by experience-dependent learning is essential for the animal's survival. Associative learning is a simple form of learning that is widely observed from worms to humans. To understand the whole process of learning, we need to know how sensory information is represented and transformed in the brain, how it is changed by experience, and how the changes are reflected on motor output. To tackle these questions, studying numerically simple invertebrate nervous systems has a great advantage. In this review, I will feature the Pavlovian olfactory learning in the fruit fly, Drosophila melanogaster. The mushroom body is a key brain area for the olfactory learning in this organism. Recently, comprehensive anatomical information and the genetic tool sets were made available for the mushroom body circuit. This greatly accelerated the physiological understanding of the learning process. One of the key findings was dopamine-induced long-term synaptic plasticity that can alter the representations of stimulus valence. I will mostly focus on the new studies within these few years and discuss what we can possibly learn about the vertebrate systems from this model organism.

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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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