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      Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability

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          Abstract

          Animals acquire predictive values of sensory stimuli through reinforcement. In the brain of Drosophila melanogaster, activation of two types of dopamine neurons in the PAM and PPL1 clusters has been shown to induce aversive odor memory. Here, we identified the third cell type and characterized aversive memories induced by these dopamine neurons. These three dopamine pathways all project to the mushroom body but terminate in the spatially segregated subdomains. To understand the functional difference of these dopamine pathways in electric shock reinforcement, we blocked each one of them during memory acquisition. We found that all three pathways partially contribute to electric shock memory. Notably, the memories mediated by these neurons differed in temporal stability. Furthermore, combinatorial activation of two of these pathways revealed significant interaction of individual memory components rather than their simple summation. These results cast light on a cellular mechanism by which a noxious event induces different dopamine signals to a single brain structure to synthesize an aversive memory.

          Author Summary

          Punishment not only repels animals but also drives the formation of aversive memory of contiguous stimuli. Guided by the memory, animals can later avoid the cues that predict negative outcome. How is a punishing event represented in the brain? We have found that at least three types of dopamine neurons in the Drosophila brain contribute to memory formation. Genetic activation of these neurons temporally paired with an odor presentation induced aversive odor memory, raising a question about the functional distinction of these neurons. Here we characterized aversive memories induced by these dopamine neurons. The magnitude of immediate memory and following memory decay differ greatly among the three cell types. Interestingly, combinatorial activation of two cell types revealed that induced memory is not a simple sum of the two memories, but rather the result of non-linear interaction specific for different retention times. Taken together, we propose that a punishing event induces aversive memory with unique temporal dynamics by tuning the activation of selective dopamine neurons.

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          Most cited references38

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          Mushroom body memoir: from maps to models.

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            Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons.

            T Kitamoto (2001)
            Behavior is a manifestation of temporally and spatially defined neuronal activities. To understand how behavior is controlled by the nervous system, it is important to identify the neuronal substrates responsible for these activities, and to elucidate how they are integrated into a functional circuit. I introduce a novel and general method to conditionally perturb anatomically defined neurons in intact Drosophila. In this method, a temperature-sensitive allele of shibire (shi(ts1)) is overexpressed in neuronal subsets using the GAL4/UAS system. Because the shi gene product is essential for synaptic vesicle recycling, and shi(ts1) is semidominant, a simple temperature shift should lead to fast and reversible effects on synaptic transmission of shi(ts1) expressing neurons. When shi(ts1) expression was directed to cholinergic neurons, adult flies showed a dramatic response to the restrictive temperature, becoming motionless within 2 min at 30 degrees C. This temperature-induced paralysis was reversible. After being shifted back to the permissive temperature, they readily regained their activity and started to walk in 1 min. When shi(ts1) was expressed in photoreceptor cells, adults and larvae exhibited temperature-dependent blindness. These observations show that the GAL4/UAS system can be used to express shi(ts1) in a specific subset of neurons to cause temperature-dependent changes in behavior. Because this method allows perturbation of the neuronal activities rapidly and reversibly in a spatially and temporally restricted manner, it will be useful to study the functional significance of particular neuronal subsets in the behavior of intact animals. Copyright 2001 John Wiley & Sons, Inc.
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              A neural circuit mechanism integrating motivational state with memory expression in Drosophila.

              Behavioral expression of food-associated memory in fruit flies is constrained by satiety and promoted by hunger, suggesting an influence of motivational state. Here, we identify a neural mechanism that integrates the internal state of hunger and appetitive memory. We show that stimulation of neurons that express neuropeptide F (dNPF), an ortholog of mammalian NPY, mimics food deprivation and promotes memory performance in satiated flies. Robust appetitive memory performance requires the dNPF receptor in six dopaminergic neurons that innervate a distinct region of the mushroom bodies. Blocking these dopaminergic neurons releases memory performance in satiated flies, whereas stimulation suppresses memory performance in hungry flies. Therefore, dNPF and dopamine provide a motivational switch in the mushroom body that controls the output of appetitive memory.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                July 2012
                July 2012
                12 July 2012
                : 8
                : 7
                : e1002768
                Affiliations
                [1 ]Max Planck Institut für Neurobiologie, Martinsried, Germany
                [2 ]Lehrstuhl für Genetik und Neurobiologie, Universität Würzburg, Würzburg, Germany
                [3 ]Institute of Molecular and Cellular Biosciences, The University of Tokyo, Tokyo, Japan
                [4 ]Universität zu Köln, Biozentrum Köln, Köln, Germany
                University of California San Francisco, United States of America
                Author notes

                ¤ a: Current address: Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, United States of America

                ¤ b: Current address: Departamento de Biología Celular y Patología, Instituto de Neurociencias de Castilla y León, León, Spain

                Conceived and designed the experiments: YA HT. Performed the experiments: YA AH MO IS TT ABF. Analyzed the data: YA IS HT. Contributed reagents/materials/analysis tools: AH MO TT KI HS. Wrote the paper: YA HT.

                Article
                PGENETICS-D-11-02116
                10.1371/journal.pgen.1002768
                3395599
                22807684
                4b17124e-1f7d-4d3c-9c18-af49a2af3314
                Aso et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 5 October 2011
                : 30 April 2012
                Page count
                Pages: 17
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Integrative Physiology
                Genetics
                Animal Genetics
                Neuroscience
                Behavioral Neuroscience
                Learning and Memory

                Genetics
                Genetics

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