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      Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory

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          Abstract

          Efficient energy use has constrained the evolution of nervous systems. However, it is unresolved whether energy metabolism may resultantly regulate major brain functions. Our observation that Drosophila flies double their sucrose intake at an early stage of long-term memory formation initiated the investigation of how energy metabolism intervenes in this process. Cellular-resolution imaging of energy metabolism reveals a concurrent elevation of energy consumption in neurons of the mushroom body, the fly's major memory centre. Strikingly, upregulation of mushroom body energy flux is both necessary and sufficient to drive long-term memory formation. This effect is triggered by a specific pair of dopaminergic neurons afferent to the mushroom bodies, via the D5-like DAMB dopamine receptor. Hence, dopamine signalling mediates an energy switch in the mushroom body that controls long-term memory encoding. Our data thus point to an instructional role for energy flux in the execution of demanding higher brain functions.

          Abstract

          Energy consumption in the brain is thought to respond to changes in neuronal activity, without informational role. Here the authors show that increased energy flux in the mushroom body, driven by a pair of input dopaminergic neurons, is a command for the formation of long-term memory in Drosophila.

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          Most cited references51

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          Mushroom body memoir: from maps to models.

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            Communication in neuronal networks.

            Brains perform with remarkable efficiency, are capable of prodigious computation, and are marvels of communication. We are beginning to understand some of the geometric, biophysical, and energy constraints that have governed the evolution of cortical networks. To operate efficiently within these constraints, nature has optimized the structure and function of cortical networks with design principles similar to those used in electronic networks. The brain also exploits the adaptability of biological systems to reconfigure in response to changing needs.
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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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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                05 June 2017
                2017
                : 8
                : 15510
                Affiliations
                [1 ]Genes and Dynamics of Memory Systems, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University , 10 rue Vauquelin, Paris 75005, France
                [2 ]Department of Biological Sciences, Border Biomedical Research Center, University of Texas at El Paso , El Paso, Texas 79968, USA
                Author notes
                [*]

                Present address: Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, USA

                [†]

                Present address: Research Center on Animal Cognition, Université Paul Sabatier, Toulouse, France

                [‡]

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-9976-1763
                Article
                ncomms15510
                10.1038/ncomms15510
                5465319
                28580949
                4a7f62a3-9cb9-4581-8334-baae4ea7573d
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 31 July 2016
                : 04 April 2017
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