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      The neuronal architecture of the mushroom body provides a logic for associative learning

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          Abstract

          We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell–MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

          DOI: http://dx.doi.org/10.7554/eLife.04577.001

          eLife digest

          One of the key goals of neuroscience is to understand how specific circuits of brain cells enable animals to respond optimally to the constantly changing world around them. Such processes are more easily studied in simpler brains, and the fruit fly—with its small size, short life cycle, and well-developed genetic toolkit—is widely used to study the genes and circuits that underlie learning and behavior.

          Fruit flies can learn to approach odors that have previously been paired with food, and also to avoid any odors that have been paired with an electric shock, and a part of the brain called the mushroom body has a central role in this process. When odorant molecules bind to receptors on the fly's antennae, they activate neurons in the antennal lobe of the brain, which in turn activate cells called Kenyon cells within the mushroom body. The Kenyon cells then activate output neurons that convey signals to other parts of the brain.

          It is known that relatively few Kenyon cells are activated by any given odor. Moreover, it seems that a given odor activates different sets of Kenyon cells in different flies. Because the association between an odor and the Kenyon cells it activates is unique to each fly, each fly needs to learn through its own experiences what a particular pattern of Kenyon cell activation means.

          Aso et al. have now applied sophisticated molecular genetic and anatomical techniques to thousands of different transgenic flies to identify the neurons of the mushroom body. The resulting map reveals that the mushroom body contains roughly 2200 neurons, including seven types of Kenyon cells and 21 types of output cells, as well as 20 types of neurons that use the neurotransmitter dopamine. Moreover, this map provides insights into the circuits that support odor-based learning. It reveals, for example, that the mushroom body can be divided into 15 anatomical compartments that are each defined by the presence of a specific set of output and dopaminergic neuron cell types. Since the dopaminergic neurons help to shape a fly's response to odors on the basis of previous experience, this organization suggests that these compartments may be semi-autonomous information processing units.

          In contrast to the rest of the insect brain, the mushroom body has a flexible organization that is similar to that of the mammalian brain. Elucidating the circuits that support associative learning in fruit flies should therefore make it easier to identify the equivalent mechanisms in vertebrate animals.

          DOI: http://dx.doi.org/10.7554/eLife.04577.002

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          Most cited references62

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          Molecular architecture of smell and taste in Drosophila.

          The chemical senses-smell and taste-allow animals to evaluate and distinguish valuable food resources from dangerous substances in the environment. The central mechanisms by which the brain recognizes and discriminates attractive and repulsive odorants and tastants, and makes behavioral decisions accordingly, are not well understood in any organism. Recent molecular and neuroanatomical advances in Drosophila have produced a nearly complete picture of the peripheral neuroanatomy and function of smell and taste in this insect. Neurophysiological experiments have begun to provide insight into the mechanisms by which these animals process chemosensory cues. Given the considerable anatomical and functional homology in smell and taste pathways in all higher animals, experimental approaches in Drosophila will likely provide broad insights into the problem of sensory coding. Here we provide a critical review of the recent literature in this field and comment on likely future directions.
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            The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis.

            We describe a new repressible binary expression system based on the regulatory genes from the Neurospora qa gene cluster. This "Q system" offers attractive features for transgene expression in Drosophila and mammalian cells: low basal expression in the absence of the transcriptional activator QF, high QF-induced expression, and QF repression by its repressor QS. Additionally, feeding flies quinic acid can relieve QS repression. The Q system offers many applications, including (1) intersectional "logic gates" with the GAL4 system for manipulating transgene expression patterns, (2) GAL4-independent MARCM analysis, and (3) coupled MARCM analysis to independently visualize and genetically manipulate siblings from any cell division. We demonstrate the utility of the Q system in determining cell division patterns of a neuronal lineage and gene function in cell growth and proliferation, and in dissecting neurons responsible for olfactory attraction. The Q system can be expanded to other uses in Drosophila and to any organism conducive to transgenesis. 2010 Elsevier Inc. All rights reserved.
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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: Reviewing editor
                Journal
                eLife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                2050-084X
                23 December 2014
                2014
                : 3
                : e04577
                Affiliations
                [1 ]Janelia Research Campus, Howard Hughes Medical Institute , Ashburn, United States
                [2 ]Howard Hughes Medical Institute, Columbia University , New York, United States
                [3 ]deptDepartment of Neuroscience, College of Physicians and Surgeons , Columbia University , New York, United States
                [4 ]deptDepartment of Physiology and Cellular Biophysics, College of Physicians and Surgeons , Columbia University , New York, United States
                [5 ]Tohuku University Graduate School of Life Sciences , Sendai, Japan
                [6 ]Max-Planck Institute of Neurobiology , Martinsried, Germany
                [7 ]deptDepartment of Biochemistry and Molecular Biophysics, College of Physicians and Surgeons , Columbia University , New York, United States
                Brandeis University , United States
                Brandeis University , United States
                Author notes
                Article
                04577
                10.7554/eLife.04577
                4273437
                25535793
                3e99ef36-bc40-46b8-98cd-d91f4ee68aff
                © 2014, Aso et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 03 September 2014
                : 05 November 2014
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000011, universityHoward Hughes Medical Institute;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000011, universityHoward Hughes Medical Institute;
                Award ID: Janelia Visiting Scientist Program
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000324, Gatsby Charitable Foundation;
                Award ID: Gatsby Initiative Fund in Brain Circuitry at Columbia University
                Award Recipient :
                Funded by: Swartz Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;
                Award ID: Bernstein Focus Neurobiology of Learning 01GQ0932
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004189, Max-Planck-Gesellschaft;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: TA 552/5-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: MEXT/JSPS KAKENHI 25890003, 26120705, 26119503 and 26250001
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007428, Naito Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001033, Jane Coffin Childs Memorial Fund for Medical Research;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001229, G Harold and Leila Y. Mathers Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                2.0
                A map of the entire array of cell types and potential projections in the mushroom body of the fruit fly brain provides insights into the circuitry that supports learning of stimulus-reward and stimulus–punishment associations.

                Life sciences
                mushroom body,olfactory learning,associative memory,neuronal circuits,dopamine,plasticity,d. melanogaster

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