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      Diversity and Wiring Variability of Olfactory Local Interneurons in the Drosophila Antennal Lobe

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          Abstract

          Local interneurons play essential roles in information processing by neural circuits. Here we present a comprehensive genetic, anatomical, and electrophysiological analysis of local interneurons (LNs) in the Drosophila antennal lobe, the first olfactory processing center in the brain. We find that LNs are diverse in their neurotransmitter profiles, connectivity, and physiological properties. Analysis of >1500 individual LNs reveals major morphological classes characterized by coarsely stereotyped glomerular innervation patterns. Some of these morphological classes exhibit distinct physiological properties. However, the finer-scale connectivity of an individual LN varies considerably across brains and there is notable physiological variability within each morphological or genetic class. Finally, we show that LN innervation requires interaction with olfactory receptor neurons during development, and some individual variability also likely reflects LN-LN interactions. Our results reveal an unexpected degree of complexity and individual variation in an invertebrate neural circuit, a result that creates challenges for solving the Drosophila connectome.

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          Most cited references43

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          Interneurons of the neocortical inhibitory system.

          Mammals adapt to a rapidly changing world because of the sophisticated cognitive functions that are supported by the neocortex. The neocortex, which forms almost 80% of the human brain, seems to have arisen from repeated duplication of a stereotypical microcircuit template with subtle specializations for different brain regions and species. The quest to unravel the blueprint of this template started more than a century ago and has revealed an immensely intricate design. The largest obstacle is the daunting variety of inhibitory interneurons that are found in the circuit. This review focuses on the organizing principles that govern the diversity of inhibitory interneurons and their circuits.
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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 molecular basis of odor coding in the Drosophila antenna.

              We have undertaken a functional analysis of the odorant receptor repertoire in the Drosophila antenna. Each receptor was expressed in a mutant olfactory receptor neuron (ORN) used as a "decoder," and the odor response spectrum conferred by the receptor was determined in vivo by electrophysiological recordings. The spectra of these receptors were then matched to those of defined ORNs to establish a receptor-to-neuron map. In addition to the odor response spectrum, the receptors dictate the signaling mode, i.e., excitation or inhibition, and the response dynamics of the neuron. An individual receptor can mediate both excitatory and inhibitory responses to different odorants in the same cell, suggesting a model of odorant receptor transduction. Receptors vary widely in their breadth of tuning, and odorants vary widely in the number of receptors they activate. Together, these properties provide a molecular basis for odor coding by the receptor repertoire of an olfactory organ.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                15 January 2010
                7 February 2010
                April 2010
                1 October 2010
                : 13
                : 4
                : 439-449
                Affiliations
                [1 ] Howard Hughes Medical Institute, Department of Biology, Stanford University, Stanford, CA 94305
                [2 ] Department of Neurobiology, Harvard Medical School, Boston, MA 02115
                Author notes
                [*]

                These authors contributed equally.

                Article
                nihpa167057
                10.1038/nn.2489
                2847188
                20139975
                42813ae3-7f5a-49c9-b3e3-e662bfed43d8

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.w3.org/1999/xlink p1: http://www.nature.com/authors/editorial_policies/license.html#terms

                History
                Funding
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: R01 DC008174-04 ||DC
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: F31 DC008277 ||DC
                Categories
                Article

                Neurosciences
                olfaction,stereotypy,connectome,variability,glomerulus
                Neurosciences
                olfaction, stereotypy, connectome, variability, glomerulus

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