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      Lateral Connectivity in the Olfactory Bulb is Sparse and Segregated

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          Abstract

          Lateral connections in the olfactory bulb were previously thought to be organized for center–surround inhibition. However, recent anatomical and physiological studies showed sparse and distributed interactions of inhibitory granule cells (GCs) which tended to be organized in columnar clusters. Little is known about how these distributed clusters are interconnected. In this study, we use transsynaptic tracing viruses bearing green or red fluorescent proteins to further elucidate mitral- and tufted-to-GC connectivity. Separate sites in the glomerular layer were injected with each virus. Columns with labeling from both viruses after transsynaptic spread show sparse red or green GCs which tended to be segregated. However, there was a higher incidence of co-labeled cells than chance would predict. Similar segregation of labeling is observed from dual injections into olfactory cortex. Collectively, these results suggest that neighboring mitral and tufted cells receive inhibitory inputs from segregated subsets of GCs, enabling inhibition of a center by specific and discontinuous lateral elements.

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          Most cited references27

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          Combinatorial receptor codes for odors.

          The discriminatory capacity of the mammalian olfactory system is such that thousands of volatile chemicals are perceived as having distinct odors. Here we used a combination of calcium imaging and single-cell RT-PCR to identify odorant receptors (ORs) for odorants with related structures but varied odors. We found that one OR recognizes multiple odorants and that one odorant is recognized by multiple ORs, but that different odorants are recognized by different combinations of ORs. Thus, the olfactory system uses a combinatorial receptor coding scheme to encode odor identities. Our studies also indicate that slight alterations in an odorant, or a change in its concentration, can change its "code," potentially explaining how such changes can alter perceived odor quality.
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            The unbiased estimation of number and sizes of arbitrary particles using the disector.

            D Sterio (1984)
            A three-dimensional counting rule and its integral test system, the disector, for obtaining unbiased estimates of the number of arbitrary particles in a specimen is presented. Used in combination with ordinary and recently developed stereological methods unbiased estimates of various mean particle sizes and the variance of particle volume are obtainable on sets of two parallel sections with a known separation. The same principle allows the unbiased estimation of the distribution of individual particle volumes in sets of serial sections.
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              Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations.

              The properties of cortical circuits underlying central representations of sensory stimuli are poorly understood. Here we use in vivo cell-attached and whole-cell voltage-clamp recordings to reveal how excitatory and inhibitory synaptic input govern odor representations in rat primary olfactory (piriform) cortex. We show that odors evoke spiking activity that is sparse across the cortical population. We find that unbalanced synaptic excitation and inhibition underlie sparse activity: inhibition is widespread and broadly tuned, while excitation is less common and odor-specific. "Global" inhibition can be explained by local interneurons that receive ubiquitous and nonselective odor-evoked excitation. In the temporal domain, while respiration imposes a slow rhythm to olfactory cortical responses, odors evoke fast (15-30 Hz) oscillations in synaptic activity. Oscillatory excitation precedes inhibition, generating brief time windows for precise and temporally sparse spike output. Together, our results reveal that global inhibition and oscillations are major synaptic mechanisms shaping odor representations in olfactory cortex.
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                Author and article information

                Journal
                Front Neural Circuits
                Front. Neural Circuits.
                Frontiers in Neural Circuits
                Frontiers Research Foundation
                1662-5110
                09 March 2011
                25 April 2011
                2011
                : 5
                : 5
                Affiliations
                [1] 1simpleDepartment of Neurobiology, Yale University School of Medicine New Haven, CT, USA
                [2] 2simpleDepartment of Physics, Yale University New Haven, CT, USA
                Author notes

                Edited by: Aravinthan Samuel, Harvard University, USA

                Reviewed by: Edward R. Soucy, Harvard University, USA; Matt Wachowiak, University of Utah, USA

                *Correspondence: David C. Willhite, Department of Neurobiology, Yale University School of Medicine, New Haven, CT 06520, USA. e-mail: david.willhite@ 123456yale.edu
                Article
                10.3389/fncir.2011.00005
                3084525
                21559072
                8bcbb6a7-e2fd-483f-bfe0-8d2d940fa972
                Copyright © 2011 Kim, Phillips, Chang, Patel, Nguyen and Willhite.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                : 07 February 2011
                : 09 April 2011
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 47, Pages: 8, Words: 6792
                Categories
                Neuroscience
                Original Research

                Neurosciences
                connectivity,olfaction,circuits,olfactory bulb,lateral inhibition
                Neurosciences
                connectivity, olfaction, circuits, olfactory bulb, lateral inhibition

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