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      On-Center/Inhibitory-Surround Decorrelation via Intraglomerular Inhibition in the Olfactory Bulb Glomerular Layer

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          Abstract

          Classical lateral inhibition, which relies on spatially ordered neural representations of physical stimuli, cannot decorrelate sensory representations in which stimulus properties are represented non-topographically. Recent theoretical and experimental studies indicate that such a non-topographical representation of olfactory stimuli predominates in olfactory bulb, thereby refuting the classical view that olfactory decorrelation is mediated by lateral inhibition comparable to that in the retina. Questions persist, however, regarding how well non-topographical decorrelation models can replicate the inhibitory “surround” that has been observed experimentally (with respect to odor feature-similarity) in olfactory bulb principal neurons, analogous to the spatial inhibitory surround generated by lateral inhibition in retina. Using two contrasting scenarios of stimulus representation – one “retinotopically” organized and one in which receptive fields are unpredictably distributed as they are in olfactory bulb – we here show that intracolumnar inhibitory interactions between local interneurons and principal neurons successfully decorrelate similar sensory representations irrespective of the scenario of representation. In contrast, lateral inhibitory interactions between these same neurons in neighboring columns are only able to effectively decorrelate topographically organized representations. While anatomical substrates superficially consistent with both types of inhibition exist in olfactory bulb, of the two only local intraglomerular inhibition suffices to mediate olfactory decorrelation.

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          Most cited references 55

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          Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns.

          The mammalian cortex is organized in a columnar fashion: neurons lying below each other from the pia to the white matter usually share many functional properties. Across the cortical surface, cells with similar response properties are also clustered together, forming elongated bands or patches. Some response properties, such as orientation preference in the visual cortex, change gradually across the cortical surface forming 'orientation maps'. To determine the precise layout of iso-orientation domains, knowledge of responses not only to one but to many stimulus orientations is essential. Therefore, the exact depiction of orientation maps has been hampered by technical difficulties and remained controversial for almost thirty years. Here we use in vivo optical imaging based on intrinsic signals to gather information on the responses of a piece of cortex to gratings in many different orientations. This complete set of responses then provides detailed information on the structure of the orientation map in a large patch of cortex from area 18 of the cat. We find that cortical regions that respond best to one orientation form highly ordered patches rather than elongated bands. These iso-orientation patches are organized around 'orientation centres', producing pinwheel-like patterns in which the orientation preference of cells is changing continuously across the cortex. We have also analysed our data for fast changes in orientation preference and find that these 'fractures' are limited to the orientation centres. The pinwheels and orientation centres are such a prominent organizational feature that it should be important to understand their development as well as their function in the processing of visual information.
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            Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb.

             K Mori,  M Yokoi,  S Nakanishi (1995)
            Mitral/tufted cells (M/T cells) and granule cells form reciprocal dendrodendritic synapses in the main olfactory bulb; the granule cell is excited by glutamate from the M/T cell and in turn inhibits M/T cells by gamma-aminobutyrate. The trans-synaptically excited granule cell is thought to induce lateral inhibition in neighboring M/T cells and to refine olfactory information. It remains, however, elusive how significantly and specifically this synaptic regulation contributes to the discrimination of different olfactory stimuli. This investigation concerns the mechanism of olfactory discrimination by single unit recordings of responses to a series of normal aliphatic aldehydes from individual rabbit M/T cells. This analysis revealed that inhibitory responses are evoked in a M/T cell by a defined subset of odor molecules with structures closely related to the excitatory odor molecules. Furthermore, blockade of the reciprocal synaptic transmission by the glutamate receptor antagonist or the gamma-aminobutyrate receptor antagonist markedly suppressed the odor-evoked inhibition, indicating that the inhibitory responses are evoked by lateral inhibition via the reciprocal synaptic transmission. The synaptic regulation in the olfactory bulb thus greatly enhances the tuning specificity of odor responses and would contribute to discrimination of olfactory information.
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              Olfactory perceptual learning requires adult neurogenesis.

              Perceptual learning is required for olfactory function to adapt appropriately to changing odor environments. We here show that newborn neurons in the olfactory bulb are not only involved in, but necessary for, olfactory perceptual learning. First, the discrimination of perceptually similar odorants improves in mice after repeated exposure to the odorants. Second, this improved discrimination is accompanied by an elevated survival rate of newborn inhibitory neurons, preferentially involved in processing of the learned odor, within the olfactory bulb. Finally, blocking neurogenesis before and during the odorant exposure period prevents this learned improvement in discrimination. Olfactory perceptual learning is thus mediated by the reinforcement of functional inhibition in the olfactory bulb by adult neurogenesis.
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                Author and article information

                Journal
                Front Integr Neurosci
                Front. Integr. Neurosci.
                Frontiers in Integrative Neuroscience
                Frontiers Research Foundation
                1662-5145
                10 February 2012
                2012
                : 6
                Affiliations
                1simpleComputational Physiology Laboratory, Cornell University Ithaca, NY, USA
                2simpleDepartment of Psychology, Cornell University Ithaca, NY, USA
                3simpleDepartment of Neurobiology and Behavior, Cornell University Ithaca, NY, USA
                Author notes

                Edited by: Alan Carleton, University of Geneva, Switzerland

                Reviewed by: Marcelo O. Magnasco, Rockefeller University, USA; Gilles Laurent, Max Planck Institute for Brain Research, Germany

                *Correspondence: Christiane Linster, Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA. e-mail: cl243@ 123456cornell.edu
                Article
                10.3389/fnint.2012.00005
                3277047
                22363271
                Copyright © 2012 Cleland and Linster.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                Page count
                Figures: 3, Tables: 1, Equations: 5, References: 55, Pages: 10, Words: 8756
                Categories
                Neuroscience
                Hypothesis and Theory

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