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      Spatiotemporal properties of whisker-evoked tactile responses in the mouse secondary somatosensory cortex

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          Abstract

          The representation of rodents’ mystacial vibrissae within the primary somatosensory (S1) cortex has become a major model for studying the cortical processing of tactile sensory information. However, upon vibrissal stimulation, tactile information first reaches S1 but also, almost simultaneously, the secondary somatosensory cortex (S2). To further understand the role of S2 in the processing of whisker inputs, it is essential to characterize the spatio-temporal properties of whisker-evoked response dynamics in this area. Here we describe the topography of the whiskers representation in the mouse S2 with voltage sensitive dye imaging. Analysis of the spatial properties of the early S2 responses induced by stimulating individually 22 to 24 whiskers revealed that they are spatially ordered in a mirror symmetric map with respect to S1 responses. Evoked signals in S2 and S1 are of similar amplitude and closely correlated at the single trial level. They confirm a short delay (~3 ms) between S1 and S2 early activation. In both S1 and S2 caudo-dorsal whiskers induce stronger responses than rostro-ventral ones. Finally, analysis of early C2-evoked responses indicates a faster activation of neighboring whisker representations in S2 relative to S1, probably due to the reduced size of the whisker map in S2.

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          Most cited references48

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          Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice.

          Tactile information is actively acquired and processed in the brain through concerted interactions between movement and sensation. Somatosensory input is often the result of self-generated movement during the active touch of objects, and conversely, sensory information is used to refine motor control. There must therefore be important interactions between sensory and motor pathways, which we chose to investigate in the mouse whisker sensorimotor system. Voltage-sensitive dye was applied to the neocortex of mice to directly image the membrane potential dynamics of sensorimotor cortex with subcolumnar spatial resolution and millisecond temporal precision. Single brief whisker deflections evoked highly distributed depolarizing cortical sensory responses, which began in the primary somatosensory barrel cortex and subsequently excited the whisker motor cortex. The spread of sensory information to motor cortex was dynamically regulated by behavior and correlated with the generation of sensory-evoked whisker movement. Sensory processing in motor cortex may therefore contribute significantly to active tactile sensory perception.
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            The functional organization of the barrel cortex.

            The tactile somatosensory pathway from whisker to cortex in rodents provides a well-defined system for exploring the link between molecular mechanisms, synaptic circuits, and behavior. The primary somatosensory cortex has an exquisite somatotopic map where each individual whisker is represented in a discrete anatomical unit, the "barrel," allowing precise delineation of functional organization, development, and plasticity. Sensory information is actively acquired in awake behaving rodents and processed differently within the barrel map depending upon whisker-related behavior. The prominence of state-dependent cortical sensory processing is likely to be crucial in our understanding of active sensory perception, experience-dependent plasticity and learning.
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              Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex.

              The rodent primary somatosensory cortex is spontaneously active in the form of locally synchronous membrane depolarizations (UP states) separated by quiescent hyperpolarized periods (DOWN states) both under anesthesia and during quiet wakefulness. In vivo whole-cell recordings and tetrode unit recordings were combined with voltage-sensitive dye imaging to analyze the relationship of the activity of individual pyramidal neurons in layer 2/3 to the ensemble spatiotemporal dynamics of the spontaneous depolarizations. These were either brief and localized to an area of a barrel column or occurred as propagating waves dependent on local glutamatergic synaptic transmission in layer 2/3. Spontaneous activity inhibited the sensory responses evoked by whisker deflection, accounting almost entirely for the large trial-to-trial variability of sensory-evoked postsynaptic potentials and action potentials. Subthreshold sensory synaptic responses evoked while a cortical area was spontaneously depolarized were smaller, briefer and spatially more confined. Surprisingly, whisker deflections evoked fewer action potentials during the spontaneous depolarizations despite neurons being closer to threshold. The ongoing spontaneous activity thus regulates the amplitude and the time-dependent spread of the sensory response in layer 2/3 barrel cortex.
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                Author and article information

                Contributors
                daniel.shulz@unic.cnrs-gif.fr
                isabelle.ferezou@unic.cnrs-gif.fr
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                21 January 2020
                21 January 2020
                2020
                : 10
                : 763
                Affiliations
                [1 ]Department of Integrative and Computational Neuroscience (ICN), Université Paris-Saclay, CNRS, Institut des Neurosciences Paris Saclay, Gif-sur-Yvette, 91190 France
                [2 ]Institut de biologie de l’École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, Paris, 75005 France
                Article
                57684
                10.1038/s41598-020-57684-6
                6972923
                31964984
                8f072d39-88ac-4247-9711-61398d16a427
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 24 July 2019
                : 27 December 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001665, Agence Nationale de la Recherche (French National Research Agency);
                Award ID: Neurowisk
                Award ID: Expect
                Award ID: SENSORY PROCESSING
                Award ID: NEUROWHISK
                Award ID: Expect
                Award ID: SensoryProcessing
                Award ID: Neurowisk
                Award ID: Expect
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100002915, Fondation pour la Recherche Médicale (Foundation for Medical Research in France);
                Award ID: Equipe DEQ20170336761
                Award ID: Equipe DEQ20170336761
                Award ID: Equipe DEQ20170336761
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100004794, Centre National de la Recherche Scientifique (National Center for Scientific Research);
                Funded by: Brainscopes and ICode are Strategic research initiatives arising from the Lidex Neuro-Saclay (supported by the national program: Investissements d'Avenir).
                Funded by: Brainscopes and ICode are Strategic research initiatives arising from the Lidex Neuro-Saclay (supported by the national program: Investissements d'Avenir).
                Funded by: Brainscopes and ICode are Strategic research initiatives arising from the Lidex Neuro-Saclay (supported by the national program: Investissements d'Avenir).
                Categories
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                Custom metadata
                © The Author(s) 2020

                Uncategorized
                sensory processing,cortex,whisker system
                Uncategorized
                sensory processing, cortex, whisker system

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