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      Entorhinal velocity signals reflect environmental geometry

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          Summary

          The entorhinal cortex contains neurons that represent self-location, including grid cells that fire in periodic locations and velocity signals that encode running speed and head direction. While the size and shape of the environment influences grid patterns, whether entorhinal velocity signals are equally influenced or provide a universal metric for self-motion across environments remains unknown. Here, we report that speed cells rescale after changes to the size and shape of the environment. Moreover, head direction cells re-organize in an experience-dependent manner to align with the axis of environmental change. A knockout mouse model allows a dissociation of the coordination between cell types, with grid and speed, but not head direction, cells responding in concert to environmental change. These results point to malleability in the coding features of multiple entorhinal cell types and have implications for which cell types contribute to the velocity signal used by computational models of grid cells.

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          Most cited references54

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          Microstructure of a spatial map in the entorhinal cortex.

          The ability to find one's way depends on neural algorithms that integrate information about place, distance and direction, but the implementation of these operations in cortical microcircuits is poorly understood. Here we show that the dorsocaudal medial entorhinal cortex (dMEC) contains a directionally oriented, topographically organized neural map of the spatial environment. Its key unit is the 'grid cell', which is activated whenever the animal's position coincides with any vertex of a regular grid of equilateral triangles spanning the surface of the environment. Grids of neighbouring cells share a common orientation and spacing, but their vertex locations (their phases) differ. The spacing and size of individual fields increase from dorsal to ventral dMEC. The map is anchored to external landmarks, but persists in their absence, suggesting that grid cells may be part of a generalized, path-integration-based map of the spatial environment.
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            Path integration and the neural basis of the 'cognitive map'.

            The hippocampal formation can encode relative spatial location, without reference to external cues, by the integration of linear and angular self-motion (path integration). Theoretical studies, in conjunction with recent empirical discoveries, suggest that the medial entorhinal cortex (MEC) might perform some of the essential underlying computations by means of a unique, periodic synaptic matrix that could be self-organized in early development through a simple, symmetry-breaking operation. The scale at which space is represented increases systematically along the dorsoventral axis in both the hippocampus and the MEC, apparently because of systematic variation in the gain of a movement-speed signal. Convergence of spatially periodic input at multiple scales, from so-called grid cells in the entorhinal cortex, might result in non-periodic spatial firing patterns (place fields) in the hippocampus.
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              Conjunctive representation of position, direction, and velocity in entorhinal cortex.

              Grid cells in the medial entorhinal cortex (MEC) are part of an environment-independent spatial coordinate system. To determine how information about location, direction, and distance is integrated in the grid-cell network, we recorded from each principal cell layer of MEC in rats that explored two-dimensional environments. Whereas layer II was predominated by grid cells, grid cells colocalized with head-direction cells and conjunctive grid x head-direction cells in the deeper layers. All cell types were modulated by running speed. The conjunction of positional, directional, and translational information in a single MEC cell type may enable grid coordinates to be updated during self-motion-based navigation.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                22 November 2019
                13 January 2020
                February 2020
                13 July 2020
                : 23
                : 2
                : 239-251
                Affiliations
                [1 ]Department of Neurobiology, Stanford University School of Medicine, Stanford CA 94305, USA
                [2 ]Department of Neurology, Vanderbilt University Medical Center, Nashville TN 37232
                Author notes

                Author Contributions: LMG and RGM conceptualized experiments and analyses. CM and RGM performed chronic implantations, and collected and analyzed in vivo data. KH provided support on analyses. DMC provided the TRIP8b KO mouse line. LMG and RGM wrote the paper with feedback from all authors.

                [* ]Corresponding authors: giocomo@ 123456stanford.edu (LMG), munnr@ 123456stanford.edu (RGM)
                Article
                NIHMS1544278
                10.1038/s41593-019-0562-5
                7007349
                31932764
                32aa8794-c28b-4bf2-b76e-b461669f2e75

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                Neurosciences
                Neurosciences

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