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      Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortex

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          Abstract

          Neurons of the medial entorhinal cortex (MEC) provide spatial representations critical for navigation. In this network, the periodic firing fields of grid cells act as a metric element for position. The location of the grid firing fields depends on interactions between self-motion information, geometrical properties of the environment and nonmetric contextual cues. Here, we test whether visual information, including nonmetric contextual cues, also regulates the firing rate of MEC neurons. Removal of visual landmarks caused a profound impairment in grid cell periodicity. Moreover, the speed code of MEC neurons changed in darkness and the activity of border cells became less confined to environmental boundaries. Half of the MEC neurons changed their firing rate in darkness. Manipulations of nonmetric visual cues that left the boundaries of a 1D environment in place caused rate changes in grid cells. These findings reveal context specificity in the rate code of MEC neurons.

          DOI: http://dx.doi.org/10.7554/eLife.16937.001

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          Most cited references 51

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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

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                23 July 2016
                2016
                : 5
                Affiliations
                [1 ]deptDepartment of Clinical Neurobiology , Medical Faculty of Heidelberg University , Heidelberg, Germany
                [2 ]German Cancer Research Center , Heidelberg, Germany
                Boston University , United States
                Boston University , United States
                Author notes
                Article
                16937
                10.7554/eLife.16937
                4987135
                27449281
                © 2016, Pérez-Escobar et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                Product
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: AL 1730/1-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB-1134
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Neuroscience
                Research Article
                Custom metadata
                2.5
                The firing rate of MEC neurons conveys information about visual landmarks.

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