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      Framing of grid cells within and beyond navigation boundaries

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          Abstract

          Grid cells represent an ideal candidate to investigate the allocentric determinants of the brain’s cognitive map. Most studies of grid cells emphasized the roles of geometric boundaries within the navigational range of the animal. Behaviors such as novel route-taking between local environments indicate the presence of additional inputs from remote cues beyond the navigational borders. To investigate these influences, we recorded grid cells as rats explored an open-field platform in a room with salient, remote cues. The platform was rotated or translated relative to the room frame of reference. Although the local, geometric frame of reference often exerted the strongest control over the grids, the remote cues demonstrated a consistent, sometimes dominant, countervailing influence. Thus, grid cells are controlled by both local geometric boundaries and remote spatial cues, consistent with prior studies of hippocampal place cells and providing a rich representational repertoire to support complex navigational (and perhaps mnemonic) processes.

          DOI: http://dx.doi.org/10.7554/eLife.21354.001

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          Most cited references86

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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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              Representation of geometric borders in the entorhinal cortex.

              We report the existence of an entorhinal cell type that fires when an animal is close to the borders of the proximal environment. The orientation-specific edge-apposing activity of these "border cells" is maintained when the environment is stretched and during testing in enclosures of different size and shape in different rooms. Border cells are relatively sparse, making up less than 10% of the local cell population, but can be found in all layers of the medial entorhinal cortex as well as the adjacent parasubiculum, often intermingled with head-direction cells and grid cells. Border cells may be instrumental in planning trajectories and anchoring grid fields and place fields to a geometric reference frame.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                13 January 2017
                2017
                : 6
                : e21354
                Affiliations
                [1 ]Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University , Baltimore, United States
                [2 ]deptSolomon H. Snyder Department of Neuroscience , Johns Hopkins University , Baltimore, United States
                [3]National Centre for Biological Sciences , India
                [4]National Centre for Biological Sciences , India
                Author notes
                Author information
                http://orcid.org/0000-0002-8588-0865
                http://orcid.org/0000-0002-1796-2930
                Article
                21354
                10.7554/eLife.21354
                5271608
                28084992
                a500b49d-c1c6-4b6f-812a-be9134041166
                © 2017, Savelli 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.

                History
                : 07 September 2016
                : 11 January 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
                Award ID: R01 NS039456
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000854, Human Frontier Science Program;
                Award ID: LT00683/2006-C
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000025, National Institute of Mental Health;
                Award ID: R01 MH079511
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                2.5
                Grid-cell maps can be aligned to both local and remote reference frames, suggesting that they provide a metric for space beyond the navigationally accessible boundaries of the local environment.

                Life sciences
                grid cell,hippocampal formation,cognitive map,spatial orientation,navigation,rat
                Life sciences
                grid cell, hippocampal formation, cognitive map, spatial orientation, navigation, rat

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