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      Environmental deformations dynamically shift the grid cell spatial metric

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          Abstract

          In familiar environments, the firing fields of entorhinal grid cells form regular triangular lattices. However, when the geometric shape of the environment is deformed, these time-averaged grid patterns are distorted in a grid scale-dependent and local manner. We hypothesized that this distortion in part reflects dynamic anchoring of the grid code to displaced boundaries, possibly through border cell-grid cell interactions. To test this hypothesis, we first reanalyzed two existing rodent grid rescaling datasets to identify previously unrecognized boundary-tethered shifts in grid phase that contribute to the appearance of rescaling. We then demonstrated in a computational model that boundary-tethered phase shifts, as well as scale-dependent and local distortions of the time-averaged grid pattern, could emerge from border-grid interactions without altering inherent grid scale. Together, these results demonstrate that environmental deformations induce history-dependent shifts in grid phase, and implicate border-grid interactions as a potential mechanism underlying these dynamics.

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          Most cited references49

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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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            Memory, navigation and theta rhythm in the hippocampal-entorhinal system.

            Theories on the functions of the hippocampal system are based largely on two fundamental discoveries: the amnestic consequences of removing the hippocampus and associated structures in the famous patient H.M. and the observation that spiking activity of hippocampal neurons is associated with the spatial position of the rat. In the footsteps of these discoveries, many attempts were made to reconcile these seemingly disparate functions. Here we propose that mechanisms of memory and planning have evolved from mechanisms of navigation in the physical world and hypothesize that the neuronal algorithms underlying navigation in real and mental space are fundamentally the same. We review experimental data in support of this hypothesis and discuss how specific firing patterns and oscillatory dynamics in the entorhinal cortex and hippocampus can support both navigation and memory.
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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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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                22 October 2018
                2018
                : 7
                : e38169
                Affiliations
                [1 ]deptDepartment of Psychology University of Pennsylvania PennsylvaniaUnited States
                [2 ]deptDepartment of Physics University of Pennsylvania PennsylvaniaUnited States
                The University of Texas at Austin, Center for Learning and Memory United States
                Brown University United States
                The University of Texas at Austin, Center for Learning and Memory United States
                Author information
                http://orcid.org/0000-0003-1622-7835
                https://orcid.org/0000-0002-6497-3819
                Article
                38169
                10.7554/eLife.38169
                6203432
                30346272
                4901afd7-8131-4cf2-be95-1890703683ea
                © 2018, Keinath 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
                : 08 May 2018
                : 21 October 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: PHY-1734030
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: EY022350
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 0966142
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: EY027047
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: PHY-1607611
                Award Recipient :
                Funded by: Honda Research Institute;
                Award ID: Curious-Minded Machines program
                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
                When a familiar environment is reshaped, the grid cell spatial code is dynamically anchored to recently encountered boundaries and changes throughout exploration with the specific movement history of the navigator.

                Life sciences
                grid cell,place cell,hippocampus,entorhinal cortex,computational model,deformation,rat
                Life sciences
                grid cell, place cell, hippocampus, entorhinal cortex, computational model, deformation, rat

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