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      Medial entorhinal cortex lesions induce degradation of CA1 place cell firing stability when self-motion information is used

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          Abstract

          The entorhinal–hippocampus network plays a central role in navigation and episodic memory formation. To investigate these interactions, we examined the effect of medial entorhinal cortex lesions on hippocampal place cell activity. Since the medial entorhinal cortex is suggested to play a role in the processing of self-motion information, we hypothesised that such processing would be necessary for maintaining stable place fields in the absence of environmental cues. Place cells were recorded as medial entorhinal cortex–lesioned rats explored a circular arena during five 16-min sessions comprising a baseline session with all sensory inputs available followed by four sessions during which environmental (i.e. visual, olfactory, tactile) cues were progressively reduced to the point that animals could rely exclusively on self-motion cues to maintain stable place fields. We found that place field stability and a number of place cell firing properties were affected by medial entorhinal cortex lesions in the baseline session. When rats were forced to rely exclusively on self-motion cues, within-session place field stability was dramatically decreased in medial entorhinal cortex rats relative to SHAM rats. These results support a major role of the medial entorhinal cortex in processing self-motion cues, with this information being conveyed to the hippocampus to help anchor and maintain a stable spatial representation during movement.

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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

                Journal
                Brain Neurosci Adv
                Brain Neurosci Adv
                BNA
                spbna
                Brain and Neuroscience Advances
                SAGE Publications (Sage UK: London, England )
                2398-2128
                30 September 2020
                Jan-Dec 2020
                : 4
                : 2398212820953004
                Affiliations
                [1-2398212820953004]Aix Marseille Université, CNRS, LNC, Laboratory of Cognitive Neuroscience, Marseille, France
                Author notes
                [*]Etienne Save, LNC, Laboratory of Cognitive Neuroscience – UMR 7291, Aix Marseille Université, CNRS, 3 place Victor Hugo, 13331 Marseille Cedex 3, France. Email: etienne.save@ 123456univ-amu.fr
                Author information
                https://orcid.org/0000-0002-3112-3949
                Article
                10.1177_2398212820953004
                10.1177/2398212820953004
                7545758
                bcb51497-9a2a-415f-8333-b3c159c5e915
                © The Author(s) 2020

                This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License ( https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

                History
                : 27 March 2020
                : 21 July 2020
                Funding
                Funded by: Ministère de l’Education Nationale, de l’Enseignement Superieur et de la Recherche, FundRef https://doi.org/10.13039/501100004562;
                Award ID: PhD fellowship
                Categories
                Within and beyond the medial temporal lobe: brain circuits and mechanisms of recognition and place memory
                Research Paper
                Custom metadata
                January-December 2020
                ts1

                entorhinal cortex,spatial cognition,place cells,hippocampus,rat

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