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      Representation of edges, head direction, and swimming kinematics in the brain of freely-navigating fish

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          Abstract

          Like most animals, the survival of fish depends on navigation in space. This capacity has been documented in behavioral studies that have revealed navigation strategies. However, little is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. We found that cells in the lateral pallium of the goldfish encode the edges of the environment, the fish head direction, the fish swimming speed, and the fish swimming velocity-vector. This study sheds light on how information related to navigation is represented in the brain of fish and addresses the fundamental question of the neural basis of navigation in this group of vertebrates.

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          Most cited references53

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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
                ronensgv@bgu.ac.il
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                8 September 2020
                8 September 2020
                2020
                : 10
                : 14762
                Affiliations
                [1 ]GRID grid.7489.2, ISNI 0000 0004 1937 0511, Department of Life Sciences, , Ben Gurion University of the Negev, ; 84105 Beer Sheva, Israel
                [2 ]GRID grid.7489.2, ISNI 0000 0004 1937 0511, Zlotowski Center for Neuroscience, , Ben Gurion University of the Negev, ; 84105 Beer Sheva, Israel
                [3 ]GRID grid.7489.2, ISNI 0000 0004 1937 0511, Department of Biomedical Engineering, , Ben Gurion University of the Negev, ; 84105 Beer Sheva, Israel
                [4 ]GRID grid.7489.2, ISNI 0000 0004 1937 0511, Department of Cognitive and Brain Sciences, , Ben-Gurion University of the Negev, ; 84105 Beer Sheva, Israel
                [5 ]GRID grid.7489.2, ISNI 0000 0004 1937 0511, Department of Computer Sciences, , Ben Gurion University of the Negev, ; 84105 Beer Sheva, Israel
                Article
                71217
                10.1038/s41598-020-71217-1
                7479115
                31913322
                03ce697e-2ee5-4641-85c9-85ff0f3635b8
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 24 March 2020
                : 7 August 2020
                Funding
                Funded by: Israel Science Foundation
                Award ID: 281/15
                Funded by: Leona M. and Harry B. Helmsley Charitable Trust
                Funded by: Frankel center, Ben Gurion University of the Negev
                Funded by: Human Frontier Science Program
                Award ID: RGP0016/2019
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                neuroscience,spatial memory
                Uncategorized
                neuroscience, spatial memory

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