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      Transformation of the head-direction signal into a spatial code

      , 1 , 2 , 1 , 4 , , 1 , 3

      Nature Communications

      Nature Publishing Group UK

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          Abstract

          Animals integrate multiple sensory inputs to successfully navigate in their environments. Head direction (HD), boundary vector, grid and place cells in the entorhinal-hippocampal network form the brain’s navigational system that allows to identify the animal’s current location, but how the functions of these specialized neuron types are acquired remain to be understood. Here we report that activity of HD neurons is influenced by the ambulatory constraints imposed upon the animal by the boundaries of the explored environment, leading to spurious spatial information. However, in the post-subiculum, the main cortical stage of HD signal processing, HD neurons convey true spatial information in the form of border modulated activity through the integration of additional sensory modalities relative to egocentric position, unlike their driving thalamic inputs. These findings demonstrate how the combination of HD and egocentric information can be transduced into a spatial code.

          Abstract

          A cognitive map of space must integrate allocentric cues such as head direction (HD) with various egocentric cues. Here the authors report that anterior thalamic (ADn) neurons encode a pure HD signal, while neurons in post-subiculum represent a conjunction of HD and egocentric cues such as body posture with respect to environment boundaries.

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          Most cited references 61

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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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            Theta oscillations in the hippocampus.

            Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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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
                adrien.peyrache@mcgill.ca
                gyorgy.buzsaki@nyumc.org
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                24 November 2017
                24 November 2017
                2017
                : 8
                Affiliations
                [1 ]ISNI 0000 0004 1936 8753, GRID grid.137628.9, Neuroscience Institute, School of Medicine, ; New York University, 450 East 29th Street, New York City, New York 10016 USA
                [2 ]ISNI 0000 0004 1936 8649, GRID grid.14709.3b, Department of Neurology and Neurosurgery, , Montreal Neurological Institute, McGill University, ; 3801 University Street, Montreal, Quebec Canada H3A 2B4
                [3 ]Center for Neuroscience, New York University, New York City, New York 10016 USA
                [4 ]ISNI 0000 0001 2248 7639, GRID grid.7468.d, Present Address: Institute for Theoretical Biology, , Department of Biology, Humboldt-Universität zu Berlin, ; 10115 Berlin, Germany
                Article
                1908
                10.1038/s41467-017-01908-3
                5700966
                29170377
                © The Author(s) 2017

                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/.

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