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      Functional connectivity changes in the entorhinal cortex of taxi drivers

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          Abstract

          Introduction

          As a major interface between the hippocampus and the neocortex, the entorhinal cortex (EC) is widely known to play a pivotal role in spatial memory and navigation. Previous studies have suggested that the EC can be divided into the anterior‐lateral (alEC) and the posterior‐medial subregions (pmEC), with the former receiving object‐related information from the perirhinal cortex and the latter receiving scene‐related information from the parahippocampal cortex. However, the functional connectivity maps of the EC subregions in the context of extensive navigation experience remain elusive. In this study, we analyzed the functional connectivity of the EC in subjects with long‐term navigation experience and aimed to find the navigation‐related change in the functional properties of the human EC.

          Methods

          We investigated the resting‐state functional connectivity changes in the EC subregions by comparing the EC functional connectivity maps of 20 taxi drivers with those of 20 nondriver controls. Furthermore, we examined whether the functional connectivity changes of the EC were related to the number of taxi driving years.

          Results

          Significantly reduced functional connectivity was found in the taxi drivers between the left pmEC and the right anterior cingulate cortex (ACC), right angular gyrus, and bilateral precuneus as well as some temporal regions, and between the right pmEC and the left inferior temporal gyrus. Notably, the strength of the functional connectivity between the left pmEC and the left precuneus, as well as the right ACC, was negatively correlated with the years of taxi driving.

          Conclusion

          This is the first study to explore the impact of long‐term navigation experience on the connectivity patterns of the EC, the results of which may shed new light on the potential influence of extensive navigational training on the functional organization of the EC in healthy human brains.

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          Most cited references34

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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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            The human hippocampus and spatial and episodic memory.

            Finding one's way around an environment and remembering the events that occur within it are crucial cognitive abilities that have been linked to the hippocampus and medial temporal lobes. Our review of neuropsychological, behavioral, and neuroimaging studies of human hippocampal involvement in spatial memory concentrates on three important concepts in this field: spatial frameworks, dimensionality, and orientation and self-motion. We also compare variation in hippocampal structure and function across and within species. We discuss how its spatial role relates to its accepted role in episodic memory. Five related studies use virtual reality to examine these two types of memory in ecologically valid situations. While processing of spatial scenes involves the parahippocampus, the right hippocampus appears particularly involved in memory for locations within an environment, with the left hippocampus more involved in context-dependent episodic or autobiographical memory.
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              Conjunctive representation of position, direction, and velocity in entorhinal cortex.

              Grid cells in the medial entorhinal cortex (MEC) are part of an environment-independent spatial coordinate system. To determine how information about location, direction, and distance is integrated in the grid-cell network, we recorded from each principal cell layer of MEC in rats that explored two-dimensional environments. Whereas layer II was predominated by grid cells, grid cells colocalized with head-direction cells and conjunctive grid x head-direction cells in the deeper layers. All cell types were modulated by running speed. The conjunction of positional, directional, and translational information in a single MEC cell type may enable grid coordinates to be updated during self-motion-based navigation.
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                Author and article information

                Contributors
                lihongwrm@vip.sina.com
                dwhu@nudt.edu.cn
                Journal
                Brain Behav
                Brain Behav
                10.1002/(ISSN)2157-9032
                BRB3
                Brain and Behavior
                John Wiley and Sons Inc. (Hoboken )
                2162-3279
                15 August 2018
                September 2018
                : 8
                : 9 ( doiID: 10.1002/brb3.2018.8.issue-9 )
                : e01022
                Affiliations
                [ 1 ] College of Mechatronics and Automation National University of Defense Technology Changsha Hunan China
                [ 2 ] Research Centre of Brain Function and Psychological Science Shenzhen University Shenzhen Guangdong China
                [ 3 ] Cognitive and Mental Health Research Center Beijing Institute of Basic Medical Sciences Beijing China
                Author notes
                [*] [* ] Correspondence

                Hong Li, Research Centre of Brain Function and Psychological Science, Shenzhen University, Shenzhen, Guangdong, 518060, China.

                Email: lihongwrm@ 123456vip.sina.com

                Dewen Hu, College of Mechatronics and Automation, National University of Defense Technology, Changsha, Hunan, 410073, China.

                Email: dwhu@ 123456nudt.edu.cn

                [†]

                These authors contributed equally to this paper.

                Author information
                http://orcid.org/0000-0003-4273-0717
                http://orcid.org/0000-0002-0515-256X
                http://orcid.org/0000-0002-5582-4555
                Article
                BRB31022
                10.1002/brb3.1022
                6160637
                30112812
                173cdf19-b4d7-47c1-b617-b619479accac
                © 2018 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 December 2017
                : 01 May 2018
                : 09 May 2018
                Page count
                Figures: 4, Tables: 2, Pages: 9, Words: 6347
                Funding
                Funded by: National Natural Science Foundation of China
                Award ID: 61420106001
                Award ID: 61503397
                Award ID: 61722313
                Award ID: 61773391
                Funded by: Fok Ying Tung Education Foundation
                Award ID: 161057
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                brb31022
                September 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.9 mode:remove_FC converted:28.09.2018

                Neurosciences
                entorhinal cortex,fmri,functional connectivity,navigation,resting‐state
                Neurosciences
                entorhinal cortex, fmri, functional connectivity, navigation, resting‐state

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