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      The Hippocampus and Entorhinal Cortex Encode the Path and Euclidean Distances to Goals during Navigation

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          Summary

          Background

          Despite decades of research on spatial memory, we know surprisingly little about how the brain guides navigation to goals. While some models argue that vectors are represented for navigational guidance, other models postulate that the future path is computed. Although the hippocampal formation has been implicated in processing spatial goal information, it remains unclear whether this region processes path- or vector-related information.

          Results

          We report neuroimaging data collected from subjects navigating London’s Soho district; these data reveal that both the path distance and the Euclidean distance to the goal are encoded by the medial temporal lobe during navigation. While activity in the posterior hippocampus was sensitive to the distance along the path, activity in the entorhinal cortex was correlated with the Euclidean distance component of a vector to the goal. During travel periods, posterior hippocampal activity increased as the path to the goal became longer, but at decision points, activity in this region increased as the path to the goal became closer and more direct. Importantly, sensitivity to the distance was abolished in these brain areas when travel was guided by external cues.

          Conclusions

          The results indicate that the hippocampal formation contains representations of both the Euclidean distance and the path distance to goals during navigation. These findings argue that the hippocampal formation houses a flexible guidance system that changes how it represents distance to the goal depending on the fluctuating demands of navigation.

          Graphical Abstract

          Highlights

          • The hippocampus represents both the path and the Euclidean distances to goals

          • Entorhinal activity reflects the change in the Euclidean distance when the goal is set

          • The posterior hippocampus represents the future path at different stages en route

          • Significant correlations are abolished when travel is guided by external cues

          Abstract

          Howard et al. reveal that during the navigation of a simulated real-word environment, hippocampal and entorhinal activity is correlated with the distance to the goal. The posterior hippocampus encodes the path during travel, decision making, and detours. The entorhinal cortex encodes the distance along the vector when the goal is set.

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          Most cited references39

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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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            Long-axis specialization of the human hippocampus.

            Investigation of the hippocampus has historically focused on computations within the trisynaptic circuit. However, discovery of important anatomical and functional variability along its long axis has inspired recent proposals of long-axis functional specialization in both the animal and human literatures. Here, we review and evaluate these proposals. We suggest that various long-axis specializations arise out of differences between the anterior (aHPC) and posterior hippocampus (pHPC) in large-scale network connectivity, the organization of entorhinal grid cells, and subfield compositions that bias the aHPC and pHPC towards pattern completion and separation, respectively. The latter two differences give rise to a property, reflected in the expression of multiple other functional specializations, of coarse, global representations in anterior hippocampus and fine-grained, local representations in posterior hippocampus. Crown Copyright © 2013. Published by Elsevier Ltd. All rights reserved.
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              Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point.

              Neural ensembles were recorded from the CA3 region of rats running on T-based decision tasks. Examination of neural representations of space at fast time scales revealed a transient but repeatable phenomenon as rats made a decision: the location reconstructed from the neural ensemble swept forward, first down one path and then the other. Estimated representations were coherent and preferentially swept ahead of the animal rather than behind the animal, implying it represented future possibilities rather than recently traveled paths. Similar phenomena occurred at other important decisions (such as in recovery from an error). Local field potentials from these sites contained pronounced theta and gamma frequencies, but no sharp wave frequencies. Forward-shifted spatial representations were influenced by task demands and experience. These data suggest that the hippocampus does not represent space as a passive computation, but rather that hippocampal spatial processing is an active process likely regulated by cognitive mechanisms.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                16 June 2014
                16 June 2014
                : 24
                : 12
                : 1331-1340
                Affiliations
                [1 ]UCL Institute of Behavioural Neuroscience, Research Department of Experimental Psychology, Division of Psychology and Language Sciences, University College London, London WC1H 0AP, UK
                [2 ]Aging & Cognition Research Group, German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany
                [3 ]UCL Centre for Advanced Biomedical Imaging, University College London, London WC1E 6DD, UK
                [4 ]School of Psychology & Neuroscience, University of St. Andrews, Fife KY16 9JP, UK
                [5 ]Department of Psychology, University of Hertfordshire, Hertfordshire AL10 9AB, UK
                Author notes
                []Corresponding author h.spiers@ 123456ucl.ac.uk
                Article
                S0960-9822(14)00526-0
                10.1016/j.cub.2014.05.001
                4062938
                24909328
                7a0fcc09-fb24-4c66-900a-19f07a7e6111
                © 2014 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

                History
                : 9 December 2013
                : 8 April 2014
                : 1 May 2014
                Categories
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                Life sciences
                Life sciences

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