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      Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation

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          Abstract

          The hippocampus plays a vital role in various aspects of cognition including both memory and spatial navigation. To understand electrophysiologically how the hippocampus supports these processes, we recorded intracranial electroencephalographic activity from 46 neurosurgical patients as they performed a spatial memory task. We measure signals from multiple brain regions, including both left and right hippocampi, and we use spectral analysis to identify oscillatory patterns related to memory encoding and navigation. We show that in the left but not right hippocampus, the amplitude of oscillations in the 1–3-Hz “low theta” band increases when viewing subsequently remembered object–location pairs. In contrast, in the right but not left hippocampus, low-theta activity increases during periods of navigation. The frequencies of these hippocampal signals are slower than task-related signals in the neocortex. These results suggest that the human brain includes multiple lateralized oscillatory networks that support different aspects of cognition.

          Abstract

          Theta oscillations are implicated in memory formation. Here, the authors show that low-theta oscillations in the hippocampus are differentially modulated between each hemisphere, with oscillations in the left increasing when successfully learning object–location pairs and in the right during spatial navigation.

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          Most cited references58

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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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              Loss of recent memory after bilateral hippocampal lesions.

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                Author and article information

                Contributors
                joshua.jacobs@columbia.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                21 June 2018
                21 June 2018
                2018
                : 9
                : 2423
                Affiliations
                [1 ]ISNI 0000000419368729, GRID grid.21729.3f, Department of Biomedical Engineering, , Columbia University, ; 351 Engineering Terrace, Mail Code 8904, 1210 Amsterdam Avenue, New York, NY 10027 USA
                [2 ]ISNI 0000000419368729, GRID grid.21729.3f, Doctoral Program in Neurobiology and Behavior, , Columbia University, ; New York, 10027 NY USA
                [3 ]ISNI 0000 0001 2292 0500, GRID grid.37172.30, Department of Bio and Brain Engineering, , Korea Advanced Institute of Science and Technology, ; Daejeon, 34141 Korea
                [4 ]ISNI 0000 0001 2160 926X, GRID grid.39382.33, Department of Neurosurgery, , Baylor College of Medicine, ; Houston, 77030 TX USA
                [5 ]ISNI 0000 0001 2285 2675, GRID grid.239585.0, Department of Neurology, , Columbia University Medical Center, ; New York, 10032 NY USA
                [6 ]ISNI 0000 0001 2285 2675, GRID grid.239585.0, Department of Neurological Surgery, , Columbia University Medical Center, ; New York, 10032 NY USA
                [7 ]ISNI 0000 0001 2166 5843, GRID grid.265008.9, Department of Neurology, , Thomas Jefferson University, ; Philadelphia, 19107 PA USA
                [8 ]ISNI 0000 0001 2166 5843, GRID grid.265008.9, Department of Neurosurgery, , Thomas Jefferson University, ; Philadelphia, 19107 PA USA
                [9 ]ISNI 0000 0000 8819 4698, GRID grid.412571.4, Shiraz Neurosciences Research Center, , Shiraz University of Medical Sciences, ; Shiraz, 71348 Iran
                [10 ]ISNI 0000 0004 0459 167X, GRID grid.66875.3a, Department of Neurology, , Mayo Clinic, ; Rochester, 55905 MN USA
                [11 ]ISNI 0000 0001 2179 2404, GRID grid.254880.3, Department of Neurology, , Geisel School of Medicine at Dartmouth, ; Lebanon, 03756 NH USA
                [12 ]ISNI 0000 0001 0941 6502, GRID grid.189967.8, Emory University School of Medicine, ; Atlanta, 30322 GA USA
                [13 ]ISNI 0000 0004 0435 0884, GRID grid.411115.1, Department of Neurology, , Hospital of the University of Pennsylvania, ; Philadelphia, 19104 PA USA
                [14 ]ISNI 0000 0000 9482 7121, GRID grid.267313.2, University of Texas–Southwestern, ; Dallas, 75390 TX USA
                [15 ]ISNI 0000 0004 1936 8972, GRID grid.25879.31, Department of Psychology, , University of Pennsylvania, ; Philadelphia, 19104 PA USA
                [16 ]ISNI 0000 0004 0435 0884, GRID grid.411115.1, Department of Radiology, , Hospital of the University of Pennsylvania, ; Philadelphia, 19104 PA USA
                [17 ]ISNI 0000 0001 2166 5843, GRID grid.265008.9, Department of Radiology, , Thomas Jefferson University, ; Philadelphia, 19107 PA USA
                Author information
                http://orcid.org/0000-0002-7887-6067
                Article
                4847
                10.1038/s41467-018-04847-9
                6013427
                29930307
                ec8e4746-8a90-43f0-9ceb-600eb65a7b01
                © The Author(s) 2018

                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
                : 16 August 2017
                : 29 May 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000025, U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH);
                Award ID: MH104606
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000065, U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS);
                Award ID: 1S10OD018211-01
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000185, DOD | Defense Advanced Research Projects Agency (DARPA);
                Award ID: Cooperative Agreement N66001-14-2-4032
                Award Recipient :
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