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      Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation

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          Abstract

          Low-Frequency Oscillations (LFO) in the range of 7–9 Hz, or theta rhythm, has been recorded in rodents ambulating in the real world. However, intra-hippocampus EEG recordings during virtual navigation in humans have consistently reported LFO that appear to predominate around 3–4 Hz. Here we report clear evidence of 7–9 Hz rhythmicity in raw intra-hippocampus EEG traces during real as well as virtual movement. Oscillations typically occur at a lower frequency in virtual than real world navigation. This study highlights the possibility that human and rodent hippocampal EEG activity are not as different as previously reported and this difference may arise, in part, due to the lack of actual movement in previous human navigation studies, which were virtual.

          Abstract

          Rhythmic oscillations in theta frequency range (7–9 Hz) are observed in rodents during navigation. Here the authors demonstrate robust similar theta rhythmicity in human hippocampus during both real and virtual movements.

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          Most cited references 25

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          Hippocampal electrical activity and voluntary movement in the rat.

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            Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice.

            The human brain activity related to strategies for navigating in space and how it changes with practice was investigated with functional magnetic resonance imaging. Subjects used two different strategies to solve a place-learning task in a computer-generated virtual environment. One-half of the subjects used spatial landmarks to navigate in the early phase of training, and these subjects showed increased activation of the right hippocampus. The other half used a nonspatial strategy and showed, with practice, sustained increased activity within the caudate nucleus during navigation. Activation common to both groups was observed in the posterior parietal and frontal cortex. These results provide the first evidence for spontaneous variability and shift in neural mechanisms during navigation in humans.
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              Loss of hippocampal theta rhythm results in spatial memory deficit in the rat.

               J Winson (1978)
              Rats learned, using distal room cues, to run to a goal on an elevated, circular track starting from any position on the track. The goal was one of eight equidistant, recessed cups set around the track, the goal cup being distinguished from the others solely by its position in the room. After learning, electrolytic lesions were made in the medial septal nucleus eliminating hippocampal theta rhythm in some animals but not in others. Rats without theta rhythm were no longer able to perform the spatial task, whereas rats with undisturbed theta rhythm retrained normal performance. Although rats without theta rhythm could not find their way directly to the goal, they recognized its location when they came upon it by chance. This type of spatial deficit appears similar to that shown by hippocampally lesioned patient H.M. Subsequent tests demonstrated that rats deprived of theta rhythm before training could nevertheless learn the task.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                14 February 2017
                2017
                : 8
                Affiliations
                [1 ]Douglas Institute, Department of Psychiatry, McGill University , 6875 boulevard LaSalle, Verdun, Quebec, Canada H4H 1R3
                [2 ]Neuroscience Graduate Group, University of California , Davis, 1 Shields Avenue, Davis, California 95616, USA
                [3 ]Montreal Neurological Institute, McGill University , 3801 University Street, Montreal, Quebec, Canada H3A 2B4
                [4 ]Center for Neuroscience, University of California , Davis, 1 Shields Avenue, Davis, California 95618, USA
                [5 ]Department of Psychology, University of California , Davis, 1 Shields Avenue, Davis, California 95618, USA
                Author notes
                Article
                ncomms14415
                10.1038/ncomms14415
                5316881
                28195129
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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