High-gamma activity in the human hippocampus and parahippocampus during inter-trial rest periods of a virtual navigation task


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Abstract

In rodents, hippocampal cell assemblies formed during learning of a navigation task are observed to re-emerge during resting (offline) periods, accompanied by high-frequency oscillations (HFOs). This phenomenon is believed to reflect mechanisms for strengthening newly-formed memory traces. Using magnetoencephalography recordings and a beamforming source location algorithm (synthetic aperture magnetometry), we investigated high-gamma (80–140 Hz) oscillations in the hippocampal region in 18 human participants during inter-trial rest periods in a virtual navigation task. We found right hippocampal gamma oscillations mirrored the pattern of theta power in the same region during navigation, varying as a function of environmental novelty. Gamma power during inter-trial rest periods was positively correlated with theta power during navigation in the first task set when the environment was new and predicted greater performance improvement in the subsequent task set two where the environment became familiar. These findings provide evidence for human hippocampal reactivation accompanied by high-gamma activities immediately after learning and establish a link between hippocampal high-gamma activities and subsequent memory performance.HighlightsUsing non-invasive magnetoencephalography recordings and a highly translational virtual Morris water maze task, we show in humans that the hippocampal and parahippocampal region used for environmental encoding accompanied by low frequency theta oscillations is reactivated accompanied by high frequency high-gamma oscillations during inter-trial rest periods.High-gamma power during rest is correlated with theta power during navigation and predicts performance improvement in the subsequent task set.This study provides evidence for human hippocampal and parahippocampal reactivation accompanied by high-gamma activities immediately after learning for memory consolidation.

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