Abstract

Author SummaryNeural activity both within and across brain regions can oscillate in different frequency ranges (such as alpha, gamma, and theta frequencies), and these different ranges are associated with distinct functions. In behaving rodents, for example, theta rhythms (4–12 Hz) in the hippocampus are prominent during the initiation of movement and have been linked to spatial exploration. Recent evidence in humans, however, suggests that the human hippocampus is involved in guiding self-directed learning. This suggests that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. In this study, we tested whether there is a human analogue for the movement-initiation-related theta rhythm found in the rodent hippocampus by using a virtual navigation paradigm, combined with non-invasive recordings and functional imaging techniques. Our recordings showed that, indeed, theta power increases are linked to movement initiation. We also examined the relationship to memory encoding, and we found that hippocampal theta oscillations related to pre-retrieval planning predicted memory performance. Imaging results revealed that periods of the task showing movement-related theta also showed increased activity in the hippocampus, as well as other brain regions associated with self-directed learning. These findings directly extend the role of the hippocampal theta rhythm in rodent spatial exploration to human memory and self-directed learning.

Highlights

  • Spatial exploration provides an ecologically valid experimental paradigm to investigate volitional behaviour and cognition across different species

  • Some studies have measured hippocampal theta during virtual navigation tasks [18,19,20,21], and these interactive. Neural activity both within and across brain regions can oscillate in different frequency ranges, and these different ranges are associated with distinct functions

  • For example, theta rhythms (4–12 Hz) in the hippocampus are prominent during the initiation of movement and have been linked to spatial exploration

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Summary

Introduction

Spatial exploration provides an ecologically valid experimental paradigm to investigate volitional behaviour and cognition across different species. The theta rhythm (,4–12 Hz) dominates the hippocampal local field potential (LFP) during translational motion, prominent during initiation of movement [1,2,3], and has been associated with the encoding and behavioural control of memories [4,5]. Movement-related theta in rodents is modulated by environmental novelty [6] and has shown a correlation between age-related memory decline and decreased amplitude [7]. In human memory there has been a slightly different examination of volitional behaviour. The ability to self-initiate memory behaviours was observed as a crucial biomarker for age-related memory decline [10] and more recently the human hippocampus was observed to be a network hub for the volitional control of memory encoding [11]. Some studies have measured hippocampal theta during virtual navigation tasks [18,19,20,21], and these interactive

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