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.

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Emerging evidence suggests that our memories for recent events depend on a dynamic interplay between multiple cortical brain regions, although previous research has also emphasized a primary role for the hippocampus in episodic memory. One challenge in determining the relative importance of interactions between multiple brain regions versus a specific brain region is a lack of analytic approaches to address this issue. Participants underwent neuroimaging while retrieving the spatial and temporal details of a recently experienced virtual reality environment; we then employed graph theory to analyze functional connectivity patterns across multiple lobes. Dense, large-scale increases in connectivity during successful memory retrieval typified network topology, with individual participant performance correlating positively with overall network density. Within this dense network, the hippocampus, prefrontal cortex, precuneus, and visual cortex served as “hubs” of high connectivity. Spatial and temporal retrieval were characterized by distinct but overlapping “subnetworks” with higher connectivity within posterior and anterior brain areas, respectively. Together, these findings provide new insight into the neural basis of episodic memory, suggesting that the interactions of multiple hubs characterize successful memory retrieval. Furthermore, distinct subnetworks represent components of spatial versus temporal retrieval, with the hippocampus acting as a hub integrating information between these two subnetworks.

Current evidence strongly supports the central involvement of the human medial temporal lobes (MTL) in storing and retrieving memories for recently experienced events. However, a critical remaining question regards exactly how the hippocampus and surrounding cortex represents spatiotemporal context defining an event in memory. Competing accounts suggest that this process may be accomplished by the following: (1) an overall increase in neural similarity of representations underlying spatial and temporal context, (2) a differentiation of competing spatiotemporal representations, or (3) a combination of the two processes, with different subregions performing these two functions within the MTL. To address these competing proposals, we used high-resolution functional magnetic resonance imaging targeting the MTL along with a multivariate pattern similarity approach with 19 participants. While undergoing imaging, participants performed a task in which they retrieved spatial and temporal contextual representations from a recently learned experience. Results showed that successfully retrieving spatiotemporal context defining an episode involved a decrease in pattern similarity between putative spatial and temporal contextual representations in hippocampal subfields CA2/CA3/DG, whereas the parahippocampal cortex (PHC) showed the opposite pattern. These findings could not be accounted for by differences in univariate activations for complete versus partial retrieval nor differences in correlations for correct or incorrect retrieval. Together, these data suggest that the CA2/CA3/DG serves to differentiate competing contextual representations, whereas the PHC stores a comparatively integrated trace of scene-specific context, both of which likely play important roles in successful episodic memory retrieval.

Summary Low-frequency (delta/theta band) hippocampal neural oscillations play prominent roles in computational models of spatial navigation but their exact function remains unknown. Some theories propose they are primarily generated in response to sensorimotor processing while others suggest a role in memory-related processing. We directly recorded hippocampal EEG activity in patients undergoing seizure monitoring while they explored a virtual environment containing teleporters. Critically, this manipulation allowed patients to experience movement through space in the absence of visual and self-motion cues. The prevalence and duration of low-frequency hippocampal oscillations were unchanged by this manipulation, indicating that sensorimotor processing was not required to elicit them during navigation. Furthermore, the frequency-wise pattern of oscillation prevalence during teleportation contained spatial information capable of classifying the distance teleported. These results demonstrate that movement-related sensory information is not required to drive spatially informative low-frequency hippocampal oscillations during navigation and suggest a specific function in memory-related spatial updating.