Numerous reports have demonstrated low-frequency oscillations during navigation using invasive recordings in the hippocampus of both rats and human patients. Given evidence, in some cases, of low-frequency synchronization between midline cortex and hippocampus, it is also possible that low-frequency movement-related oscillations manifest in healthy human neocortex. However, this possibility remains largely unexplored, in part due to the difficulties of coupling free ambulation and effective scalp EEG recordings. In the current study, participants freely ambulated on an omnidirectional treadmill and explored an immersive virtual reality city rendered on a head-mounted display while undergoing simultaneous wireless scalp EEG recordings. We found that frontal-midline (FM) delta-theta (2-7.21 Hz) oscillations increased during movement compared to standing still periods, consistent with a role in navigation. In contrast, posterior alpha (8.32-12.76 Hz) oscillations were suppressed in the presence of visual input, independent of movement. Our findings suggest that FM delta-theta and posterior alpha oscillations arise at independent frequencies, under complementary behavioral conditions, and, at least for FM delta-theta oscillations, at independent recordings sites. Together, our findings support a double dissociation between movement-related FM delta-theta and resting-related posterior alpha oscillations. Our study thus provides novel evidence that FM delta-theta oscillations arise, in part, from real-world ambulation, and are functionally independent from posterior alpha oscillations.

Judging how far something is and how long it takes to get there is critical to memory and navigation. Yet, the neural codes for spatial and temporal information remain unclear, particularly the involvement of neural oscillations in maintaining such codes. To address these issues, we designed an immersive virtual reality environment containing teleporters that displace participants to a different location after entry. Upon exiting the teleporters, participants made judgments from two given options regarding either the distance they had traveled (spatial distance condition) or the duration they had spent inside the teleporters (temporal duration condition). We wirelessly recorded scalp EEG while participants navigated in the virtual environment by physically walking on an omnidirectional treadmill and traveling through teleporters. An exploratory analysis revealed significantly higher alpha and beta power for short-distance versus long-distance traversals, whereas the contrast also revealed significantly higher frontal midline delta–theta–alpha power and global beta power increases for short versus long temporal duration teleportation. Analyses of occipital alpha instantaneous frequencies revealed their sensitivity for both spatial distances and temporal durations, suggesting a novel and common mechanism for both spatial and temporal coding. We further examined the resolution of distance and temporal coding by classifying discretized distance bins and 250-msec time bins based on multivariate patterns of 2- to 30-Hz power spectra, finding evidence that oscillations code fine-scale time and distance information. Together, these findings support partially independent coding schemes for spatial and temporal information, suggesting that low-frequency oscillations play important roles in coding both space and time.

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Previous research has demonstrated that humans combine multiple sources of spatial information, such as allothetic and idiothetic cues, while navigating through an environment. However, it is unclear whether this involves comparing multiple representations from multiple sources during encoding (parallel hypothesis) or primarily accumulating idiothetic information until the end of the navigation to integrate with allothetic information (serial hypothesis). We tested these two hypotheses in an active navigation task using mobile scalp EEG recordings. Participants walked through an immersive virtual hallway with or without conflicts between allothetic and idiothetic cues and pointed toward the starting position of the hallway. By analyzing the scalp oscillatory activities during the navigation phase, we found that path segments including memory anchors -- such as path intersections -- were more strongly associated with the pointing error, regardless of when they appeared during encoding. This indicates that the integration of spatial information of a walked path likely begins in the early stages of navigation rather in late stages alone, supporting the parallel hypothesis. Furthermore, theta oscillations in frontal-midline regions during active navigation were related to memory of the path rather than only movement through the path, supporting a mnemonic role of theta oscillations.

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