Mobile deep brain recordings during real-world and imagined navigation

COEX 

Recent neurotechnological developments have enabled the study of real-world navigation in humans. Previous research in freely-moving rodents proposed a central role of the medial temporal lobe’s (MTL) involvement in spatial navigation and the formation of novel memory. Whether navigation and memory paradigms elicit functional similarities in the human MTL, which might generalize to more abstract cognitive domains such as imagination, remains unknown.
Here, we examined motion capture and intracranial electroencephalography (iEEG) from participants who had undergone chronic implantation of the responsive neurostimulation device, RNS System (NeuroPace, Inc.) for the treatment of epilepsy. We instructed participants to navigate two routes, including four turns each, in the real-world and imagine navigating the very same routes. Participants learned to perform this real-world spatial navigation task in an indoor room (14.6 × 13.5 m2) fully equipped with motion capture. Feedback on their performance was derived from motion capture and displayed on a tablet screen to refine their walking routes after each run by overlaying their actual movement trajectories recorded with motion capture on the ideal, instructed routes. After each actual walk, participants walked on a treadmill while imagining these walking routes in their minds.
Mobile iEEG was recorded from electrodes located in the deep brain within the MTL. In agreement with previous reports, transient theta oscillations were evident in each participant at spectral peaks in the 3-10 Hz frequency range. Short-lasting theta bouts frequently occurred at upcoming turns and formed temporal dynamics resembling the maze structure consistently across trials (30-35, left/right walks each). Similarly, we found that theta bouts occurred at specific time points during imagined navigation but not during sole treadmill walking, which we used as a control condition. These theta dynamics encoded the routes’ geometry comparably during real-world and imagined navigation. In both types of navigation, temporally structured theta bouts were present at the same anatomical locations, suggesting the involvement of similar functional networks supporting real-world and imagined navigation. Visual flow was absent during imagined navigation and bodily cues were identical to sole treadmill walking. Therefore, these findings demonstrate the capability of the MTL to internally generate theta dynamics relevant for memory retrieval and spontaneous imagination in the absence of environmental cues.
Altogether, our results open up novel avenues to study real-world spatial navigation, episodic memory, imagination, and possible future behaviors. The non-continuous but structured nature of human theta oscillations we report enables the opportunity to compare the timing and structure of these transient oscillations across cognitive tasks and behaviors. In studies including human participants, imaginations can be instructed and verbally reported, allowing the investigation of the neural mechanisms of abstract, hypothetical, or unprecedented future scenarios parallel to real-world behaviors.