Theta activity supports landmark-based correction of naturalistic human path integration.

Abstract

How do humans integrate landmarks to update their spatial position during active navigation? Using immersive virtual reality and high-density mobile EEG, we investigated the neural underpinnings of landmark-based recalibration during path integration in freely moving male and female humans. Participants navigated predefined routes, indicated the start position to quantify accumulated errors, and once per route corrected their estimate using a visual landmark. Our findings reveal that homing error accumulated along the course of navigation, but a briefly presented intra-maze landmark effectively corrected accumulated errors. However, this effect was transient and less pronounced when participants were highly confident in their self-motion-based spatial representation suggesting that internal priors can hinder the assimilation of novel spatial cues. Theta activity in the retrosplenial complex supported the realignment of internal spatial representations by anchoring self-motion-derived estimates to visual landmark cues. Increased theta power and phase resetting upon landmark presentation accompanied subtle corrections, supporting a smooth realignment of spatial representations, whereas diminished synchronization marked the need for more extensive spatial updating. In addition, we identified motor-related theta response that scaled with rotational acceleration. Taken together, these findings highlight the dual role of theta oscillations in flexibly integrating multimodal signals, supporting both the recalibration of spatial representations to external cues and the encoding of self-motion information during naturalistic human navigation.Significance Statement Spatial navigation depends on the continuous integration of internally generated self-motion cues with external environmental landmarks to construct and maintain spatial representations. Despite its central role in adaptive behavior, the neural dynamics underlying this intermodal integration in humans remain unclear. Using noninvasive mobile EEG with immersive virtual reality, we identify a dynamic mechanism within the retrosplenial complex that realigns internal and external spatial representations based on visual landmarks during naturalistic navigation. This process is mediated by theta-band activity, which not only supports visuo-spatial realignment but also encodes vestibular signals. These dual theta signatures demonstrate how the human brain flexibly integrates multimodal information to update spatial representations, highlighting theta oscillations as a unifying neural substrate for both perceptual and motor components of navigation.