Frontal-midline theta and posterior alpha oscillations index early processing of spatial representations during active navigation

Abstract

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.

Theta and alpha oscillations in human hippocampus and medial parietal cortex support the formation of location‐based representations

“…Theta power changes during memory encoding often localize to the medial temporal lobes (among other structures), including the hippocampus and parahippocampal regions (Backus et al, 2016;Crespo-García et al, 2016;Fellner et al, 2016Fellner et al, , 2019Griffiths et al, 2016;Hanslmayr et al, 2011;Staudigl & Hanslmayr, 2013). Note, this theta effect is likely distinct from frontal mid-line theta, found during cognitive control and working memory tasks, which typically localizes to medial prefrontal regions (Chrastil et al, 2022;Du et al, 2023;Summerfield & Mangels, 2005;Zuure et al, 2020). Thus, a large body of evidence exists for the role of theta in forming associations between information in both spatial and non-spatial contexts.…”

“…Specifically, changes in theta oscillatory power have been observed on the scalp during learning of specific items (words/pictures/scenes; Fellner et al, 2013Fellner et al, , 2019Guderian et al, 2009;Hanslmayr et al, 2009Hanslmayr et al, , 2011Khader et al, 2010;Osipova et al, 2006), lists of items (Fellner et al, 2016;Griffiths et al, 2016;Meeuwissen et al, 2011;Sederberg et al, 2006), and during associative learning (Backus et al, 2016;Caplan & Glaholt, 2007;Crespo-García et al, 2016;Griffiths et al, 2016;Joensen et al, 2023;Staudigl & Hanslmayr, 2013;Summerfield & Mangels, 2005). Theta power changes have also been found when participants learn spatial layouts as they combine sensory input in new environments compared to when they freely explore a new spatial layout in the absence of an overt task (Chrastil et al, 2022;Du et al, 2023;Kaplan et al, 2012;Pu et al, 2017). Therefore, a large body of evidence indicates that theta power changes observed on the scalp are important for both nonspatial (episodic) and spatial memory formation.…”

Theta and alpha oscillations in human hippocampus and medial parietal cortex support the formation of location-based representations

“…Theta power changes during memory encoding often localise to the medial temporal lobes (among other structures), including the hippocampus and parahippocampal regions (Backus et al, 2016;Crespo-García et al, 2016;Fellner et al, 2016Fellner et al, , 2019Griffiths et al, 2016;Hanslmayr et al, 2011;Staudigl & Hanslmayr, 2013). Note, this theta effect is likely distinct from frontal mid-line theta, found during cognitive control and working memory tasks, which typically localises to medial prefrontal regions (Chrastil et al, 2022;Du et al, 2023;Summerfield & Mangels, 2005;Zuure et al, 2020). Thus, a large body of evidence exists for the role of theta in forming associations between information in both spatial and non-spatial contexts.…”

“…Specifically, changes in theta oscillatory power have been observed on the scalp during learning of specific items (words/pictures/scenes; Fellner et al, 2013Fellner et al, , 2019Guderian et al, 2009;Hanslmayr et al, 2009Hanslmayr et al, , 2011Khader et al, 2010;Osipova et al, 2006), lists of items (Fellner et al, 2016;Griffiths et al, 2016;Meeuwissen et al, 2011;Sederberg et al, 2006), and during associative learning (Backus et al, 2016;Caplan & Glaholt, 2007;Crespo-García et al, 2016;Griffiths et al, 2016;Joensen et al, 2023;Staudigl & Hanslmayr, 2013;Summerfield & Mangels, 2005). Theta power changes have also been found when participants learn spatial layouts as they combine sensory input in new environments compared to when they freely explore a new spatial layout in the absence of an overt task (Chrastil et al, 2022;Du et al, 2023;Kaplan et al, 2012;Pu et al, 2017). Therefore, a large body of evidence indicates that theta power changes observed on the scalp are important for both non-spatial (episodic) and spatial memory formation.…”