EEG correlates of spatial orientation in the human retrosplenial complex

© 2015 Elsevier Inc. Studies on spatial navigation reliably demonstrate that the retrosplenial complex (RSC) plays a pivotal role for allocentric spatial information processing by transforming egocentric and allocentric spatial information into the respective other spatial reference frame (SRF). While more and more imaging studies investigate the role of the RSC in spatial tasks, high temporal resolution measures such as electroencephalography (EEG) are missing. To investigate the function of the RSC in spatial navigation with high temporal resolution we used EEG to analyze spectral perturbations during navigation based on allocentric and egocentric SRF. Participants performed a path integration task in a clearly structured virtual environment providing allothetic information. Continuous EEG recordings were decomposed by independent component analysis (ICA) with subsequent source reconstruction of independent time source series using equivalent dipole modeling. Time-frequency transformation was used to investigate reference frame-specific orientation processes during navigation as compared to a control condition with identical visual input but no orientation task. Our results demonstrate that navigation based on an egocentric reference frame recruited a network including the parietal, motor, and occipital cortices with dominant perturbations in the alpha band and theta modulation in frontal cortex. Allocentric navigation was accompanied by performance-related desynchronization of the 8-13. Hz frequency band and synchronization in the 12-14. Hz band in the RSC. The results support the claim that the retrosplenial complex is central to translating egocentric spatial information into allocentric reference frames. Modulations in different frequencies with different time courses in the RSC further provide first evidence of two distinct neural processes reflecting translation of spatial information based on distinct reference frames and the computation of heading changes

Brain Dynamics of Spatial Reference Frame Proclivity in Active Navigation.

Recent research into navigation strategy of different spatial reference frames (self-centered egocentric reference frame and environment-centered allocentric reference frame) has revealed that the parietal cortex plays an important role in processing allocentric information to provide a translation function between egocentric and allocentric spatial reference frames. However, most studies merely focused on a passive experimental environment, which is not truly representative of our daily spatial learning/navigation tasks. This study investigated the factor associated with brain dynamics that causes people to switch their preferred spatial strategy in both active and passive navigations to bridge the gap. Virtual reality (VR) technique and Omni treadmill are applied to realize actively walking for active navigation, and for passive navigation, participants were sitting while conducting the same task. Electroencephalography (EEG) signals were recorded to monitor spectral perturbations on transitions between egocentric and allocentric frames during a path integration task. Forty-one right-handed male participants from authors' university participated this study. Our brain dynamics results showed navigation involved areas including the parietal cortex with modulation in the alpha band, the occipital cortex with beta and low gamma band perturbations, and the frontal cortex with theta perturbation. Differences were found between two different turning-angle paths in the alpha band in parietal cluster event-related spectral perturbations (ERSPs). In small turning-angle paths, allocentric participants showed stronger alpha desynchronization than egocentric participants; in large turning-angle paths, participants for two reference frames had a smaller difference in the alpha frequency band. Behavior results of homing errors also corresponded to brain dynamic results, indicating that a larger angle path caused the allocentric to have a higher tendency to become egocentric navigators in the active navigation environment

Cultural background shapes spatial reference frame proclivity

Spatial navigation is an essential human skill that is influenced by several factors. The present study investigates how gender, age, and cultural background account for differences in reference frame proclivity and performance in a virtual navigation task. Using an online navigation study, we recorded reaction times, error rates (confusion of turning axis), and reference frame proclivity (egocentric vs. allocentric reference frame) of 1823 participants. Reaction times significantly varied with gender and age, but were only marginally influenced by the cultural background of participants. Error rates were in line with these results and exhibited a significant influence of gender and culture, but not age. Participants cultural background significantly influenced reference frame selection; the majority of North-Americans preferred an allocentric strategy, while Latin-Americans preferred an egocentric navigation strategy. European and Asian groups were in between these two extremes. Neither the factor of age nor the factor of gender had a direct impact on participants navigation strategies. The strong effects of cultural background on navigation strategies without the influence of gender or age underlines the importance of socialized spatial cognitive processes and argues for socio-economic analysis in studies investigating human navigation

Cultural background shapes spatial reference frame proclivity

Spatial navigation is an essential human skill that is influenced by several factors. The present study investigates how gender, age, and cultural background account for differences in reference frame proclivity and performance in a virtual navigation task. Using an online navigation study, we recorded reaction times, error rates (confusion of turning axis), and reference frame proclivity (egocentric vs. allocentric reference frame) of 1823 participants. Reaction times significantly varied with gender and age, but were only marginally influenced by the cultural background of participants. Error rates were in line with these results and exhibited a significant influence of gender and culture, but not age. Participants’ cultural background significantly influenced reference frame selection; the majority of North-Americans preferred an allocentric strategy, while Latin-Americans preferred an egocentric navigation strategy. European and Asian groups were in between these two extremes. Neither the factor of age nor the factor of gender had a direct impact on participants’ navigation strategies. The strong effects of cultural background on navigation strategies without the influence of gender or age underlines the importance of socialized spatial cognitive processes and argues for socio-economic analysis in studies investigating human navigation.This work was funded by the European research grant: ERC- 2010-AdG #269716 – MULTISENSE, together with the Cognition and Neuroergonomics/Collaborative Technology Alliance #W911NF-10-2-0022

Lost in spatial translation - A novel tool to objectively assess spatial disorientation in Alzheimer's disease and frontotemporal dementia

Spatial disorientation is a prominent feature of early Alzheimer's disease (AD) attributed to degeneration of medial temporal and parietal brain regions, including the retrosplenial cortex (RSC). By contrast, frontotemporal dementia (FTD) syndromes show generally intact spatial orientation at presentation. However, currently no clinical tasks are routinely administered to objectively assess spatial orientation in these neurodegenerative conditions. In this study we investigated spatial orientation in 58 dementia patients and 23 healthy controls using a novel virtual supermarket task as well as voxel-based morphometry (VBM). We compared performance on this task with visual and verbal memory function, which has traditionally been used to discriminate between AD and FTD. Participants viewed a series of videos from a first person perspective travelling through a virtual supermarket and were required to maintain orientation to a starting location. Analyses revealed significantly impaired spatial orientation in AD, compared to FTD patient groups. Spatial orientation performance was found to discriminate AD and FTD patient groups to a very high degree at presentation. More importantly, integrity of the RSC was identified as a key neural correlate of orientation performance. These findings confirm the notion that i) it is feasible to assess spatial orientation objectively via our novel Supermarket task; ii) impaired orientation is a prominent feature that can be applied clinically to discriminate between AD and FTD and iii) the RSC emerges as a critical biomarker to assess spatial orientation deficits in these neurodegenerative conditions

Orientation and metacognition in virtual space

Cognitive scientists increasingly use virtual reality scenarios to address spatial perception, orientation, and navigation. If based on desktops rather than mobile immersive environments, this involves a discrepancy between the physically experienced static position and the visually perceived dynamic scene, leading to cognitive challenges that users of virtual worlds may or may not be aware of. The frequently reported loss of orientation and worse performance in point-to-origin tasks relate to the difficulty of establishing a consistent reference system on an allocentric or egocentric basis. We address the verbalisability of spatial concepts relevant in this regard, along with the conscious strategies reported by participants. Behavioural and verbal data were collected using a perceptually sparse virtual tunnel scenario that has frequently been used to differentiate between humans' preferred reference systems. Surprisingly, the linguistic data we collected relate to reference system verbalisations known from the earlier literature only to a limited extent, but instead reveal complex cognitive mechanisms and strategies. Orientation in desktop VR appears to pose considerable challenges, which participants react to by conceptualising the task in individual ways that do not systematically relate to the generic concepts of egocentric and allocentric reference frames

Anterior/Posterior Competitive Deactivation/Activation Dichotomy in the Human Hippocampus as Revealed by a 3D Navigation Task

Anterior/posterior long axis specialization is thought to underlie the organization of the hippocampus. However it remains unclear whether antagonistic mechanisms differentially modulate processing of spatial information within the hippocampus. We used fMRI and a virtual reality 3D paradigm to study encoding and retrieval of spatial memory during active visuospatial navigation, requiring positional encoding and retrieval of object landmarks during the path. Both encoding and retrieval elicited BOLD activation of the posterior most portion of hippocampus, while concurrent deactivations (recently shown to reflect decreases in neural responses) were found in the most anterior regions. Encoding elicited stronger activity in the posterior right than the left hippocampus. The former structure also showed significantly stronger activity for allocentric vs. egocentric processing during retrieval. The anterior vs. posterior pattern mimics, from a functional point, although at much distinct temporal scales, the previous anatomical findings in London taxi drivers, whereby posterior enlargement was found at the cost of an anterior decrease, and the mirror symmetric findings observed in blind people, in whom the right anterior hippocampus was found to be larger, at the cost of a smaller posterior hippocampus, as compared with sighted people. In sum, we found a functional dichotomy whereby the anterior/posterior hippocampus shows antagonistic processing patterns for spatial encoding and retrieval of 3D spatial information. To our knowledge, this is the first study reporting such a dynamical pattern in a functional study, which suggests that differential modulation of neural responses within the human hippocampus reflects distinct roles in spatial memory processing

Single‐trial regression of spatial exploration behavior indicates posterior EEG alpha modulation to reflect egocentric coding

Learning to navigate uncharted terrain is a key cognitive ability that emerges as a deeply embodied process, with eye movements and locomotion proving most useful to sample the environment. We studied healthy human participants during active spatial learning of room-scale virtual reality (VR) mazes. In the invisible maze task, participants wearing a wireless electroencephalography (EEG) headset were free to explore their surroundings, only given the objective to build and foster a mental spatial representation of their environment. Spatial uncertainty was resolved by touching otherwise invisible walls that were briefly rendered visible inside VR, similar to finding your way in the dark. We showcase the capabilities of mobile brain/body imaging using VR, demonstrating several analysis approaches based on general linear models (GLMs) to reveal behavior-dependent brain dynamics. Confirming spatial learning via drawn sketch maps, we employed motion capture to image spatial exploration behavior describing a shift from initial exploration to subsequent exploitation of the mental representation. Using independent component analysis, the current work specifically targeted oscillations in response to wall touches reflecting isolated spatial learning events arising in deep posterior EEG sources located in the retrosplenial complex. Single-trial regression identified significant modulation of alpha oscillations by the immediate, egocentric, exploration behavior. When encountering novel walls, as well as with increasing walking distance between subsequent touches when encountering novel walls, alpha power decreased. We conclude that these oscillations play a prominent role during egocentric evidencing of allocentric spatial hypotheses