Mobile brain/body imaging of landmark‐based navigation with high‐density EEG

Coupling behavioral measures and brain imaging in naturalistic, ecological conditions is key to comprehend the neural bases of spatial navigation. This highly integrative function encompasses sensorimotor, cognitive, and executive processes that jointly mediate active exploration and spatial learning. However, most neuroimaging approaches in humans are based on static, motion-constrained paradigms and they do not account for all these processes, in particular multisensory integration. Following the Mobile Brain/Body Imaging approach, we aimed to explore the cortical correlates of landmark-based navigation in actively behaving young adults, solving a Y-maze task in immersive virtual reality. EEG analysis identified a set of brain areas matching state-of-the-art brain imaging literature of landmark-based navigation. Spatial behavior in mobile conditions additionally involved sensorimotor areas related to motor execution and proprioception usually overlooked in static fMRI paradigms. Expectedly, we located a cortical source in or near the posterior cingulate, in line with the engagement of the retrosplenial complex in spatial reorientation. Consistent with its role in visuo-spatial processing and coding, we observed an alpha-power desynchronization while participants gathered visual information. We also hypothesized behavior-dependent modulations of the cortical signal during navigation. Despite finding few differences between the encoding and retrieval phases of the task, we identified transient time-frequency patterns attributed, for instance, to attentional demand, as reflected in the alpha/gamma range, or memory workload in the delta/theta range. We confirmed that combining mobile high-density EEG and biometric measures can help unravel the brain structures and the neural modulations subtending ecological landmark-based navigation

Unsupervised detection of microsaccades in a high-noise regime

International audienceMicromovements of the eye during visual fixations provide clues about how our visual system acquires information. The analysis of fixational eye movements can thus serve as a noninvasive means to detect age-related or pathological changes in visual processing, which can in turn reflect associated cognitive or neurological disorders. However, the utility of such diagnostic approaches relies on the quality and usability of detection methods applied for the eye movement analysis. Here, we propose a novel method for (micro)saccade detection that is resistant to high-frequency recording noise, a frequent problem in video-based eye tracking in either aged subjects or subjects suffering from a vision-related pathology. The method is fast, it does not require manual noise removal, and it can work with position, velocity, or acceleration features, or a combination thereof. The detection accuracy of the proposed method is assessed on a new dataset of manually labeled recordings acquired from 14 subjects of advanced age (69-81 years old), performing an ocular fixation task. It is demonstrated that the detection accuracy of the new method compares favorably to that of two frequently used reference methods and that it is comparable to the best of the two algorithms when tested on an existing low-noise eye-tracking dataset

Differential Brain Activity in Regions Linked to Visuospatial Processing During Landmark-Based Navigation in Young and Healthy Older Adults

International audienceOlder adults have difficulties in navigating unfamiliar environments and updating their wayfinding behavior when faced with blocked routes. This decline in navigational capabilities has traditionally been ascribed to memory impairments and dysexecutive function, whereas the impact of visual aging has often been overlooked. The ability to perceive visuospatial information such as salient landmarks is essential to navigating efficiently. To date, the functional and neurobiological factors underpinning landmark processing in aging remain insufficiently characterized. To address this issue, functional magnetic resonance imaging (fMRI) was used to investigate the brain activity associated with landmark-based navigation in young and healthy older participants. The performances of 25 young adults (μ = 25.4 years, σ = 2.7; seven females) and 17 older adults (μ = 73.0 years, σ = 3.9; 10 females) were assessed in a virtual-navigation task in which they had to orient using salient landmarks. The underlying whole-brain patterns of activity as well as the functional roles of specific cerebral regions involved in landmark processing, namely the parahippocampal place area (PPA), the occipital place area (OPA), and the retrosplenial cortex (RSC), were analyzed. Older adults' navigational abilities were overall diminished compared to young adults. Also, the two age groups relied on distinct navigational strategies to solve the task. Better performances during landmark-based navigation were associated with increased neural activity in an extended neural network comprising several cortical and cerebellar regions. Direct comparisons between age groups revealed that young participants had greater anterior temporal activity. Also, only young adults showed significant activity in occipital areas corresponding to the cortical projection of the central visual field during landmark-based navigation. The region-of-interest analysis revealed an increased OPA activation in older adult participants during the landmark condition. There were no significant between-group differences in PPA and RSC activations. These preliminary results hint at the possibility that aging diminishes fine-grained information processing in occipital and temporal regions, thus hindering the capacity to use landmarks adequately for navigation. Keeping sight of its exploratory nature, this work helps towards a better comprehension of the neural dynamics subtending landmark-based navigation and it provides new insights on the impact of age-related visuospatial processing differences on navigation capabilities

Age-related preference for geometric spatial cues during real-world navigation

International audienceAgeing effects on spatial navigation are characterized mainly in terms of impaired allocentric strategies. However, an alternative hypothesis is that navigation difficulties in aged people are associated with deficits in processing and encoding spatial cues. We tested this hypothesis by studying how geometry and landmark cues control navigation in young and older adults in a real, ecological environment. Recordings of body and gaze dynamics revealed a preference for geometry-based navigation in older adults, and for landmark-based navigation in younger ones. While cue processing was associated with specific fixation patterns, advanced age manifested itself in a longer reorientation time, reflecting an unbalanced exploration-exploitation trade-off in scanning policies. Moreover, a battery of tests revealed a specific cognitive deficit in older adults with geometric preference. These results suggest that allocentric strategy deficits in ageing can result from difficulties related to landmark coding, and predict recovery of allocentric strategies in geometrically polarized environments

Modulation of spatial cue processing across the lifespan: a geometric polarization of space restores allocentric navigation strategies in children and older adults

The impact of development and healthy aging on spatial cognition has been traditionally attributed to a difficulty in using allocentric strategies and a preference for egocentric ones. An alternative possibility, suggested by our previous works, is that this preference is actually conditioned by the spatial cues (e.g. geometric of landmark cues) present in the environment rather than a strategic choice per se. We tested this prediction by having 79 subjects (children, young and older adults) navigating a Y-maze composed either of landmarks or geometric cues, with an immersive head-mounted display that allows us to record both head and eye movements. Our results show that when the performance is based on landmarks solely, children and older adults exhibit a deficit in using allocentric strategies when compared to young adults. Hence, an inverted U-profile of allocentric strategies was observed across the lifespan. This was not due to a default of attention to the landmarks, as evidenced by analysis of gaze dynamics. When geometric were provided, however, older adults and children used allocentric strategies in the same proportion as young adults. They were, in addition, as efficient and quick to implement the strategy. We thus propose a reinterpretation of the previous data in the literature, whereby reference to geometric cues is the default mode for spatial representations, which is immune to age, whereas spatial representations fail to be anchored on landmarks early in development and later in aging. This new interpretation has the potential to reunify several data from the literature, ranging from spatial cues processing to strategy preference, and including other spatial skills like path integration and route learning

Selective neural coding of object, feature, and geometry spatial cues in humans

International audienceOrienting in space requires the processing of visual spatial cues. The dominant hypothesis about the brain structures mediating the coding of spatial cues stipulates the existence of a hippocampal-dependent system for the representation of geometry and a striatal-dependent system for the representation of landmarks. However, this dual-system hypothesis is based on paradigms that presented spatial cues conveying either conflicting or ambiguous spatial information and that used the term landmark to refer to both discrete three-dimensional objects and wall features. Here, we test the hypothesis of complex activation patterns in the hippocampus and the striatum during visual coding. We also postulate that object-based and feature-based navigation are not equivalent instances of landmark-based navigation. We examined how the neural networks associated with geometry-, object-, and feature-based spatial navigation compared with a control condition in a two-choice behavioral paradigm using fMRI. We showed that the hippocampus was involved in all three types of cue-based navigation, whereas the striatum was more strongly recruited in the presence of geometric cues than object or feature cues. We also found that unique, specific neural signatures were associated with each spatial cue. Object-based navigation elicited a widespread pattern of activity in temporal and occipital regions relative to feature-based navigation. These findings extend the current view of a dual, juxtaposed hippocampal–striatal system for visual-spatial coding in humans. They also provide novel insights into the neural networks mediating object versus feature spatial coding, suggesting a need to distinguish these two types of landmarks in the context of human navigation

Landmark-based spatial navigation across the human lifespan

International audienceHuman spatial cognition has been mainly characterized in terms of egocentric (body-centered) and allocentric (world-centered) wayfinding bhavior. It was hypothesized that allocentric spatial coding, as a special high-level cognitive ability, develops later and deteriorates earlier than the egocentric one throughout lifetime. We challenged this hypothesis by testing the use of landmarks versus geometric cues in a cohort of 96 deeply phenotyped participants, who physically navigated an equiangular Y maze, surrounded by landmarks or an anisotropic one. The results show that an apparent allocentric deficit in children and aged navigators is caused specifically by difficulties in using landmarks for navigation while introducing a geometric polarization of space made these participants as efficient allocentric navigators as young adults. This finding suggests that allocentric behavior relies on two dissociable sensory processing systems that are differentially affected by human aging. Whereas landmark processing follows an inverted-U dependence on age, spatial geometry processing is conserved, highlighting its potential in improving navigation performance across the lifespan

Landmark-based spatial navigation across the human lifespan

Human spatial cognition has been mainly characterized in terms of egocentric (body-centered) and allocentric (world-centered) wayfinding behavior. It was hypothesized that allocentric spatial coding, as a special high-level cognitive ability, develops later and deteriorates earlier than the egocentric one throughout lifetime. We challenged this hypothesis by testing the use of landmarks versus geometric cues in a cohort of 96 deeply phenotyped participants, who physically navigated an equiangular Y maze, surrounded by landmarks or an anisotropic one. The results show that an apparent allocentric deficit in children and aged navigators is caused specifically by difficulties in using landmarks for navigation while introducing a geometric polarization of space made these participants as efficient allocentric navigators as young adults. This finding suggests that allocentric behavior relies on two dissociable sensory processing systems that are differentially affected by human aging. Whereas landmark processing follows an inverted-U dependence on age, spatial geometry processing is conserved, highlighting its potential in improving navigation performance across the lifespan