Landmark-based spatial navigation across the human lifespan
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Evaluation Summary:
This is an important study that investigates whether older adults have selective impairments in allocentric navigation (using distal cues to navigate). Using a combination of ecologically inspired real-world navigation, virtual reality, eye tracking, and body-tracking, the study reports, for the first time, that older adults show no difference from younger adults when using geometry to navigate a Y maze. Instead, their deficits appear to relate to perceptual difficulties with processing individual landmarks. This large sample study therefore provides somewhat compelling evidence of age-related difficulties in processing landmarks visually rather than a selective deficit in allocentric navigation.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
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.
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Evaluation Summary:
This is an important study that investigates whether older adults have selective impairments in allocentric navigation (using distal cues to navigate). Using a combination of ecologically inspired real-world navigation, virtual reality, eye tracking, and body-tracking, the study reports, for the first time, that older adults show no difference from younger adults when using geometry to navigate a Y maze. Instead, their deficits appear to relate to perceptual difficulties with processing individual landmarks. This large sample study therefore provides somewhat compelling evidence of age-related difficulties in processing landmarks visually rather than a selective deficit in allocentric navigation.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive …
Evaluation Summary:
This is an important study that investigates whether older adults have selective impairments in allocentric navigation (using distal cues to navigate). Using a combination of ecologically inspired real-world navigation, virtual reality, eye tracking, and body-tracking, the study reports, for the first time, that older adults show no difference from younger adults when using geometry to navigate a Y maze. Instead, their deficits appear to relate to perceptual difficulties with processing individual landmarks. This large sample study therefore provides somewhat compelling evidence of age-related difficulties in processing landmarks visually rather than a selective deficit in allocentric navigation.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
This study attempts to understand the source of problems in allocentric navigation in older adults and children compared to young adults. Using a simple and elegant Y-maze design with extensive behavioral analyses, the authors convincingly show that older adults and children are impaired with respect to the ability to use landmark cues, but not geometric cues, in order to orient in the environment. Their testing further shows that this results from a problem of remembering spatial relations between landmarks and using those to navigate, and not an issue of encoding the landmarks themselves or attending to them. The findings are important in two respects: 1) understanding the navigational problems of older adults, 2) understanding the cognitive systems underlying allocentric navigation. With regard to the …
Reviewer #1 (Public Review):
This study attempts to understand the source of problems in allocentric navigation in older adults and children compared to young adults. Using a simple and elegant Y-maze design with extensive behavioral analyses, the authors convincingly show that older adults and children are impaired with respect to the ability to use landmark cues, but not geometric cues, in order to orient in the environment. Their testing further shows that this results from a problem of remembering spatial relations between landmarks and using those to navigate, and not an issue of encoding the landmarks themselves or attending to them. The findings are important in two respects: 1) understanding the navigational problems of older adults, 2) understanding the cognitive systems underlying allocentric navigation. With regard to the first point, the authors' results from the map drawing task demonstrate that the problem is specifically with remembering the relative configuration of the landmarks with respect to one another and to the start and goal location. With regard to the second point, the paper is exciting in that it demonstrates a dissociation between two systems of allocentric navigation - landmark-based and geometry-based. As the authors point out, most papers refer to "allocentric navigation" as a process where subjects use either the geometry or landmarks interchangeably as reference points in their mental map, but these findings suggest that those systems might be dissociable. Overall, I think that the study is well-designed, the analyses are adequate, and the research questions are addressed appropriately. The authors took care to exclude other sources of difference between groups by having both physical and virtual reality mazes, using a walking VR paradigm to eliminate computer use proficiency differences, and testing visual attention and gaze as well as an array of other variables.
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Reviewer #2 (Public Review):
Becu and colleagues describe results from a cross-sectional study examining age-related differences in navigation performance in a cohort of children, young adults, and healthy older adults. Participants navigated a virtual Y-maze in one of two conditions. In the equiangular landmark condition, three distal cues appeared above the maze which could be used to inform successful navigation. In the geometric polarization condition, the relative angles of the respective maze arms could be used to inform successful navigation; no distal cues were present in this condition. In each condition, subjects learned to locate the rewarded arm and, after reaching criterion, advanced to the probe phase of the experiment. Compared to young adults, children and older adults were less likely to adopt an 'allocentric' strategy …
Reviewer #2 (Public Review):
Becu and colleagues describe results from a cross-sectional study examining age-related differences in navigation performance in a cohort of children, young adults, and healthy older adults. Participants navigated a virtual Y-maze in one of two conditions. In the equiangular landmark condition, three distal cues appeared above the maze which could be used to inform successful navigation. In the geometric polarization condition, the relative angles of the respective maze arms could be used to inform successful navigation; no distal cues were present in this condition. In each condition, subjects learned to locate the rewarded arm and, after reaching criterion, advanced to the probe phase of the experiment. Compared to young adults, children and older adults were less likely to adopt an 'allocentric' strategy in the equiangular landmark condition, consistent with the traditional view of an age-related 'egocentric' bias. Similar age differences were not evident in the geometry condition, where all age groups were equally likely to engage in an allocentric strategy. Examination of oculomotor data indicated that age-related differences in the landmark condition could not be accounted for by a failure to attend to the landmark cues during spatial learning. The authors conclude that prior accounts of a selective age-related deficit in allocentric-based navigation may be confounded by paradigms that solely use distal landmark cues; inclusion of informative geometric cues may mitigate or even eliminate some of these observed age differences.
1. The principal findings showing that young and older adults do not differ in their tendency to adopt allocentric-based navigation strategies in the presence of informative geometric cues is important and potentially high impact. I believe the authors are correct when they emphasize the need to revisit the long-held allocentric vs. egocentric dichotomy in the field of aging and navigation. It is not clear, however, whether the authors performed any analyses necessary to identify a significant age group x condition interaction, which is necessary to determine whether the availability of geometric cues truly moderates the effect of age on navigation. Given the data presented in Figure 2, I suspect this will be the case, but the results of a formal interaction analysis should be reported to back the authors' claims.
2. The use of the term 'evolution' in the title and elsewhere throughout the paper, as well as some of the broader interpretations of the results, is misleading. This cross-section research was performed in a cohort of children (10-11 years), young adults (23-37 years) and healthy older adults (67-81 adults). While it is certainly clear that young adults outperformed both children and older adults (in terms of their ability to engage in 'allocentric' strategies during landmark-based navigation), it is a leap to assume that the pattern of results is driven by the maturation (childhood) and eventual deterioration (older age) of spatial cue processing abilities, which ultimately necessitates a longitudinal design. This certainly does not negate the findings presented in this paper, but some of the language used when describing the results and their interpretation should be qualified by the limitations of a cross-sectional design.
3. The authors rule out the possibility that age-related differences in performance in the landmark and geometry conditions are driven by systematic differences in task complexity, but this analysis is based solely on null differences observed in young adults only (Supplementary Figure 4). This does not rule out the possibility that the two conditions recruit limited capacity resources that are differentially available in young and older adults. For example, the evolution of gaze altitude illustrated Figure 7A and 7B suggests that during the landmark condition, both age groups attempt to track multiple features of the environment (landmarks, ground, maze walls). The lack of sky-based landmarks in the geometry condition, however, permits subjects to simply maintain focus on the maze walls, which in this condition were informative. One interpretation might be that older adults simply had more difficulty tracking, processing, and maintaining such disparate cues when navigating, rather than a selective deficit in using distal landmark cues. This interpretation is of course speculative but is meant to underscore the limitations of using performance in one age group to infer task complexity/difficulty experienced by the other age groups.
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