Aging and Spatial Navigation: When landmarks are not enough
Our ability to navigate from place to place, which is essential for our wellbeing and independence, declines as we get older (Head and Isom, 2010). Even in healthy individuals, this decline can have a significant impact on quality of life and can foreshadow the onset of Alzheimer’s disease years before the appearance of clinical symptoms (Levine et al., 2020). Likewise, spatial disorientation is among the earliest behavioral symptoms of Alzheimer’s disease and can lead to a loss of personal autonomy and heightened risk of mental distress, physical injury, or even death. Impaired spatial navigation has therefore gained traction as a promising diagnostic marker of age-related cognitive dysfunction and as a potential target for disease-modifying interventions (Coughlan et al., 2018; Segen et al., 2022).
Successful spatial navigation is typically conceived as relying on two complementary strategies. Allocentric or world-centered navigation requires an individual to learn the relationship between external spatial cues such as landmarks in order to form an internal topographic map of their environment. Egocentric or person-centered navigation strategies place a greater reliance on traversing familiar and well-learned routes, and are generally regarded as less flexible and efficient than allocentric navigation. The dominant theory in the field of aging is that allocentric-based navigation is impaired in older age, resulting in a preference for egocentric-based navigation strategies (Moffat et al., 2006; Moffat and Resnick, 2002).
Now, in eLife, Angelo Arleo and colleagues at Sorbonne Université – including Marcia Bécu as first author – report that the ability to engage in putative allocentric-based navigation may depend largely on the types of spatial cues present in the environment (Bécu et al., 2023). Critically, children and older individuals were just as likely as young adults to use allocentric strategies when geometric spatial cues (as opposed to landmarks) were available to guide navigation. The work adds to mounting evidence that allocentric navigation may show some degree of preservation with age.
Bécu et al. examined the types of strategies children, young adults, and healthy older adults used when navigating a Y-maze using a virtual reality headset that allowed them to move freely (Figure 1). The Y-maze has a long history of being used to examine spatial strategies in rodents. However, the task typically relies exclusively on visual landmarks to guide navigation. Here, participants were randomly assigned to navigate in one of two Y-Maze conditions. In the classic landmark condition, participants navigated an equiangular maze in which three distal landmarks surrounding the maze could be used to infer their location. In the geometry condition, the angles between respective maze arms were not equal, allowing participants to determine their position in the maze in the absence of landmarks. Children and older adults were more likely than young adults to prefer an egocentric strategy when navigating the landmark condition, replicating numerous prior studies. However, this age-related preference for egocentric navigation was eliminated in the geometry condition, with most participants in all three age groups preferring an allocentric search strategy.
Next, Bécu et al. analyzed eye-tracking data to examine whether age differences in visual sampling of the environment might account for the age-related preference for egocentric navigation observed in the landmark condition. Young adults and older adults did not differ in the proportion of time spent visually fixating on the landmarks when learning the maze in the landmark condition. Likewise, there was no difference between those who used egocentric navigation and those who used allocentric navigation, independent of age. These results suggest that the age-related preference for egocentric navigation observed during the landmark condition was not caused by a failure to attend to the landmarks during learning. Instead, allocentric navigators, regardless of age, spent a greater proportion of time fixating on the landmarks as they planned a locomotor response during probe trials.
Taken together, the findings reported by Bécu et al. suggest that rather than a selective deficit in allocentric-based navigation, spatial challenges in older individuals may be the result of difficulties processing landmark cues in order to orient in space. These results complement recently published findings from a study of over 37,000 individuals collected using the mobile app Sea Hero Quest, which showed that landmark-based navigation strategies decline linearly with age (West et al., 2023). Critically, this work challenges decades of prior work to suggest that wayfinding deficits in older age are unlikely to be accounted for by a simple dichotomy between allocentric and egocentric navigation.
The finding that older adults seemingly maintain the ability to orient in space as well as their younger counterparts when geometric spatial cues are available offers exciting opportunities for future research. Studies examining the perceptual, cognitive and/or neural basis of geometric cue processing could make significant contributions to the development of more comprehensive models of aging and navigation. It will also be interesting to explore whether longitudinal declines in landmark-based processing are sensitive to pathologic changes associated with Alzheimer’s disease and related dementias. This knowledge could be important when designing accessible environments for vulnerable aging populations.
Spatial navigation deficits - Overlooked cognitive marker for preclinical Alzheimer disease?Nature Reviews Neurology 14:496–506.https://doi.org/10.1038/s41582-018-0031-x
Age effects on wayfinding and route learning skillsBehavioural Brain Research 209:49–58.https://doi.org/10.1016/j.bbr.2010.01.012
Spatial navigation ability predicts progression of dementia symptomatologyAlzheimer’s & Dementia 16:491–500.https://doi.org/10.1002/alz.12031
Effects of age on virtual environment place navigation and allocentric cognitive mappingBehavioral Neuroscience 116:851–859.https://doi.org/10.1037//0735-7044.116.5.851
Path integration in normal aging and Alzheimer’s diseaseTrends in Cognitive Sciences 26:142–158.https://doi.org/10.1016/j.tics.2021.11.001
Landmark-dependent navigation strategy declines across the human life-span: evidence from over 37,000 participantsJournal of Cognitive Neuroscience 35:452–467.https://doi.org/10.1162/jocn_a_01956
Article and author information
- Version of Record published: April 21, 2023 (version 1)
© 2023, Hill
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
- Page views
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Early-life experiences may promote stereotyped behavioral alterations that are dynamic across development time, but also behavioral responses that are variable among individuals, even when initially exposed to the same stimulus. Here, by utilizing longitudinal monitoring of Caenorhabditis elegans individuals throughout development we show that behavioral effects of early-life starvation are exposed during early and late developmental stages and buffered during intermediate stages of development. We further found that both dopamine and serotonin shape the discontinuous behavioral responses by opposite and temporally segregated functions across development time. While dopamine buffers behavioral responses during intermediate developmental stages, serotonin promotes behavioral sensitivity to stress during early and late stages. Interestingly, unsupervised analysis of individual biases across development uncovered multiple individuality dimensions that coexist within stressed and unstressed populations and further identified experience-dependent effects on variation within specific individuality dimensions. These results provide insight into the complex temporal regulation of behavioral plasticity across developmental timescales, structuring shared and unique individual responses to early-life experiences.
- Computational and Systems Biology
Inhibition is crucial for brain function, regulating network activity by balancing excitation and implementing gain control. Recent evidence suggests that beyond simply inhibiting excitatory activity, inhibitory neurons can also shape circuit function through disinhibition. While disinhibitory circuit motifs have been implicated in cognitive processes including learning, attentional selection, and input gating, the role of disinhibition is largely unexplored in the study of decision-making. Here, we show that disinhibition provides a simple circuit motif for fast, dynamic control of network state and function. This dynamic control allows a disinhibition-based decision model to reproduce both value normalization and winner-take-all dynamics, the two central features of neurobiological decision-making captured in separate existing models with distinct circuit motifs. In addition, the disinhibition model exhibits flexible attractor dynamics consistent with different forms of persistent activity seen in working memory. Fitting the model to empirical data shows it captures well both the neurophysiological dynamics of value coding and psychometric choice behavior. Furthermore, the biological basis of disinhibition provides a simple mechanism for flexible top-down control of the network states, enabling the circuit to capture diverse task-dependent neural dynamics. These results suggest a biologically plausible unifying mechanism for decision-making and emphasize the importance of local disinhibition in neural processing.