Landmark-based spatial navigation across the human lifespan
- Norwegian University of Science and Technology, Norway
- Sorbonne Université, France
- Streetlab, Institut de la Vision, France
- University of Pittsburgh, United States
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 life span.
Data availability
All data and code used in the analyses are available as an Open Science Framework deposit, accessible at https://osf.io/zhrk4.
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Evolution of landmark-based spatial navigation across the human lifespanOpen Science Framework.
Article and author information
Author details
Denis Sheynikhovich
Funding
ANR (ANR-14-CHIN-0001 ANR-14-CHIN-0002)
- Angelo Arleo
ANR (Labex LifeSenses ANR-10-LABX-65)
- José-Alain Sahel
- Angelo Arleo
ANR (IHU FOReSIGHT grant ANR-18-IAHU-01)
- José-Alain Sahel
- Angelo Arleo
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: All participants were voluntary and they (or their parents in the case of children) gave an informed consent for inclusion in the study. All screening and experimental procedures were in accordance with the tenets of the Declaration of Helsinki, and they were approved by the Ethical Committee CPP Ile de France V (ID_RCB 2015-A01094-45, No. CPP: 16122 MSB).
Copyright
© 2023, Bécu et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Landmark-based spatial navigation across the human lifespan
eLife 12:e81318.
https://doi.org/10.7554/eLife.81318
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
