Landmark-based spatial navigation across the human lifespan

  1. Marcia Bécu  Is a corresponding author
  2. Denis Sheynikhovich
  3. Stephen Ramanoël
  4. Guillaume Tatur
  5. Anthony Ozier-Lafontaine
  6. Colas N Authié
  7. José-Alain Sahel
  8. Angelo Arleo  Is a corresponding author
  1. Norwegian University of Science and Technology, Norway
  2. Sorbonne Université, France
  3. Streetlab, Institut de la Vision, France
  4. 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.

The following data sets were generated

Article and author information

Author details

  1. Marcia Bécu

    Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology, Trondheim, Norway
    For correspondence
    marcia.becu@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4564-1023
  2. Denis Sheynikhovich

    INSERM, CNRS, Institut de la Vision, Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7737-8907
  3. Stephen Ramanoël

    INSERM, CNRS, Institut de la Vision, Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4735-1097
  4. Guillaume Tatur

    INSERM, CNRS, Institut de la Vision, Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Anthony Ozier-Lafontaine

    INSERM, CNRS, Institut de la Vision, Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Colas N Authié

    Institut de la Vision, Streetlab, Institut de la Vision, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. José-Alain Sahel

    Department of Ophthalmology, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Angelo Arleo

    INSERM, CNRS, Institut de la Vision, Sorbonne Université, Paris, France
    For correspondence
    angelo.arleo@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.

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.

Reviewing Editor

  1. Arne Ekstrom, University of Arizona

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).

Version history

  1. Preprint posted: February 13, 2020 (view preprint)
  2. Received: June 22, 2022
  3. Accepted: March 11, 2023
  4. Accepted Manuscript published: March 13, 2023 (version 1)
  5. Version of Record published: March 23, 2023 (version 2)
  6. Version of Record updated: May 11, 2023 (version 3)

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.

Metrics

  • 1,789
    Page views
  • 238
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

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)

  1. Marcia Bécu
  2. Denis Sheynikhovich
  3. Stephen Ramanoël
  4. Guillaume Tatur
  5. Anthony Ozier-Lafontaine
  6. Colas N Authié
  7. José-Alain Sahel
  8. Angelo Arleo
(2023)
Landmark-based spatial navigation across the human lifespan
eLife 12:e81318.
https://doi.org/10.7554/eLife.81318

Share this article

https://doi.org/10.7554/eLife.81318

Further reading

    1. Neuroscience
    Harry Clark, Matthew F Nolan
    Research Article

    Grid firing fields have been proposed as a neural substrate for spatial localisation in general or for path integration in particular. To distinguish these possibilities, we investigate firing of grid and non-grid cells in the mouse medial entorhinal cortex during a location memory task. We find that grid firing can either be anchored to the task environment, or can encode distance travelled independently of the task reference frame. Anchoring varied between and within sessions, while spatial firing of non-grid cells was either coherent with the grid population, or was stably anchored to the task environment. We took advantage of the variability in task-anchoring to evaluate whether and when encoding of location by grid cells might contribute to behaviour. We find that when reward location is indicated by a visual cue, performance is similar regardless of whether grid cells are task-anchored or not, arguing against a role for grid representations when location cues are available. By contrast, in the absence of the visual cue, performance was enhanced when grid cells were anchored to the task environment. Our results suggest that anchoring of grid cells to task reference frames selectively enhances performance when path integration is required.

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.