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A novel real-space navigation paradigm reveals age- and gender-dependent changes of navigational strategies and hippocampal activation

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Abstract

Objective

To establish a novel multimodal real-space navigation paradigm and define age- and gender-related normative values for navigation performance and visual exploration strategies in space.

Methods

A group of 30 healthy subjects (mean age 45.9 ± 16.5 years, 16 men) performed a real-space navigation paradigm, requiring allo- and egocentric spatial orientation abilities. Visual exploration behaviour and navigation strategy were documented by a gaze-controlled, head-fixed camera. Allo- and egocentric spatial orientation performance were compared in younger and older subjects (age threshold 50 years) as well as men and women. Navigation-induced changes of regional cerebral glucose metabolism (rCGM) were measured by [18F]-fluorodeoxyglucose-positron emission tomography in a subgroup of 15 subjects (8 men) and compared across age and gender.

Results

The majority of healthy subjects (73.3%) completed the navigation task without errors. There was no gender difference in navigation performance. Normalized total error rates increased slightly, but significantly with age (r = 0.36, p = 0.05). Analysis of navigation path indicated a significantly reduced use of short cuts in older age (r = 0.44, p = 0.015). Visual exploration analysis revealed that older subjects made significantly more total saccades (r = 0.49, p = 0.006) and search saccades (r = 0.54, p = 0.002) during navigation. All visual exploration parameters were similar in men and women. Navigation-induced rCGM decreased with age in the hippocampus and precuneus and increased in the frontal cortex, basal ganglia and cerebellum. Women showed an increase of rCGM in the left hippocampus and right middle temporal gyrus, men in the superior vermis.

Conclusion

Real-space navigation testing was a feasible and sensitive method to depict age-related changes in navigation performance and strategy. Normalized error rates, total mean durations per item and total number of saccades were the most sensitive and practical parameters to indicate deterioration of allocentric navigation strategies and right hippocampal function in age irrespective of gender.

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Acknowledgements

The authors thank Judy Benson for copy-editing the manuscript and Kathrin Richter for excellent technical support.

Funding

The study was performed as a project of the German Center for Vertigo and Balance Disorders (DSGZ) (Grant number 01 EO 0901) with support of the German Federal Ministry of Education and Health (BMBF) and the Hertie Foundation (to TB).

Author information

Authors and Affiliations

  1. German Center for Vertigo and Balance Disorders, DSGZ, Ludwig-Maximilians-University, Marchioninistrasse 15, 81377, Munich, Germany

    Stephanie Irving, Florian Schöberl, Cauchy Pradhan, Peter Bartenstein, Marianne Dieterich, Thomas Brandt & Andreas Zwergal

  2. Department of Neurology, Ludwig-Maximilians-University, Munich, Germany

    Florian Schöberl, Marianne Dieterich & Andreas Zwergal

  3. Department of Nuclear Medicine, Ludwig-Maximilians-University, Munich, Germany

    Matthias Brendel & Peter Bartenstein

  4. Munich Cluster of Systems Neurology, SyNergy, Munich, Germany

    Peter Bartenstein & Marianne Dieterich

  5. Clinical Neurosciences, Ludwig-Maximilians-University, Munich, Germany

    Thomas Brandt

Authors
  1. Stephanie Irving
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  2. Florian Schöberl
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  3. Cauchy Pradhan
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  4. Matthias Brendel
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  6. Marianne Dieterich
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  7. Thomas Brandt
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  8. Andreas Zwergal
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Corresponding author

Correspondence to Andreas Zwergal.

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Conflict of interest

The authors report no conflict of interest.

Ethical approval

All experiments were done in accordance with ethical standards of the Declaration of Helsinki.

Additional information

This manuscript is part of a supplement sponsored by the German Federal Ministry of Education and Research within the funding initiative for integrated research and treatment centers.

Electronic supplementary material

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415_2018_8987_MOESM1_ESM.tif

Supplementary Fig. 1: PET acquisition protocol. [18F]-FDG was injected at the beginning of the 10 min navigation period. This paradigm was chosen because the cerebral glucose utilisation is known to be weighted to the first 10 min following [18F]-FDG injection and is integrative due to intracellular trapping of the tracer. Given the [18F]-FDG half-life time of 110 min, image acquisition (30 min after tracer administration) allows to depict the glucose consumption pattern acquired during navigation (TIF 87 KB)

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Irving, S., Schöberl, F., Pradhan, C. et al. A novel real-space navigation paradigm reveals age- and gender-dependent changes of navigational strategies and hippocampal activation. J Neurol 265 (Suppl 1), 113–126 (2018). https://doi.org/10.1007/s00415-018-8987-4

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  • DOI: https://doi.org/10.1007/s00415-018-8987-4

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