Abstract

Older adults have difficulties in navigating unfamiliar environments and updating their wayfinding behavior when faced with blocked routes. This decline in navigational capabilities has traditionally been ascribed to memory impairments and dysexecutive function, whereas the impact of visual aging has often been overlooked. The ability to perceive visuospatial information such as salient landmarks is essential to navigating efficiently. To date, the functional and neurobiological factors underpinning landmark processing in aging remain insufficiently characterized. To address this issue, functional magnetic resonance imaging (fMRI) was used to investigate the brain activity associated with landmark-based navigation in young and healthy older participants. The performances of 25 young adults (μ = 25.4 years, σ = 2.7; seven females) and 17 older adults (μ = 73.0 years, σ = 3.9; 10 females) were assessed in a virtual-navigation task in which they had to orient using salient landmarks. The underlying whole-brain patterns of activity as well as the functional roles of specific cerebral regions involved in landmark processing, namely the parahippocampal place area (PPA), the occipital place area (OPA), and the retrosplenial cortex (RSC), were analyzed. Older adults’ navigational abilities were overall diminished compared to young adults. Also, the two age groups relied on distinct navigational strategies to solve the task. Better performances during landmark-based navigation were associated with increased neural activity in an extended neural network comprising several cortical and cerebellar regions. Direct comparisons between age groups revealed that young participants had greater anterior temporal activity. Also, only young adults showed significant activity in occipital areas corresponding to the cortical projection of the central visual field during landmark-based navigation. The region-of-interest analysis revealed an increased OPA activation in older adult participants during the landmark condition. There were no significant between-group differences in PPA and RSC activations. These preliminary results hint at the possibility that aging diminishes fine-grained information processing in occipital and temporal regions, thus hindering the capacity to use landmarks adequately for navigation. Keeping sight of its exploratory nature, this work helps towards a better comprehension of the neural dynamics subtending landmark-based navigation and it provides new insights on the impact of age-related visuospatial processing differences on navigation capabilities.

Highlights

  • The 21st century is characterized by an unprecedented increase in the number of older adults within the worldwide population

  • Older subjects were significantly slower to reach the goal than younger subjects in the landmark condition (19.85 s ± 1.67 vs. 11.97 s ± 0.13; U(40) = 418, p = 10−6, r = 0.81, 95% confidence interval (CI) of the difference [3.40, 8.36]; Figure 2Ai) and in the control condition (20.83 s ± 0.95 vs. 14.07 s ± 0.27; U(40) = 418, p = 10−6, r = 0.81, 95% CI of the difference [4.70, 8.15]; Figure 2Aii)

  • Sex and total intracranial volume were included as covariates in the functional magnetic resonance imaging (fMRI) multiple regression analyses

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Summary

Introduction

The 21st century is characterized by an unprecedented increase in the number of older adults within the worldwide population. To identify appropriate biomarkers of age-related sensori-cognitive alterations, it is critical to gain a better understanding of brain changes in healthy aging. In this context, spatial navigation as a complex behavior encompassing perceptual and cognitive processes provides an ideal framework for the study of normal and pathological aging (Gazova et al, 2012; Lithfous et al, 2013; Allison et al, 2016; Laczó et al, 2017, 2018; Coughlan et al, 2018). Cross-sectional studies in VR have shed light on an age-related shift in the use of navigation strategies: older adults favor response over place-based strategies (Bohbot et al, 2012; Rodgers et al, 2012). Successful navigation requires the perception and the integration of relevant visual-spatial cues such as buildings or monuments, and the binding of these salient elements to directional information (Ekstrom, 2015; Epstein et al, 2017; Julian et al, 2018)

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