Research reportAge effects on wayfinding and route learning skills
Introduction
Advancing age is associated with decrements in spatial navigation skills. These age-associated limitations in navigation could potentially lead to restrictions in daily activities, resistance to new environments or difficulty in transitioning to new environments, such as nursing homes [e.g., 1]. Thus, it is important to gain a greater understanding of the nature of age-related difficulties in navigation as well as better delineate the neural substrates of these deficits.
Successful navigation involves identification and knowledge of salient environmental features, critical route events, course-maintaining actions and the temporal and spatial sequence of such events and actions. Navigation may proceed based upon the development of two somewhat distinct representations. Response learning, or learning a specific route through the environment, entails the development of an action-based representation such that the sequence of body movements associated with environmental features is represented. In contrast, in place learning a more flexible internal representation or “cognitive map” of the spatial relationships amongst landmarks in the environment is formed [2]. While a distributed network of cortical and subcortical regions contributes to successful navigation [3], [4], [5], [6], these representations have relatively distinct neural underpinnings. Response learning appears to be more dependent on the striatal system whereas place learning is primarily subserved by hippocampal circuits [2], [7], [8], [9], [10], [11], [12]. Prefrontal regions may contribute to both types of learning [13], [14], [15], [16].
Previous literature provides some indications of the nature of age-related deficits with effects observed for both types of learning. Studies involving the learning of routes indicate that older adults perform more poorly than their younger counterparts [17], [18], [19]. Younger adults also outperform older adults on tasks designed to be more reliant on place learning and thus the acquisition and use of a cognitive map [20], [21], [22], [23], [24], [25]. Rather than solely a global age-related deficit, there is also evidence that age effects are apparent on specific component processes of navigation including selecting critical rather than only salient environmental features (e.g., landmarks), temporally and spatially organizing the relevant features, landmark recall, scene recognition, landmark location identification and self-orientation [19], [26], [27], [28], [29], [30], [31], [32].
While advancing age is associated with deterioration of the neural substrates of response and place learning, such as frontostriatal and hippocampal circuits [see 33 for a review], there is only limited direct evidence of the contribution of these regions to the behavioral deficits. Structural neuroimaging investigations have linked navigational success to frontostriatal [25] and hippocampal regions [21] in older adults. Both of these investigations used a virtual Morris Water Maze task, which although associated with use of a cognitive map may also incorporate aspects of response learning [23]. Route encoding has been associated with age-related alterations in neural activity in prefrontal, caudate, parahippocampal and parietal regions whereas place learning has been associated with age-related reductions in prefrontal, hippocampal, parahippocampal, retrosplenial, and parietal regions [20], [34], [35], suggesting differential involvement of the caudate and hippocampus in response and place learning, respectively, consistent with the animal literature.
The primary goal of the current study was to characterize age effects on spatial navigation abilities taking into account the multiple components that contribute to successful navigation. Performance on tasks of wayfinding (i.e., place learning) and route learning (i.e., response learning) in a virtual reality environment and the degree to which individuals were acquiring the environmental knowledge that facilitates navigation and learning new environments and routes were examined in young and older adults. In addition, associations between structural brain volumes and navigation performance were examined in older adults with the expectation that the hippocampus would be associated with wayfinding performance and the caudate nucleus would be associated with route learning. The prefrontal cortex was also examined as it has been suggested that executive deficits may at least in part underlie age effects on navigational skills [25], aging is associated with differential declines in the prefrontal cortex [33] and animal studies suggest a potential role for the prefrontal cortex in place and response learning [13], [14], [15], [16]. Thus, we hypothesized that prefrontal cortex volume would be associated with both wayfinding and route learning in the current study.
Section snippets
Participants
Older adults were recruited from a prior unpublished study on older adults in the lab that included an MRI scan to address the question regarding the neural correlates of spatial navigation in older adults. Additional older adults were recruited from an established subject pool in the Psychology Department at Washington University and young adults were undergraduate students at Washington University for the behavioral analyses. All participants were screened using a health questionnaire for
Visuomotor expertise and experience with computers, computer games and virtual reality
Although all participants completed the visuomotor expertise task in the allotted 2 min, there were age differences in the time to completion (F(1, 44) = 6.22, p < .05). There was not an effect of gender on time to complete the visuomotor maze (F < 1). In addition, there were age-related reductions in the amount of experience with computers (F(1, 44) = 16.19, p < .001), computer games (F(1, 44) = 5.67, p < .05) and with virtual reality (F(1, 44) = 22.98, p < .001). There were no significant gender differences in
Discussion
The present investigation examined age differences in spatial navigation and the role of individual differences in neural substrates. We used experimental paradigms to separately examine wayfinding and route learning and additionally assessed specific component processes that contribute to successful performance. Results confirm an age-related deficit in these two strategies for navigating and further provide indications of specific component processes and brain regions that may contribute to
Acknowledgments
This work was supported in part by the McDonnell Center for Higher Brain functions. We thank Paul Speigel and Rachel Bock for virtual reality programming, and Dana Cooper, Jennifer Travis and Tanya Antonini for assistance with data collection.
References (71)
- et al.
Human spatial navigation: cognitive maps, sexual dimorphism, and neural substrates
Curr Opin Neurobiol
(1999) - et al.
Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning
Neurobiol Learn Mem
(1996) - et al.
Multiple parallel memory systems in the brain of the rat
Neurobiol Learn Mem
(2002) - et al.
Place and response learning of rats in a Morris water maze: differential effects of fimbria fornix and medial prefrontal lesions
Neurobiol Learn Mem
(2001) - et al.
Response learning of rats in a Morris water maze: involvement of the medial prefrontal cortex
Behav Brain Res
(1997) - et al.
Place learning and object recognition by rats subjected to transection of the fimbria-fornix and/or ablation of the prefrontal cortex
Brain Res Bull
(2004) - et al.
Egocentric spatial orientation in a water maze by rats subjected to transaction of the fimbria-fornix and/or ablation of the prefrontal cortex
Brain Res Bull
(2005) - et al.
Age differences in spatial memory in a virtual environment navigation task
Neurobiol Aging
(2001) - et al.
Age differences in the neural systems supporting human allocentric spatial navigation
Neurobiol Aging
(2006) - et al.
Virtual navigation in humans: the impact of age, sex and hormones on place learning
Horm Behav
(2005)
Age differences in the formation and use of cognitive maps
Behav Brain Res
Differential aging of the brain: patterns, cognitive correlates and modifiers
Neurosci Biobehav Rev
Age differences in neural correlates of route encoding and route recognition
NeuroImage
The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans
Neuron
A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: Reliability and validation against manual measurement of total intracranial volume
NeuroImage
An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest
NeuroImage
Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain
Neuron
Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients
Neuropsychologia
Dissociations between memory for temporal order and recognition memory in aging
Neuropsychologia
Competition among multiple memory systems: converging evidence from animal and human bain studies
Neuropsychologia
Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory
Behav Brain Res
Navigation and mobility of older drivers
J Gerontol B: Psychol Sci Soc Sci
The hippocampus as a cognitive map
Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps
Eur J Neurosci
Knowing where and getting there: a human navigation network
Science
Navigation ability dependent neural activation in the human brain: an fMRI study
Neurosci Res
Place navigation impaired in rats with hippocampal lesions
Nature
Learning and memory functions of the basal ganglia
Annu Rev Neurosci
Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice
J Neurosci
Navigational skills correlate with hippocampal fractional anisotropy in humans
Hippocampus
Age-related decline in route learning ability
Dev Neuropsychol
Age-related differences in an ecologically based study of route learning
Psychol Aging
The aging hippocampus: cognitive, biochemical and structural findings
Cereb Cortex
Effects of age on virtual environment place navigation and allocentric cognitive mapping
Behav Neurosci
Extrahippocampal contributions to age differences in spatial navigation
Cereb Cortex
Cited by (222)
How pathways' configuration impact wayfinding in young and older adults
2023, Journal of Environmental PsychologyAssociations of environmental and lifestyle factors with spatial navigation in younger and older adults
2023, Journal of the International Neuropsychological Society