Mathew A. Harris

Maladaptive Bias for Extrahippocampal Navigation Strategies in Aging Humans

Efficient spatial navigation requires not only accurate spatial knowledge but also the selection of appropriate strategies. Using a novel paradigm that allowed us to distinguish between beacon, associative cue, and place strategies, we investigated the effects of cognitive aging on the selection and adoption of navigation strategies in humans. Participants were required to rejoin a previously learned route encountered from an unfamiliar direction. Successful performance required the use of an allocentric place strategy, which was increasingly observed in young participants over six experimental sessions. In contrast, older participants, who were able to recall the route when approaching intersections from the same direction as during encoding, failed to use the correct place strategy when approaching intersections from novel directions. Instead, they continuously used a beacon strategy and showed no evidence of changing their behavior across the six sessions. Given that this bias was already apparent in the first experimental session, the inability to adopt the correct place strategy is not related to an inability to switch from a firmly established response strategy to an allocentric place strategy. Rather, and in line with previous research, age-related deficits in allocentric processing result in shifts in preferred navigation strategies and an overall bias for response strategies. The specific preference for a beacon strategy is discussed in the context of a possible dissociation between beacon-based and associative-cue-based response learning in the striatum, with the latter being more sensitive to age-related changes.

Ageing effects on path integration and landmark navigation

Navigation abilities show marked decline in both normal ageing and dementia. Path integration may be particularly affected, as it is supported by the hippocampus and entorhinal cortex, both of which show severe degeneration with ageing. Age differences in path integration based on kinaesthetic and vestibular cues have been clearly demonstrated, but very little research has focused on visual path integration, based only on optic flow. Path integration is complemented by landmark navigation, which may also show age differences, but has not been well studied either. Here we present a study using several simple virtual navigation tasks to explore age differences in path integration both with and without landmark information. We report that, within a virtual environment that provided only optic flow information, older participants exhibited deficits in path integration in terms of distance reproduction, rotation reproduction, and triangle completion. We also report age differences in triangle completion within an environment that provided landmark information. In all tasks, we observed a more restricted range of responses in the older participants, which we discuss in terms of a leaky integrator model, as older participants showed greater leak than younger participants. Our findings begin to explain the mechanisms underlying age differences in path integration, and thus contribute to an understanding of the substantial decline in navigation abilities observed in ageing.

Aging specifically impairs switching to an allocentric navigational strategy.

Navigation abilities decline with age, partly due to deficits in numerous component processes. Impaired switching between these various processes (i.e., switching navigational strategies) is also likely to contribute to age-related navigational impairments. We tested young and old participants on a virtual plus maze task (VPM), expecting older participants to exhibit a specific strategy switching deficit, despite unimpaired learning of allocentric (place) and egocentric (response) strategies following reversals within each strategy. Our initial results suggested that older participants performed worse during place trial blocks but not response trial blocks, as well as in trial blocks following a strategy switch but not those following a reversal. However, we then separated trial blocks by both strategy and change type, revealing that these initial results were due to a more specific deficit in switching to the place strategy. Place reversals and switches to response, as well as response reversals, were unaffected. We argue that this specific “switch-to-place” deficit could account for apparent impairments in both navigational strategy switching and allocentric processing and contributes more generally to age-related decline in navigation.

How age-related strategy switching deficits affect wayfinding in complex environments

Although most research on navigation in aging focuses on allocentric processing deficits, impaired strategy switching may also contribute to navigational decline. Using a specifically designed task involving navigating a town-like virtual environment, we assessed the ability of young and old participants to switch from following learned routes to finding novel shortcuts. We found large age differences in the length of routes taken during testing and in use of shortcuts, as, while nearly all young participants switched from the egocentric route-following strategy to the allocentric wayfinding strategy, none of the older participants stably switched. Although secondary tasks confirmed that older participants were impaired both at strategy switching and allocentric processing, the difficulty in using shortcuts was selectively related to impaired strategy switching. This may in turn relate to dysfunction of the prefrontal-noradrenergic network responsible for coordinating switching behavior. We conclude that the large age difference in performance at the shortcutting task demonstrates for the first time, how strategy switching deficits can have a severe impact on navigation in aging.

Personality stability from age 14 to age 77 years.

There is evidence for differential stability in personality trait differences, even over decades. The authors used data from a sample of the Scottish Mental Survey, 1947 to study personality stability from childhood to older age. The 6-Day Sample (N = 1,208) were rated on six personality characteristics by their teachers at around age 14. In 2012, the authors traced as many of these participants as possible and invited them to take part in a follow-up study. Those who agreed (N = 174) completed a questionnaire booklet at age 77 years, which included rating themselves and asking someone who knew them well to rate them on the same 6 characteristics on which they were rated in adolescence. Each set of 6 ratings was reduced to the same single underlying factor, denoted dependability, a trait comparable to conscientiousness. Participants’ and others’ older-age personality characteristic ratings were moderately correlated with each other, and with other measures of personality and wellbeing, but correlations suggested no significant stability of any of the 6 characteristics or their underlying factor, dependability, over the 63-year interval. However, a more complex model, controlling rater effects, indicated significant 63-year stability of 1 personality characteristic, Stability of Moods, and near-significant stability of another, Conscientiousness. Results suggest that lifelong differential stability of personality is generally quite low, but that some aspects of personality in older age may relate to personality in childhood.

Wakeful rest promotes the integration of spatial memories into accurate cognitive maps

Flexible spatial navigation, e.g. the ability to take novel shortcuts, is contingent upon accurate mental representations of environments‐cognitive maps. These cognitive maps critically depend on hippocampal place cells. In rodents, place cells replay recently travelled routes, especially during periods of behavioural inactivity (sleep/wakeful rest). This neural replay is hypothesised to promote not only the consolidation of specific experiences, but also their wider integration, e.g. into accurate cognitive maps. In humans, rest promotes the consolidation of specific experiences, but the effect of rest on the wider integration of memories remained unknown. In the present study, we examined the hypothesis that cognitive map formation is supported by rest‐related integration of new spatial memories. We predicted that if wakeful rest supports cognitive map formation, then rest should enhance knowledge of overarching spatial relations that were never experienced directly during recent navigation. Forty young participants learned a route through a virtual environment before either resting wakefully or engaging in an unrelated perceptual task for 10 min. Participants in the wakeful rest condition performed more accurately in a delayed cognitive map test, requiring the pointing to landmarks from a range of locations. Importantly, the benefit of rest could not be explained by active rehearsal, but can be attributed to the promotion of consolidation‐related activity. These findings (i) resonate with the demonstration of hippocampal replay in rodents, and (ii) provide the first evidence that wakeful rest can improve the integration of new spatial memories in humans, a function that has, hitherto, been associated with sleep.

Comparable rest-related promotion of spatial memory consolidation in younger and older adults.

Flexible spatial navigation depends on cognitive mapping, a function that declines with increasing age. In young adults, a brief period of postnavigation rest promotes the consolidation and integration of spatial memories into accurate cognitive maps. We examined (1) whether rest promotes spatial memory consolidation and integration in older adults; and (2) whether the magnitude of the rest benefit changes with increasing age. Young and older adults learned a route through a virtual environment, followed by a 10-minute delay comprising either wakeful rest or a perceptual task, and a subsequent cognitive mapping task, requiring the pointing to landmarks from different locations. Pointing accuracy was lower in the older than younger adults. However, there was a comparable rest-related enhancement in pointing accuracy in the 2 age groups. Together our findings suggest that (1) the age-related decline in cognitive mapping cannot be explained by increased consolidation interference in older adults; and (2) as we grow older, rest continues to support the consolidation and integration of spatial memories.

Stress in childhood, adolescence and early adulthood, and cortisol levels in older age

Abstract The glucocorticoid hypothesis suggests that overexposure to stress may cause permanent upregulation of cortisol. Stress in youth may therefore influence cortisol levels even in older age. Using data from the 6-Day Sample, we investigated the effects of high stress in childhood, adolescence and early adulthood – as well as individual variables contributing to these measures; parental loss, social deprivation, school and home moves, illness, divorce and job instability – upon cortisol levels at age 77 years. Waking, waking +45 min (peak) and evening salivary cortisol samples were collected from 159 participants, and the 150 who were not using steroid medications were included in this study. After correcting for multiple comparisons, the only significant association was between early-adulthood job instability and later-life peak cortisol levels. After excluding participants with dementia or possible mild cognitive impairment, early-adulthood high stress showed significant associations with lower evening and mean cortisol levels, suggesting downregulation by stress, but these results did not survive correction for multiple comparisons. Overall, our results do not provide strong evidence of a relationship between stress in youth and later-life cortisol levels, but do suggest that some more long-term stressors, such as job instability, may indeed produce lasting upregulation of cortisol, persisting into the mid-to-late seventies.

Cognitive ability across the life course and cortisol levels in older age

Elevated cortisol levels have been hypothesized to contribute to cognitive aging, but study findings are inconsistent. In the present study, we examined the association between salivary cortisol in older age and cognitive ability across the life course. We used data from 370 members of the 36-Day Sample of the Scottish Mental Survey 1947, who underwent cognitive testing at age 11 years and were then followed up at around age 78 years, completing further cognitive tests and providing diurnal salivary cortisol samples. We hypothesized that higher cortisol levels would be associated with lower cognitive ability in older age and greater cognitive decline from childhood to older age but also lower childhood cognitive ability. Few of the tested associations were significant, and of those that were, most suggested a positive relationship between cortisol and cognitive ability. Only 1 cognitive measure showed any sign of cortisol-related impairment. However, after correcting for multiple comparisons, no results remained significant. These findings suggest that cortisol may not play an important role in cognitive aging across the life course.

Personality and Other Lifelong Influences on Older‐Age Health and Wellbeing: Preliminary Findings in Two Scottish Samples

Recent observations that personality traits are related to later–life health and wellbeing have inspired considerable interest in exploring the mechanisms involved. Other factors, such as cognitive ability and education, also show longitudinal influences on health and wellbeing, but it is not yet clear how all these early–life factors together contribute to later–life health and wellbeing. In this preliminary study, we assessed hypothesised relations among these variables across the life course, using structural equation modelling in a sample assessed on dependability (a personality trait related to conscientiousness) in childhood, cognitive ability and social class in childhood and older age, education, and health and subjective wellbeing in older age. Our models indicated that both health and subjective wellbeing in older age were influenced by childhood IQ and social class, via education. Some older–age personality traits mediated the effects of early–life variables, on subjective wellbeing in particular, but childhood dependability did not show significant associations. Our results therefore did not provide evidence that childhood dependability promotes older–age health and wellbeing, but did highlight the importance of other early–life factors, particularly characteristics that contribute to educational attainment. Further, personality in later life may mediate the effects of early–life factors on health and subjective wellbeing.