Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing

Abstract

Cognitive ageing research examines the cognitive abilities that are preserved and/or those that decline with advanced age. There is great individual variability in cognitive ageing trajectories. Some older adults show little decline in cognitive ability compared with young adults and are thus termed 'optimally ageing'. By contrast, others exhibit substantial cognitive decline and may develop dementia. Human neuroimaging research has led to a number of important advances in our understanding of the neural mechanisms underlying these two outcomes. However, interpreting the age-related changes and differences in brain structure, activation and functional connectivity that this research reveals is an ongoing challenge. Ambiguous terminology is a major source of difficulty in this venture. Three terms in particular - compensation, maintenance and reserve - have been used in a number of different ways, and researchers continue to disagree about the kinds of evidence or patterns of results that are required to interpret findings related to these concepts. As such inconsistencies can impede progress in both theoretical and empirical research, here, we aim to clarify and propose consensual definitions of these terms.

Figure 1.

A. Individual differences in cognitive aging have been attributed to three interacting mechanisms, reserve, maintenance, and compensation mechanisms, which are all affected by genetic and environmental factors. B-D. Schematic charts illustrate hypothesized changes in brain resources and cognitive demand as a result of reserve, maintenance and compensation mechanisms. In the ideal scenario, these mechanisms completely eliminate age effects, whereas in the typical scenario, they only attenuate age effects. Reserve, maintenance, and compensation are hypothesized to involve an increase in brain resources (blue upward arrows) but differ regarding (1) the order of the brain resource increase in relation to brain decline (blue downward arrow), (2) the time-scale of the changes (x-axes of the graphs), and (3) the relation to cognitive demands. B. In the case of reserve, neural resources accumulate beyond what it is required to satisfy current cognitive demands, so that when these resources start to decline in old age, cognitive decline is attenuated. It is important to note that although the graph shows resources accumulating during childhood and young adulthood, cognitive reserve can continue growing in old age. C. In the case of maintenance, processes of neural decline are continuously offset by processes of neural enhancement. Given that neural decline increases in old age, greater maintenance is also required to maintain the same level of performance. The figure shows neural decline (downward arrows) and neural enhancement processes in alternation for illustration purposes only, as these processes can occur simultaneously. D. In the case of compensation, a task-related increase in cognitive demands is counteracted by the recruitment of additional neural resources.

Figure 2.. Maintenance.

A. Consistent with the idea stable cognitive performance is associated with maintenance, individuals aged 65–80 yrs who showed minimal episodic memory decline on verbal immediate free recall and delayed cued recall tasks during a 4-year period (maintainers) also showed less hippocampal volume decline, as measured by FreeSurfer using the Desikan-Killiany atlas, over 4 years compared to decliners (from REF.). B. Also consistent with maintenance, over a period of two decades, Old-maintainers (mean age = 68.8 yrs) who showed no significant episodic memory decline on verbal immediate free recall and delayed cued recall tasks compared to young adults (mean age = 35.3), also displayed comparable levels of hippocampal activity during an fMRI study of face-name associative encoding, compared to young adults. In contrast, Old-decliners showed longitudinal episodic memory decline in the aforementioned verbal tasks, and exhibited significantly lower hippocampal activity during associative encoding, compared to young adults and Old-maintainers (from REF.). Consistent with the idea that there can be high-maintenance and low-maintenance, in these studies, maintainers and decliners were defined independently of their absolute levels of memory and hippocampal activity. It is impossible in these studies to know if maintenance involved repair or just absence of decline.

Figure 3.. Compensation.

A. Hypothetical demand-activity function in young and old adults: as task demands increase activity first rises, then asymptotes, and finally declines. Because of reduced neural resources, this demand-activity function is shifted to the left in older adults, and hence they tend to show greater activity in the same regions as younger adults at lower levels of task difficulty (e.g., level 2) but lower activity at higher levels of task difficulty. B. Example of compensation by upregulation (consistent with the hypothetical function in panel A): in an fMRI study, older adults showed greater working memory activity in the right DLPFC than younger adults at lower levels of task demands (working memory load of 5 letters) but less activity at higher levels of task demands higher working memory load (working memory load of 7 letters, from REF.) . C. Example of compensation by selection. This fMRI study compared age effects on the rich form of memory known as “recollection” and the less precise form of memory known as “familiarity,” measured in the same recognition memory task. Compared to younger adults, older adults showed reduced recollection-related activity in the hippocampus but increased familiarity-related activity in rhinal cortex . Thus, older adults compensated for deficits in an optimal but demanding process (recollection) by recruiting a suboptimal but less demanding process (familiarity). D. Example of compensation by reorganization. During an episodic memory retrieval task, young adults and low-performing older adults showed unilateral frontal activity whereas high-performing older adults showed bilateral frontal activity, suggesting a reorganization of the episodic retrieval network (from REF.).