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

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.

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

In the originally published version of article, there were two errors in the references. The reference "Nilsson, J. & Lövdén, M. Naming is not explaining: future directions for the "cognitive reserve" and "brain maintenance" theories. Alzheimer's Res. Ther. 10, 34 (2018)" was missing. This reference has been added as REF. 14 in the HTML and PDF versions of the article and cited at the end of the sentence "However, over the years, these terms have been used inconsistently, creating confusion and slowing progress." on page 701 and at the end of the sentence "If reserve is defined merely as the factor that individuals with greater reserve have and then this factor is used to explain why some individuals have greater reserve, the argument is clearly circular." on page 704. The reference list has been renumbered accordingly. In addition, in the original reference list, REF. 91 was incorrect. The reference should have read "Cabeza, R. Hemispheric asymmetry reduction in older adults. The HAROLD model. Psychol. Aging 17, 85-100 (2002)". This reference, which is REF. 92 in the corrected reference list, has been corrected in the HTML and PDF versions of the article.

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

In Figure 3b of the originally published article, the colours of the bars were incorrectly reversed. The bars shown in green should have been shown in blue to represent the findings from older adults, whereas the bars shown in blue should have been shown in green to represent the findings from young adults. This has been corrected in the HTML and PDF versions of the article. Images of the original figure are shown in the correction notice.

Gray Matter Volume as Evidence for Cognitive Reserve in Bilinguals With Mild Cognitive Impairment.

BACKGROUND: Compared with monolinguals, bilinguals have a later onset of mild cognitive impairment (MCI) and Alzheimer disease symptoms and greater neuropathology at similar cognitive and clinical levels. The present study follows a previous report showing the faster conversion from MCI to Alzheimer disease for bilingual patients than comparable monolinguals, as predicted by a cognitive reserve (CR). PURPOSE: Identify whether the increased CR found for bilinguals in the previous study was accompanied by greater gray matter (GM) atrophy than was present for the monolinguals. METHODS: A novel deep-learning technique based on convolutional neural networks was used to enhance clinical scans into 1 mm MPRAGEs and analyze the GM volume at the time of MCI diagnosis in the earlier study. PATIENTS: Twenty-four bilingual and 24 monolingual patients were diagnosed with MCI at a hospital memory clinic. RESULTS: Bilingual patients had more GM loss than monolingual patients in areas related to language processing, attention, decision-making, motor function, and episodic memory retrieval. Bilingualism and age were the strongest predictors of atrophy after other variables such as immigration and education were included in a multivariate model. DISCUSSION: CR from bilingualism is evident in the initial stages of neurodegeneration after MCI has been diagnosed.

Reducing age-related Memory Deficits: The Roles of Environmental Support and self-initiated Processing Activities.

BACKGROUND: The notion that memory performance in older adults can be boosted by information provided by the environment was proposed by Craik (1983). The suggestion was that age-related memory deficits can be attenuated and sometimes even eliminated by a complementary combination of environmental support and consciously controlled self-initiated activities. OBJECTIVE: The objective of the present article was to review the subsequent empirical and theoretical work on the topics of environmental support and self-initiated ativities as they relate to the effects of aging on human memory. DISCUSSION: The notion of schematic support from the person's knowledge base is introduced and its relevance discussed. In addition, the effects of various types of support on encoding and retrieval processes in older adults are desribed, and the increasing theoretical importance of executive processes in reducing age-related memory deficits is discussed. CONCLUSION: As one main conclusion, it is suggested that self-initiated control processes interact with both information provided by the environment and by the person's knowledge base to improve the effectiveness of encoding and retrieval processing in older adults.

Remembering: An Activity of Mind and Brain.

I present the case for viewing human memory as a set of dynamic processes rather than as structural entities or memory stores. This perspective stems largely from the construct of levels of processing, reflecting work I published with Robert Lockhart and with Endel Tulving. I describe the personal and professional contexts in which these and other ideas evolved, and I discuss criticisms of the ideas and our responses to critics. I also show how later versions of a processing approach to memory may fit with current findings and theories in memory research. In related work I have been involved in studies of cognitive aging, and I describe some theoretical and empirical points deriving from this aspect of my research efforts. Finally, I deal briefly with some experiments and reflections on divided attention, consolidation, and bilingualism and touch upon the neural bases of a processing approach.

Conversion of Mild Cognitive Impairment to Alzheimer Disease in Monolingual and Bilingual Patients.

PURPOSE: Conversion rates from mild cognitive impairment (MCI) to Alzheimer disease (AD) were examined considering bilingualism as a measure of cognitive reserve. METHODS: Older adult bilingual (n=75) and monolingual (n=83) patients attending a memory clinic who were diagnosed with MCI were evaluated for conversion to AD. Age of MCI and AD diagnoses and time to convert were recorded and compared across language groups. PATIENTS: Patients were consecutive patients diagnosed with MCI at a hospital memory clinic. RESULTS: Bilingual patients were diagnosed with MCI at a later age than monolingual patients (77.8 and 75.5 y, respectively), a difference that was significant in some analyses. However, bilingual patients converted faster from MCI to AD than monolingual patients (1.8 and 2.8 y, respectively) resulting in no language group difference in age of AD diagnosis. This relationship held after accounting for education, cognitive level, immigration status, and sex. DISCUSSION: The findings suggest that greater cognitive reserve as measured by language status leads to faster conversion between MCI and AD, all else being equal.

Prospective Memory Is a Key Predictor of Functional Independence in Older Adults.

OBJECTIVES: Prospective memory (PM), the ability to execute delayed intentions, has received increasing attention in neuropsychology and gerontology. Most of this research is motivated by the claim that PM is critical for maintaining functional independence; yet, there is a dearth of empirical evidence to back up the claims. Thus, the present study tested whether PM predicts functional independence in older adults using validated behavioral performance measures for both PM and functional independence. METHODS: Fifty-eight healthy older adults performed a computerized PM paradigm, the Virtual Week task, as well as a timed version of an instrumental activities of daily living (TIADL) task. Furthermore, we assessed vocabulary, processing speed, and self-reported prospective remembering. RESULTS: TIADL scores correlated significantly with performance in the Virtual Week task, vocabulary, and processing speed. Hierarchical linear regressions revealed that vocabulary and Virtual Week performance were significant predictors for TIADL. However, self-reported PM scores did not predict everyday functioning. CONCLUSIONS: The findings indicate that PM is an important cognitive ability for successful and independent everyday life beyond vocabulary. Moreover, the results show a substantial incremental contribution of intact PM performance for the prediction of everyday functioning by using objective PM measures. (JINS, 2018, 24, 640-645).

Effects of divided attention at encoding and retrieval: Further data.

Division of attention (DA) at the time of learning has large detrimental effects on subsequent memory performance, but DA at retrieval has much smaller effects (Baddeley, Lewis, Eldridge, & Thomson, 1984, Journal of Experimental Psychology: General, 113, 518-540; Craik, Govoni, Naveh-Benjamin, & Anderson, 1996, Journal of Experimental Psychology: General, 125, 159-180). Experiment 1 confirmed the relatively small effects of DA on retrieval and also showed that retrieval operations do consume processing resources. The experiment also found that the effect is not attributable to a trade-off in performance with the concurrent task or to recognition decisions made on the basis of familiarity judgments. Participants made levels-of-processing (LOP) judgments during encoding to check whether deeper semantic judgments were differentially vulnerable to the effects of DA. In fact DA did not interact with LOP. Experiment 2 explored reports that the comparatively slight effect of DA on recognition accuracy is accompanied by a compensatory increase in recognition latency (Baddeley et al., 1984). The experiment replicated findings that neither DA nor differential emphasis between recognition and a concurrent continuous reaction time (CRT) task affected recognition accuracy, but also found evidence for a lawful trade-off in decision latencies between recognition and CRT performance. Further analysis showed that the relationship between response rates on the two tasks was well described by a linear function, and that this function was demonstrated by the majority of individual participants. It is concluded that the small effect of DA on recognition performance is attributable to a trade-off within the recognition task itself; accuracy is maintained by a compensatory increase in decision latency.

Learning facts during aging: the benefits of curiosity.

Background/study context: Recent studies have shown that young adults better remember factual information they are curious about. It is not entirely clear, however, whether this effect is retained during aging. Here, the authors investigated curiosity-driven memory benefits in young and elderly individuals. METHODS: In two experiments, young (age range 18-26) and older (age range 65-89) adults read trivia questions and rated their curiosity to find out the answer. They also attended to task-irrelevant faces presented between the trivia question and the answer. The authors then administered a surprise memory test to assess recall accuracy for trivia answers and recognition memory performance for the incidentally learned faces. RESULTS: In both young and elderly adults, recall performance was higher for answers to questions that elicited high levels of curiosity. In Experiment 1, the authors also found that faces presented in temporal proximity to curiosity-eliciting trivia questions were better recognized, indicating that the beneficial effects of curiosity extended to the encoding of task-irrelevant material. CONCLUSIONS: These findings show that elderly individuals benefit from the memory-enhancing effects of curiosity. This may lead to the implementation of learning strategies that target and stimulate curiosity in aging.

Levels of processing in working memory: differential involvement of frontotemporal networks.

How does the brain maintain to-be-remembered information in working memory (WM), particularly when the focus of attention is drawn to processing other information? Cognitive models of WM propose that when items are displaced from focal attention recall involves retrieval from long-term memory (LTM). In this fMRI study, we tried to clarify the role of LTM in performance on a WM task and the type of representation that is used to maintain an item in WM during rehearsal-filled versus distractor-filled delays. Participants made a deep or shallow levels-of-processing (LOP) decision about a single word at encoding and tried to recall the word after a delay filled with either rehearsal of the word or a distracting math task. Recalling one word after 10 sec of distraction demonstrated behavioral and neural indices of retrieval from LTM (i.e., LOP effects and medial-temporal lobe activity). In contrast, recall after rehearsal activated cortical areas that reflected reporting the word from focal attention. In addition, areas that showed an LOP effect at encoding (e.g., left ventrolateral VLPFC and the anterior temporal lobes [ATLs]) were reactivated at recall, especially when recall followed distraction. Moreover, activity in left VLPFC during encoding, left ATL during the delay, and left hippocampus during retrieval predicted recall success after distraction. Whereas shallow LOP and rehearsal-related areas supported active maintenance of one item in focal attention, the behavioral processes and neural substrates that support LTM supported recall of one item after it was displaced from focal attention.

Short-term retention of a single word relies on retrieval from long-term memory when both rehearsal and refreshing are disrupted.

Many working memory (WM) models propose that the focus of attention (or primary memory) has a capacity limit of one to four items, and therefore, that performance on WM tasks involves retrieving some items from long-term (or secondary) memory (LTM). In the present study, we present evidence suggesting that recall of even one item on a WM task can involve retrieving it from LTM. The WM task required participants to make a deep (living/nonliving) or shallow ("e"/no "e") level-of-processing (LOP) judgment on one word and to recall the word after a 10-s delay on each trial. During the delay, participants either rehearsed the word or performed an easy or a hard math task. When the to-be-remembered item could be rehearsed, recall was fast and accurate. When it was followed by a math task, recall was slower, error-prone, and benefited from a deeper LOP at encoding, especially for the hard math condition. The authors suggest that a covert-retrieval mechanism may have refreshed the item during easy math, and that the hard math condition shows that even a single item cannot be reliably held in WM during a sufficiently distracting task--therefore, recalling the item involved retrieving it from LTM. Additionally, performance on a final free recall (LTM) test was better for items recalled following math than following rehearsal, suggesting that initial recall following math involved elaborative retrieval from LTM, whereas rehearsal did not. The authors suggest that the extent to which performance on WM tasks involves retrieval from LTM depends on the amounts of disruption to both rehearsal and covert-retrieval/refreshing maintenance mechanisms.

Endel Tulving (1927-2023).

This article presents an obituary for Endel Tulving. Tulving's educational and professional careers are summarized. His work in the field of human memory is detailed. It is noted that Tulving's look at the field of verbal learning in the late 1950s persuaded him that the dominant associative tradition missed many important aspects of human memory. His research found that at the time of retrieval, memory for the original event may be successfully reinstated only by contextual cues that interact in a complementary fashion with the specifically encoded memory trace, a process that Tulving referred to as "synergistic ecphory". He is also known for his work on memory systems. In his book, Elements of Episodic Memory published in 1983, Tulving proposed that memory for experienced events, episodic memory, should be distinguished from general knowledge of the world, semantic memory, and from procedural memory, the learned ability to perform such skilled procedures as riding a bicycle or playing a musical instrument. He also proposed an evolutionary framework for these different but related systems, suggesting that simple animals show only procedural memory, more complex animals are consciously aware of their knowledge of the world, but only humans possess episodic memory-the ability to use "mental time travel" to consciously recreate past experiences and to imagine possible future events. Although known initially for his purely cognitive behavioral research, during the 1980s and 1990s, Tulving increasingly incorporated neuropsychological and neuroimaging approaches into his work. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

The role of intentionality in memory and learning: Comments on Popov and Dames (2022).

This commentary is a reply to the article "Intent matters: Resolving the intentional versus incidental learning paradox in episodic long-term memory" by Popov and Dames (2022). In their article, the authors question the view that once adequate deep, elaborate, and organizational processes have been induced incidentally, the intention to learn adds nothing further to the level of subsequent retention. Opposing this view, Popov and Dames conclude that intention to learn is always necessary for good memory performance and support this claim with the results of 11 experiments in which they find strong effects of intentionality using mixed-list designs in which all items are processed semantically but only half need be remembered later. The present commentary suggests that intentionality leads to selectively greater amounts of item processing and organizational processing of the to-be-remembered items in mixed lists, and that these further operations result in higher levels of recall. In light of this interpretation, the commentary argues for the validity of the original conclusion that retention is determined by the qualitative type of processing carried out on the items to be remembered, however that processing is induced. The commentary concludes by discussing various factors that modulate the effect of intentionality on memory and learning, and by suggesting a scheme that may aid the understanding of these effects, and serve as a framework for future studies. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Memory, aging and the brain: Old findings and current issues.

In this article I reprise some selected findings and issues from my previous behavioural work on age-related differences in memory, and relate them to current work on the neural correlates of encoding, retrieval and representation. In particular, I describe the case study of a woman who had persistent experiences of erroneous recollection. I also describe the results of a study showing a double dissociation of implicit and explicit memory in younger and older adults. Finally, I assess recent work on loss of specificity in older adults' encoding and retrieval processes of episodic events. In all cases I attempt to relate these older findings to current ideas and empirical results in the area of memory, aging, and the brain.

The cognitive tenacity of self-directed ageism.

Ageism refers to prejudice or discrimination based on a person's age. When ageism is directed at older people, it is unique in two ways: it is socially condoned in a manner that other types of prejudice are not, and the animus is eventually self-directed. Of central interest here is why ageism becomes self-directed in late adulthood, despite its potentially harmful personal costs. We present a cognitive model in which negative ageist beliefs become increasingly accessible and difficult to eliminate owing to broader developmental shifts in mentation. Given that these effects are contingent on our social environment, systemic changes in societal conceptions of age and aging are needed if we are to reduce vulnerability to self-directed ageism.

Lifelong bilingualism maintains white matter integrity in older adults.

Previous research has shown that bilingual speakers have higher levels of cognitive control than comparable monolinguals, especially at older ages. The present study investigates a possible neural correlate of this behavioral effect. Given that white matter (WM) integrity decreases with age in adulthood, we tested the hypothesis that bilingualism is associated with maintenance of WM in older people. Using diffusion tensor imaging, we found higher WM integrity in older people who were lifelong bilinguals than in monolinguals. This maintained integrity was measured by fractional anisotropy (FA) and was found in the corpus callosum extending to the superior and inferior longitudinal fasciculi. We also hypothesized that stronger WM connections would be associated with more widely distributed patterns of functional connectivity in bilinguals. We tested this by assessing the resting-state functional connectivity of frontal lobe regions adjacent to WM areas with group differences in FA. Bilinguals showed stronger anterior to posterior functional connectivity compared to monolinguals. These results are the first evidence that maintained WM integrity is related to lifelong naturally occurring experience; the resulting enhanced structural and functional connectivity may provide a neural basis for "brain reserve."

How does bilingualism modify cognitive function? Attention to the mechanism.

It has been claimed that bilingual experience leads to an enhancement of cognitive control across the lifespan, a claim that has been investigated by comparing monolingual and bilingual groups performing standard executive function (EF) tasks. The results of these studies have been inconsistent, however, leading to controversy over the essential assumptions underlying the research program, namely, whether bilingualism produces cognitive change. We argue that the source of the inconsistency is not in the evidence but rather in the framework that has typically been used to motivate the research and interpret the results. We examine the componential view of EF with its central role for inhibition and argue that it provides a poor fit to both bilingual experience and the results of these studies. As an alternative, we propose a more holistic account based on attentional control that overrides the processes in the componential model of EF and applies to a wider range of tasks. The key element in our account is that behavioral differences between monolingual and bilingual individuals reflect differences in the efficiency and deployment of attentional control between the two language groups. In support of this point we show how attentional control provides a more satisfactory account for a range of findings that cannot reasonably be attributed to inhibition. We also suggest that group differences will emerge only when the attentional demands of a task exceed the control abilities of one of the groups, regardless of the EF components involved. We then review literature from across the lifespan to evaluate the extent to which this account is consistent with existing evidence, and conclude with some suggestions on how the field may be advanced by new lines of empirical enquiry.

Past experience modulates the neural mechanisms of episodic memory formation.

Neuroscientists have observed the "birth" of memories, but have not explored how an organism's past experience with materials interacts with the neural mechanisms of episodic memory formation. Using functional neuroimaging, we searched for such an interaction by examining brain activity during memory encoding that predicted participants' subsequent episodic memory for novel and repeated scenes. Memory for both scene types was predicted by a common posterior network in occipital and parietal cortices. Medial temporal memory predictors were modulated by scene repetition: the right anterior hippocampus and right amygdala predicted memory for novel scenes only, whereas posterior hippocampi predicted memory for repeated scenes only. There was also greater functional connectivity between the temporal pole and anterior versus posterior hippocampus, and this link predicted memory for novel but not repeated scenes. In contrast, there was greater functional connectivity between the precuneus and posterior versus anterior hippocampus, and this link predicted memory for repeated but not novel scenes. Together, these results reveal a functional specialization within the hippocampus for the encoding of novel and previously experienced materials, and suggest that the topography of this specialization might be related to local variations in connectivity. Because episodic memory for repeated scenes was superior, our results also support traditional views of encoding emphasizing the role of prior representations, and illuminate one way in which humans use existing memories to help form new ones. In so doing, our results challenge recent novelty-encoding hypotheses.