Neurocognitive Aging and the Compensation Hypothesis

ABSTRACT— The most unexpected and intriguing result from functional brain imaging studies of cognitive aging is evidence for age-related overactivation: greater activation in older adults than in younger adults, even when performance is age-equivalent. Here we examine the hypothesis that age-related overactivation is compensatory and discuss the compensation-related utilization of neural circuits hypothesis (CRUNCH). We review evidence that favors a compensatory account, discuss questions about strategy differences, and consider the functions that may be served by overactive brain areas. Future research directed at neurocognitively informed training interventions may augment the potential for plasticity that persists into the later years of the human lifespan.     

Age-related changes in discrimination of unfamiliar odors

If odor perception involves mnemonic processes, differences in olfactory experience should affect discriminative ability. This was examined here by comparing discriminative performance in children and adults. Using an oddity test of discrimination, in Experiment 1 we tested 6-year-olds (G1), 11-year-olds (G6), and adults (A) on their ability to discriminate unfamiliar odors that varied either in quality (Q) or in quality and intensity (QI). G1 participants were poorer at discriminating the QI set, relative to G6 and A. In Experiment 2, we used an analogous visual procedure and confirmed that this age-related difference was olfactory specific. In Experiment 3, we repeated Experiment 1 but used an articulatory suppression task. G1 participants were poorer than G6 and A participants for both the Q and the QI sets. The implications of these findings for experiential accounts of odor perception and olfactory working memory are discussed.     

Adaptation to direction-dependent visuo-motor rotations and its decay in younger and older adults

We studied adaptation to a direction-dependent visuo-motor rotation in adults of early and late working age. For hand movements to the right, visual motion of the cursor on a monitor was rotated clockwise, for forward movements rotation of the cursor motion was zero, and for directions in-between rotation was intermediate. In contrast to previous studies, in which adaptation was more difficult (larger visuo-motor rotation, larger number of targets during practice) and the older age group was of higher age, we found no age-related deficit of adaptation. However, consistent with previous studies we found an age-related impairment of explicit knowledge of the visuo-motor rotation and no age-related differences of aftereffects. Across periods of not performing the task for 24 h and of performing the task for a prolonged period of time without visual feedback, we observed a decay of adaptation which did not depend on age. The present findings cast doubts on the prevalent interpretation of age-related impairments of adaptation in the absence of age-related changes of aftereffects as resulting from intentional strategic corrections, which become less efficient at higher age.     

Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function

Given the aging populations in many countries throughout the world, there is an increasing interest in lifestyle factors and interventions that will enhance the cognitive vitality of older adults and reduce the risk for age-related neurological disorders, such as Alzheimer's disease. In this review, we evaluate the hypothesis that physical activity and exercise might serve to protect, and also enhance, cognitive and brain function across the adult lifespan. To this end, we critically review three separate literatures that have examined the influence of physical activity and exercise on cognition, brain function and brain structure of adults, including epidemiological or prospective observational studies, randomized human clinical interventions and non-human animal studies. We suggest that this literature supports the claim that physical activity enhances cognitive and brain function, and protects against the development of neurodegenerative diseases. We discuss future directions to address currently unresolved questions, such as interactions between multiple lifestyle factors on offsetting or protecting against cognitive and neural decline, and conclude that physical activity is an inexpensive treatment that could have substantial preventative and restorative properties for cognitive and brain function.     

A systematic review of interventions for adults who stutter

PurposeTo examine the effectiveness of (i) face to face interventions (ii) models of service delivery and (iii) psychological treatments combined with speech-focused interventions for adults who stutter.MethodsFive electronic databases and three clinical trial registries were searched. Systematic reviews, randomised controlled trials (RCTs) and studies that applied an intervention with adults who stutter were included. Pharmaceutical interventions were excluded. Primary outcomes included a measure of stuttering severity. Risk of bias assessment was conducted on included studies and overall quality of the evidence was graded.ResultsFive RCTS, four registered trials and three systematic reviews met inclusion criteria. Intervention approaches included speech restructuring programs (e.g. Camperdown Program) and transcranial direct current stimulation (tDCS). One study investigated cognitive behaviour therapy (CBT) alongside speech restructuring. Overall, studies were classified low risk of bias and good quality. Speech restructuring was included in all but one study (tDCS study) and had the most evidence i.e. supported by the greatest number of RCTs. On average, stuttering frequency was reduced by 50–57 % using speech restructuring approaches. No study reduced stuttering to the same level as community controls who don’t stutter. The study on tDCS reduced stuttering frequency by 22–27 %. Speech restructuring delivered via telehealth was non-inferior to face-to-face intervention. One study reported CBT was an effective adjunct to speech restructuring interventions.ConclusionSpeech restructuring interventions were found to reduce stuttering in adults, however degree and maintenance of fluency varied. The body of evidence surrounding tDCS and psychological interventions is limited. Replication studies should be considered.     

Binocular detection of masked patterns in young and old observers

A visual pattern embedded in noise is detected appreciably better when the stimulus complex contains interocular cues (dichoptic condition) than when such cues are absent (binoptic condition). In a recent study (F. Speranza, G. Moraglia, & B. A. Schneider, 1995) the authors showed that the relative difference between binoptic and dichoptic thresholds does not change with age. However, older adults showed higher binoptic and dichoptic thresholds, thus suggesting an age-related difficulty with degraded stimulation. In this article the authors first replicated these findings and proceeded next to investigating whether age-related changes in processing efficiency, additive internal noise, and the spatial frequency bandwidth of the detecting filters could account, separately or concurrently, for the elevated thresholds in noise exhibited by the older adults. Results indicate that this increase is not attributable to age-related changes in filter bandwidth or internal noise. Rather, the findings can be explained in terms of a decrease in processing efficiency with age.     

Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons

Mutations in the neuronal-specific microtubule-binding protein TAU are associated with several dementias and neurodegenerative diseases. However, the effects of elevated TAU accumulation on behavioral plasticity are unknown. We report that directed expression of wild-type vertebrate and Drosophila TAU in adult mushroom body neurons, centers for olfactory learning and memory in Drosophila, strongly compromised associative olfactory learning and memory, but olfactory conditioning-relevant osmotactic and mechanosensory responses remained intact. In addition, TAU accumulation in mushroom body neurons did not result in detectable neurodegeneration or premature death. Therefore, TAU-mediated structural or functional perturbation of the microtubular cytoskeleton in mushroom body neurons is likely causal of the behavioral deficit. These results indicate that behavioral plasticity decrements may be the earliest detectable manifestations of tauopathies.     

Cognitive Interventions for Cognitively Healthy,Mildly Impaired,and Mixed Samples of Older Adults: A Systematic Review and Meta-Analysis of Randomized-Controlled Trials

Cognitive interventions may improve cognition, delay age-related cognitive declines, and improve quality of life for older adults. The current meta-analysis was conducted to update and expand previous work on the efficacy of cognitive interventions for older adults and to examine the impact of key demographic and methodological variables. EBSCOhost and Embase online databases and reference lists were searched to identify relevant randomized-controlled trials (RCTs) of cognitive interventions for cognitively healthy or mildly impaired (MCI) older adults (60+ years). Interventions trained a single cognitive domain (e.g., memory) or were multi-domain training, and outcomes were assessed immediately post-intervention using standard neuropsychological tests. In total, 279 effects from 97 studies were pooled based on a random-effects model and expressed as Hedges’ g (unbiased). Overall, results indicated that cognitive interventions produce a small, but significant, improvement in the cognitive functioning of older adults, relative to active and passive control groups (g = 0.298, p < .001, 95% CI = 0.248–0.347). These results were confirmed using multi-level analyses adjusting for nesting of effect sizes within studies (g = 0.362, p < .001, 95% CI = 0.275, 0.449). Age, education, and cognitive status (healthy vs. MCI) were not significant moderators. Working memory interventions proved most effective (g = 0.479), though memory, processing speed, and multi-domain interventions also significantly improved cognition. Effects were larger for directly trained outcomes but were also significant for non-trained outcomes (i.e., “transfer effects”). Implications for future research and clinical practice are discussed. This project was pre-registered with PROSPERO (#42016038386).     

Age-related differences in memory after attending to distinctiveness or similarity during learning

Episodic memory is vulnerable to age-related change, with older adults demonstrating both impairments in retrieving contextual details and susceptibility to interference among similar events. Such impairments may be due in part to an age-related decline in the ability to encode distinct memory representations. Recent research has examined how manipulating stimulus properties to emphasize distinctiveness can reduce age-related deficits in memory. However, few studies have addressed whether learning strategies that differentially encourage distinctiveness processing attenuate age-related differences in episodic memory. In the present study, participants engaged in two incidental encoding tasks emphasizing either distinctiveness or similarity processing. Results demonstrated higher rates of recollection for stimuli studied under the distinctiveness task than the similarity task in younger but not older adults. These findings suggest a declining capacity for distinctiveness processing to benefit memory in older adults, and raise the possibility that strategies that enhance gist-based encoding may attenuate age-related memory deficits.     

The attentional demands of encoding and retrieval in younger and older adults: 2. Evidence from secondary task reaction time distributions

Three studies examined the effects of encoding or retrieval on properties of secondary task reaction time (RT) distributions in younger and older adults. Relative to full attention conditions, encoding and retrieval increased secondary task RT medians and standard deviations more for older adults than for younger adults, and the age-related RT increase was most pronounced among the slowest RTs. Hierarchical regression analyses revealed two age-related mechanisms underlying these effects, which were interpreted as cognitive slowing and reductions in attentional resources. Cognitive slowing affects the entire RT distribution regardless of the memory task. By contrast, reduced attentional resources result in very long RTs, especially when the tasks require self-initiated encoding or retrieval operations.     

The Effect of Education on Age-Related Functional Activation During Working Memory

Education has been suggested to play a protective role against the development of age-related dementias. Accordingly, we examined modulation of functional activation during working memory by age and education. Eight older individuals with a college education, six older individuals with a high school education, and eight younger individuals with a college education performed a working memory task during O¹⁵ [water] PET scanning. In a voxel-by-voxel whole brain search, older participants with less education demonstrated greater left frontal activation relative to older participants with more education. Older participants with more education demonstrated greater right precuneus activation relative to older participants with less education. This suggests that older less educated participants may have used additional frontal resources to compensate for dysfunctional parietal cortex. These results occurred in the context of similar activation in well-educated younger and older participants. Younger participants had one unique area of activation in the left posterior parietal cortex and no differences in frontal activation were observed between these two groups. The results of this study indicate the need to consider education in age-related neuroimaging studies.     

Olfactory–Visual Congruence Effects Stable Across Ages: Yellow Is Warmer When It Is Pleasantly Lemony

This study aimed to examine the age-related differences in the olfactory–visual cross-correspondences and the extent to which they are moderated by the odors pleasantness. Sixty participants aged from 20- to 75- years (young, middle-aged and older adults) performed a priming task to explore the influence of six olfactory primes (lemon, orange, rose, thyme, mint and fish) on the categorization (cool vs. warm) of six subsequent color targets (yellow, orange, pink, malachite green, grass-green, and blue-gray). We tested mixed effects models. Response times were regressed on covariates models using both fixed effects (Groups of age, olfactory Pleasantness and multimodal Condition) and cross-random effects (Subject, Color and Odor). The random effects coding for Odor (p < .001) and Color (p = .001) were significant. There was a significant interaction effect ( p= .004) between Condition × Pleasantness, but not with Groups of age. The compatibility effect (i.e., when odors and colors were congruent, the targets processing were facilitated) was as much enhanced as the olfactory primes were pleasant. Cross-correspondences between olfaction and vision may be robust in aging. They should be considered alongside spatiotemporal but also emotional congruency.     

Age-related changes in brain–behaviour relationships: Evidence from event-related functional MRI studies

A fundamental aim of studies in neurocognitive ageing is to understand age-related changes in brain–behaviour relationships. Neuroimaging techniques such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) can be used for observation of these age-related changes only if the assumption of age-equivalent relations between neural activity and haemodynamic activity is valid. In one study, we characterised age-related differences in the coupling of the haemodynamic response to neural activity and found greater voxel-wise noise in older than in younger adults, but age-equivalent signal magnitude. These results suggested that alternative techniques may be necessary for analysing age-related differences in neuroimaging data. In a second study, we utilised one alternative method for comparing fMRI activation between younger and older adults performing a working memory (WM) task. Across three experiments, the results suggested that age-related functional changes in fMRI activation can be isolated to dorsolateral prefrontal cortex (PFC) during memory retrieval. These results suggest a plausible model for WM decline with normal ageing. In a third study we propose and test a model of age-related PFC dysfunction that may account for these and other age-related differences in cognitive performance.     

Differential effects of age on item and associative measures of memory: a meta-analysis

In this meta-analysis, the authors evaluated recent suggestions that older adults' episodic memory impairments are partially due to a reduced ability to encode and retrieve associated/bound units of information. Results of 90 studies of episodic memory for both item and associative information in 3,197 young and 3,192 older adults provided support for the age-related associative/binding deficit suggestion, indicating a larger effect of age on memory for associative information than for item information. Moderators assessed included the type of associations, encoding instructions, materials, and test format. Results indicated an age-related associative deficit in memory for source, context, temporal order, spatial location, and item pairings, in both verbal and nonverbal material. An age-related associative deficit was quite pronounced under intentional learning instructions but was not clearly evident under incidental learning instructions. Finally, test format was also found to moderate the associative deficit, with older adults showing an associative/binding deficit when item memory was evaluated via recognition tests but not when item memory was evaluated via recall tests, in which case the age-related deficits were similar for item and associative information.     

Decision-making competence in younger and older adults: which cognitive abilities contribute to the application of decision rules?

Older adults perform worse than younger adults when applying decision rules to choose between options that vary along multiple attributes. Although previous studies have shown that general fluid cognitive abilities contribute to the accurate application of decision rules, relatively little is known about which specific cognitive abilities play the most important role. We examined the independent roles of working memory, verbal fluency, semantic knowledge, and components of executive functioning. We found that age-related decline in applying decision rules was statistically mediated by age-related decline in working memory and verbal fluency. Our results have implications for theories of aging and decision-making.     

The role of regional heterogeneity in age-related differences in functional hemispheric asymmetry: an fMRI study

Neuroimaging literature has documented age-related hemispheric asymmetry reduction in frontal regions during task performances. As most studies employed working memory paradigms, it is therefore less clear if this pattern of neural reorganization is constrained by working memory processes or it would also emerge in other cognitive domains which are predominantly lateralized. Using blocked functional magnetic resonance imaging (fMRI), the present study used a homophone judgment task and a line judgment task to investigate age-related differences in functional hemispheric asymmetry in language and visuospatial processing respectively. Young and older adults achieved similar task accuracy although older adults required a significantly longer time. Age-related functional hemispheric asymmetry reduction was found only in dorsal inferior frontal gyrus and was associated with better performance when the homophone condition was contrasted against fixation, and not line condition. Our data thus highlights the importance of considering regional heterogeneity of aging effects together with general age-related cognitive processes.     

情景记忆成功年老化的神经机制

随着年龄的增长, 大部分老年人的情景记忆会出现衰退, 但也会有一部分老年人的情景记忆表现出成功的年老化, 即记忆成绩较好或随增龄的衰退程度较小。脑保持理论、神经去分化理论、认知储备理论以及神经补偿理论分别从不同角度解释了情景记忆成功年老化的神经机制。基于选择性优化与补偿模型对现有理论进行整合, 发现情景记忆成功年老化可能与个体的认知储备水平直接相关：高认知储备的老年人能够对情景记忆相关的脑区和脑网络进行优化且具备更强的神经补偿能力, 因而其脑功能(比如, 神经表征和神经加工通路的特异性)可能会保持地更好。未来研究需要更多地采用纵向设计来考察各理论之间的关系及其影响因素, 从而更好地解释记忆成功年老化的神经机制并为提升老年人的脑与认知健康提供支持。     

Age-related deficits in face recognition are related to underlying changes in scanning behavior

Previous studies demonstrating age-related impairments in recognition memory for faces are suggestive of underlying differences in face processing. To study these differences, we monitored eye movements while younger and older adults viewed younger and older faces. Compared to the younger group, older adults showed increased sampling of facial features, and more transitions. However, their scanning behavior was most similar to the younger group when looking at older faces. Moreover, while older adults exhibited worse recognition memory than younger adults overall, their memory was more accurate for older faces. These findings suggest that age-related differences in recognition memory for faces may be related to changes in scanning behavior, and that older adults may use social group status as a compensatory processing strategy.     

Neurocognitive ageing of storage and executive processes

Converging behavioural and neuropsychological evidence indicates that age-related changes in working memory contribute substantially to cognitive decline in older adults. Important questions remain about the relationship between working memory storage and executive components and how they are affected by the normal ageing process. In several studies using positron emission tomography (PET), we find age differences in the patterns of frontal activation during working memory tasks. We find that separable age differences can be linked to different cognitive operations underlying short-term information storage, and interference resolution. Some operations are associated with age-related increases in activation, with older adults displaying bilateral activations and recruiting prefrontal areas more than younger adults. Other operations are associated with age-related decreases in activation. We consider the implications of these results for understanding the working memory system and potential compensatory processes in the ageing brain.     

The effects of attention on age-related relational memory deficits: evidence from a novel attentional manipulation

Healthy aging is often accompanied by episodic memory decline. Prior studies have consistently demonstrated that older adults show disproportionate deficits in relational memory (RM) relative to item memory (IM). Despite rich evidence of an age-related RM deficit, the source of this deficit remains unspecified. One of the most widely investigated factors of age-related RM impairment is a reduction in attentional resources. However, no prior studies have demonstrated that reduced attentional resources are the critical source of age-related RM deficits. Here, we used qualitatively different attention tasks and tested whether reduced attention for relational processing underlies the RM deficit observed in aging. In Experiment 1, we imposed either item-detection or relation-detection attention tasks on young adults during episodic memory encoding and found that only the concurrent attention task that involves relational processing disproportionately impaired RM performance in young adults. Moreover, by ruling out the possible confound of task difficulty on the disproportionate RM impairment, we further demonstrated that reduced relational attention is a key factor for the age-related RM deficit. In Experiment 2, we replicated the results from Experiment 1 by using different materials of stimuli and found that the effect of relational attention on RM is material general. The results of Experiment 2 also showed that reducing attentional resources for relational processing in young adults strikingly equated their RM performance to that of older adults. Thus, this study documents the first evidence that reduced attentional resources for relational processing are a critical factor for the relational memory impairment observed in aging.