Influence of memory strategies on memory test performance: A study in healthy and pathological aging

ABSTRACT

The ability to generate memory strategies is a key factor in the performance of episodic memory tasks. Whether the ability to generate memory strategies exerts an influence in the performance of memory tests in the elderly population is still a matter of debate. Here we present results from an experimental memory task (Test of Memory Strategies, TMS), comprised of five lists of words starting from an incidental learning task, and four more lists which progressively gain in their external organization of the material, reducing the necessity of mobilizing complex memory strategies. TMS has been applied to four groups of elderly patients (amnestic Mild Cognitive Impairment – aMCI, multidomain (mMCI), and Vascular Cognitive Impairment – VCI and Depression) and a healthy aging group. In conditions with low organization of the material, the mMCI and VCI groups (both showing a greater executive function impairment) have shown lower performance. However, as the material was progressively organized, they improved their performance. The aMCI group showed similar performance to the control group at the lower level of external organization but did not improve performance in conditions with a high level of external organization. The mMCI and VCI groups showed lower performance on all TMS conditions compared with controls. Discriminant analysis revealed 90% sensitivity and specificity to differentiate between groups based on TMS conditions. These results indicate how executive functions influence performance on memory tasks in elderly subjects with different neuropsychological profiles.     

Gesturing helps memory encoding in aMCI

Encoding in episodic memory is a step often impaired in patients with amnestic Mild Cognitive Impairment (aMCI). However, procedural memory processes are still relatively preserved. In line with previous research on the enactment effect, we investigated the potential benefit of encoding words combined with imitative gestures on episodic memory. Based on the Grober and Buschke’s free/cued recall procedure, we developed the Symbiosis test in which 13 patients with aMCI and 16 healthy elderly participants learned 32 words belonging to 16 different semantic categories either in a verbal encoding (A) or a bimodal (B; verbal and motor imitation) condition, using a blocked ABBA/BAAB procedure. Overall, memory retrieval was better in healthy participants than in patients with aMCI, and better for cued retrieval in the bimodal encoding (gesture cues) than the verbal encoding (category cues) condition, but there was no interaction effect between group and encoding conditions. These results show that performing concomitant gestures can enhance cued episodic memory retrieval in patients with aMCI and in healthy elderly controls. The Symbiosis test broadens the scope of the enactment effect, from action phrases to isolated words learning in patients with aMCI. Future work should investigate how bimodal encoding provides novel perspectives for memory rehabilitation in patients with aMCI.     

Knowledge and use of memory strategies in amnestic mild cognitive impairment

Despite the inclusion of memory strategy training in many interventions for amnestic mild cognitive impairment (aMCI), little research has directly examined knowledge and use of memory strategies in aMCI and their relationship to memory performance in order to guide the development of targeted interventions. The present study aimed to compare strategy knowledge and use between an aMCI and a healthy older adult (HOA) sample, and to determine the contribution of strategy knowledge and use to memory performance in each of these groups. The sample comprised 37 aMCI and 52 HOA participants aged over 60 years. All participants completed questionnaires to assess strategy knowledge and self-reported use of internal and external strategies in everyday life. In addition, strategy use was observed on the measures of retrospective and prospective memory performance (the CVLT-II and the CAMPROMPT). The aMCI group demonstrated decreased strategy knowledge and observed use of internal strategies, although equivalent observed use of external strategies compared with the HOA group. Furthermore, they reported equivalent use of both internal and external strategies. Observed use of strategies was significantly associated with retrospective memory performance for both groups and prospective memory performance for the aMCI group, supporting the inclusion of strategy training in interventions.     

Memory awareness disruptions in amnestic mild cognitive impairment: comparison of multiple awareness types for verbal and visuospatial material

Successful memory is normally accompanied by explicit awareness of retrieval and confidence in the accuracy of the retrieval product. Prior findings suggest that these features of metamemory can be dissociated from retrieval accuracy in Amnestic Mild Cognitive Impairment (aMCI). However, the literature on this question contains variable and conflicting results, likely because of differences in experimental conditions. We sought to systematically evaluate memory awareness disruptions in aMCI using multiple measures and stimulus formats within the same individuals. Memory awareness was tested with global predictions and postdictions, judgments of learning, confidence level ratings, and modified feeling-of-knowing ratings in tasks of visuospatial and verbal memory. These tests were administered to 14 individuals with aMCI and 15 healthy, age-matched controls. Memory awareness accuracy was calculated as the correspondence between subjective judgments and memory performance.Individuals with aMCI demonstrated impaired global and trial-level retrospective task awareness for visuospatial and verbal stimuli. Additionally, modified feeling-of-knowing awareness was impaired selectively for verbal stimuli. Statistical effect sizes for global awareness impairments were comparable to impairments in several objective neuropsychological memory assessments.Memory awareness (metamemory) disruptions in aMCI were most evident for a subset of subjective judgment types and task input modalities. These findings advance understanding of the nature of memory impairments in aMCI and support the utility of incorporating memory awareness testing to better characterize memory integrity in older adults.     

Investigating virtual reality navigation in amnestic mild cognitive impairment using fMRI

Spatial navigation requires a well-established network of brain regions, including the hippocampus, caudate nucleus, and retrosplenial cortex. Amnestic Mild Cognitive Impairment (aMCI) is a condition with predominantly memory impairment, conferring a high predictive risk factor for dementia. aMCI is associated with hippocampal atrophy and subtle deficits in spatial navigation. We present the first use of a functional Magnetic Resonance Imaging (fMRI) navigation task in aMCI, using a virtual reality analog of the Radial Arm Maze. Compared with controls, aMCI patients showed reduced activity in the hippocampus bilaterally, retrosplenial cortex, and left dorsolateral prefrontal cortex. Reduced activation in key areas for successful navigation, as well as additional regions, was found alongside relatively normal task performance. Results also revealed increased activity in the right dorsolateral prefrontal cortex in aMCI patients, which may reflect compensation for reduced activations elsewhere. These data support suggestions that fMRI spatial navigation tasks may be useful for staging of progression in MCI.     

Movements execution in amnestic mild cognitive impairment and Alzheimer's disease

We evaluated the relationship between motor and neuropsychological deficits in subjects affected by amnestic Mild Cognitive Impairment (aMCI) and early Alzheimer's Disease (AD). Kinematics of goal-directed movement of aMCI and AD subjects were compared to those of age-matched control subjects. AD showed a slowing down of motor performance compared to aMCI and controls. No relationships were found between motor and cognitive performances in both AD and aMCI. Our results suggest that the different motor behaviour between AD and aMCI cannot be related to memory deficits, probably reflecting the initial degeneration of parietal-frontal circuits for movement planning. The onset of motor dysfunction in early AD could represent the transition from aMCI to AD.     

Increased sensitivity to proactive interference in amnestic mild cognitive impairment is independent of associative and semantic impairment

Episodic memory deficit is the hallmark of amnestic mild cognitive impairment (aMCI). There is, however, an overlap in performance among patients with aMCI and elderly controls (EC). The memory deficit in aMCI therefore needs to be better characterized. Studies have shown that associative memory is selectively impaired in aMCI, and recent work suggested that aMCI may be hypersensitive to semantic proactive interference (PI). It is not known whether this increased PI is related to associative or semantic impairment. EC (n = 44) and patients with aMCI (n = 30) performed two tasks presenting a gradually increasing PI effect across four lists. One task used semantic cueing, the other phonological cueing. We controlled for associative memory by introducing it as a covariate and by matching our subjects for it. Patients with aMCI had a greater PI effect than EC matched for associative memory, regardless of the type of cueing. The increased PI effect in patients with aMCI is independent of their associative and semantic impairment.     

Insights into spared memory capacity in amnestic MCI and Alzheimer's Disease via minimal interference

Impairment on standard tests of delayed recall is often already maximal in the aMCI stage of Alzheimer's Disease. Neuropathological work shows that the neural substrates of memory function continue to deteriorate throughout the progression of the disease, hinting that further changes in memory performance could be tracked by a more sensitive test of delayed recall. Recent work shows that retention in aMCI patients can be raised well above floor when the delay period is devoid of further material - 'Minimal Interference'. This memory enhancement is thought to be the result of improved memory consolidation. Here we used the minimal interference/interference paradigm (word list retention following 10 min of quiet resting vs. picture naming) in a group of 17 AD patients, 25 aMCI patients and 25 controls. We found (1) that retention can be improved significantly by minimal interference in patients with aMCI and patients with mild to moderate AD; (2) that the minimal interference paradigm is sensitive to decline in memory function with disease severity, even when performance on standard tests has reached floor; and (3) that this paradigm can differentiate well (80% sensitivity and 100% specificity) between aMCI patients who progress and do not progress to AD within 2 years. Our findings support the notion that the early memory dysfunction in AD is associated with an increased susceptibility to memory interference and are suggestive of a gradual decline in consolidation capacity with disease progression.     

Relationship of cognitive strategy use to prospective memory performance in a diverse sample of nondemented older adults with varying degrees of cognitive complaints and impairment

Although older adults typically have better performance on prospective memory (PM) tasks carried out in naturalistic settings, a paucity of research directly assesses older adults’ use of compensatory strategies on such tasks. The current study investigates external memory strategy use during performance of a clinical PM test that features both short-term (in laboratory) and long-term (out of laboratory) subtasks (i.e., the Royal Prince Alfred Prospective Memory Test – RPA-ProMem. Nondemented, community-dwelling older adults (n = 214; mean age = 80.5; 68.2% female; 39.7% non-white) with mild cognitive impairment, subjective cognitive decline, and healthy controls completed the RPA-ProMem while external strategy use was permitted and recorded. Overall, participants utilized external strategies 41% of the time on the RPA-ProMem. Increased utilization of external memory strategies was significantly associated with better PM performance. Additionally, better performance on executive functioning tasks was associated with increased use of external memory strategies. Results are discussed in relation to how memory strategy use can be enhanced to improve everyday memory ability in older adults at risk for dementia.     

Alterations in working memory networks in amnestic mild cognitive impairment

Patients with amnestic mild cognitive impairment (aMCI) show preserved or mildly impaired working memory, despite their deficits in episodic memory. We aimed to identify performance and/or neural differences between aMCI patients and matched controls on a standard working memory fMRI task. Neuropsychological assessment demonstrated aMCI impairments in verbal and visual episodic long-term memory, with intact IQ and executive function. Participants completed a standard three-level N-back task where patients were unimpaired. Functional activations in the control group were found in expected areas, including the inferior parietal lobule and dorsolateral prefrontal cortex. Group differences were found in the insula and lingual gyrus and, in a region of interest analysis, in the hippocampus. In all cases, these were caused by an absence of task-related deactivations in the aMCI group. The results are consistent with reports of failure in task-related deacivations in aMCI and could be early indications of pathology.     

Working memory and the control of action: evidence from task switching.

A series of 7 experiments used dual-task methodology to investigate the role of working memory in the operation of a simple action-control plan or program involving regular switching between addition and subtraction. Lists requiring switching were slower than blocked lists and showed 2 concurrent task effects. Demanding executive tasks impaired performance on both blocked and switched lists, whereas articulatory suppression impaired principally the switched condition. Implications for models of task switching and working memory and for the Vygotskian concept of verbal control of action are discussed.     

Central executive involvement in children's spatial memory

Previous research with adults found that spatial short-term and working memory tasks impose similar demands on executive resources. We administered spatial short-term and working memory tasks to 8- and 11-year-olds in three separate experiments. In Experiments 1 and 2 an executive suppression task (random number generation) was found to impair performances on a short-term memory task (Corsi blocks), a working memory task (letter rotation), and a spatial visualisation task (paper folding). In Experiment 3 an articulatory suppression task only impaired performance on the working memory task. These results suggest that short-term and working memory performances are dependent on executive resources. The degree to which the short-term memory task was dependent on executive resources was expected to be related to the amount of experience children have had with such tasks. Yet we found no significant age-related suppression effects. This was attributed to differences in employment of cognitive strategies by the older children.     

Explicit and implicit memory in dementia and normal ageing

Summary In two experiments, young subjects, healthy elderly subjects (spouses), and highly intelligent elderly subjects (elite elderly), were compared with dementia patients in a variety of explicit and implicit memory tasks, to investigate two issues: whether priming in Alzheimer-type dementia is contingent upon the presence of pre-existing representations, and whether intelligence modulates performance in explicit memory tasks in healthy ageing. Dementia patients performed as well as spouses in a homophone-spelling task. Moreover, they established new contextual associations when memory was tested by word-stem completion. The hypothesis that priming in dementia is contingent upon pre-existing memory representations was not supported. Spouses, elite elderly, and young subjects did not differ in their ability to recognize correctly recently heard stimuli or to complete word stems. However, recall of lists of words and paired associates was better in both young and elite elderly subjects than in spouses. It is concluded that intellectual capacity rather than chronological age in healthy subjects modulates performance in explicit-memory tasks.Now at The Social Psychiatry Unit, Australian National University, Canberra, ACT, Australia     

Central executive involvement in children's spatial memory

Previous research with adults found that spatial short-term and working memory tasks impose similar demands on executive resources. We administered spatial short-term and working memory tasks to 8- and 11-year-olds in three separate experiments. In Experiments 1 and 2 an executive suppression task (random number generation) was found to impair performances on a short-term memory task (Corsi blocks), a working memory task (letter rotation), and a spatial visualisation task (paper folding). In Experiment 3 an articulatory suppression task only impaired performance on the working memory task. These results suggest that short-term and working memory performances are dependent on executive resources. The degree to which the short-term memory task was dependent on executive resources was expected to be related to the amount of experience children have had with such tasks. Yet we found no significant age-related suppression effects. This was attributed to differences in employment of cognitive strategies by the older children.     

Aging and self-reported internal and external memory strategy uses: The role of executive functioning

The aim of this study was to investigate the effect of advanced age on self-reported internal and external memory strategy uses, and whether this effect can be predicted by executive functioning. A sample of 194 participants aged 21 to 80 divided into three age groups (21-40, 41-60, 61-80) completed the two strategy scales of the Metamemory in Adulthood (MIA) questionnaire, differentiating between internal and external everyday memory strategy uses, and three tests of executive functioning. The results showed that: (1) the use of external memory strategies increased with age, whereas use of internal memory strategy decreased; (2) executive functioning appeared to be related only to internal strategies, the participants who reported the greatest use of internal strategies having the highest executive level; and (3) executive functioning accounted for a sizeable proportion of the age-related variance in internal strategy use. These findings suggest that older adults preferentially use external memory strategies to cope with everyday memory impairment due to aging. They also support the view that the age-related decrease in the implementation of internal memory strategies can be explained by the executive hypothesis of cognitive aging. This result parallels those observed using objective laboratory memory strategy measures and then supports the validity of self-reported memory strategy questionnaire.     

Central executive function in mild cognitive impairment: a PET activation study

Using positron emission tomography (PET), we explored the neural correlates of an executive function, dual tasking, in patients with amnestic mild cognitive impairment (aMCI) and in elderly controls. The experiment employed simple auditory and visual tasks that were presented both in isolation and simultaneously to create a task condition requiring enhanced attentional control. Behaviorally, both groups performed well, albeit the patients made more errors on the visual task. The PET analysis focused at prefrontal regions where group differences in task-related activation patterns were expected. During dual task performance, the patients showed attenuated activity in the left inferior frontal region when compared to the controls. This suggests abnormalities in the neural processes underlying attentional control in aMCI.     

日常前瞻记忆的年龄差异

在年龄—前瞻记忆悖论现象中,老年人在完成日常前瞻记忆任务时,其表现优于年轻人的现象尤其引人注意。研究者一方面探讨了动机水平、责任心、生活状态以及外部帮助与提示等与主体有关的因素等对这一结果的影响;另一方面也研究了任务本身因素的影响,根据不同任务情境和任务性质的前瞻记忆年龄比较的结果,可以推断日常前瞻记忆年龄差异的来源在于任务的性质而非任务的情境。将来的研究可通过元分析、中介效应检验等手段进一步确定日常前瞻记忆年龄差异的机制。     

Acute pain disrupts prospective memory cue detection processes

Prospective memory refers to the planning, retention, retrieval, and execution of intentions for future behaviours and it is integral to the enterprise of daily living. Although prospective memory relies upon retrospective memory and executive processes often disrupted by pain, limited research has explored the influence of acute or chronic pain on the ability to complete prospective memory tasks. In the present study we investigated the influence of acute pain on prospective memory tasks that varied in their demands on executive processes (i.e., non-focal versus focal prospective memory cues). Complex-span working memory tasks were also administered to examine whether individual differences in working memory capacity moderated any negative impact of pain on prospective memory. Acute pain significantly impaired prospective memory performance in conditions that encouraged non-focal strategic processing of prospective memory cues, but not in conditions that encouraged more spontaneous focal processing. Individual differences in working memory capacity did not moderate the effect of acute pain on non-focal prospective memory. These findings provide new insights into prospective memory dysfunction created by painful experiences.     

A modality congruency effect in verbal false memory

The involvement of working memory sub-systems in syllogistic reasoning problems was assessed by dual task methods. Effects of skill level and training on working memory involvement in syllogistic reasoning were examined. In Study 1, participants were pre-selected into groups of High and Low skill at syllogistic reasoning on the basis of a pencil-and-paper screening test. Six separate High and Low skill groups completed syllogistic reasoning tasks in control conditions and each group was also tested under one of the following six dual task conditions: articulatory suppression, unattended speech, verbal random generation, spatial random generation, tapping in a simple pattern, unattended pictures. The results indicated that the more skilled participants were generally following a high demand strategy, which loaded the central executive, phonological loop and imagery sub-systems, but that lower skill participants were generally following a less demanding strategy which did not load working memory components so heavily. In two Pilot Studies a training procedure was assessed and validated. In Study 2, participants were selected, on the basis of a screening test, as being unskilled at solving syllogisms but as performing above guessing level. These participants underwent the training regime validated in the Pilot Studies. Following training, separate groups of participants carried out syllogistic tests with and without one of the following four secondary tasks: articulatory suppression, unattended pictures, spatial random generation, and verbal random generation. The pattern of results indicated that training had induced high demand strategies (often logic-equivalent), which loaded the central executive and to a lesser extent the phonological loop.     

Short-term memory performances during sustained wakefulness in patients with obstructive sleep apnea-hypopnea syndrome

Both working and immediate memories were assessed every 4h by specific short-term memory tasks over sustained wakefulness in 12 patients with obstructive sleep apnea and hypopnea syndrome (OSAHS) and 10 healthy controls. Results indicated that OSAHS patients exhibited lower working memory performances than controls on both backward digit span and complex Sternberg tasks. Speed and accuracy on Sternberg tasks were affected by memory load in both groups. However, immediate memory was not impaired in OSAHS patients. Diurnal and nocturnal SaO(2) were correlated with speed and accuracy high-speed memory scanning performance on Sternberg tasks in patients. These results suggest specific working memory deficits associated with OSAHS over sustained wakefulness with a possible deficiency in the central executive responsible for the higher information processing, in addition to a potentially insufficient storage capacity. Among OSAHS patients, working memory ability involved in high-speed memory scanning may be impaired by chronic hypoxemia.