Preserved priming but insensitivity to perceptual fluency on recognition judgments in Alzheimer's disease

Background: Previous research on Alzheimer's disease (AD) has not yielded a consensus regarding the preservation of automatic memory processes, although there is a consensus that conscious recollection processes are impaired in AD. Methods: In the present study, we examined perceptual specificity effects (PSEs) in word recognition judgments (explicit memory task; Experiment 1) and word fragment completion (implicit memory task; Experiment 2) performed by individuals with mild AD and elderly adults without dementia (controls). Results: In recognition judgments, control subjects, but not individuals with AD, demonstrated PSEs (Experiment 1). In contrast, neither group showed PSEs on word fragment completion and their priming magnitudes were comparable (Experiment 2). Conclusions: The findings suggest that perceptually automatic processes in explicit memory judgments and implicit memory processes are different and that the former are specifically impaired in AD.     

Successive memory test performance and priming in Alzheimer's disease: evidence from the word-fragment completion task

This study assessed the performance of patients with Alzheimer's disease and healthy controls in a successive memory test paradigm. Subjects studied lists of words. Following study, tests of recognition (an explicit memory task) and primed word fragment completion (an implicit memory task) were administered. Since the same words were used in the two tasks, we were able to calculate the degree of dependence between recognition performance and primed word fragment completion. AD patients evidenced impaired recognition memory. In contrast, priming was intact. The pattern of correlation between the two tasks was similar in healthy controls and in AD. Independence between recognition and fragment completion was obtained when recognition preceded the fragment completion task, but not when fragment completion preceded recognition.     

Emotional enhancement of perceptual priming is preserved in aging and early-stage Alzheimer's disease

Perceptual priming for emotionally-negative and neutral scenes was tested in early-stage Alzheimer's disease (AD) patients and healthy younger, middle-aged and older adults. In the study phase, participants rated the scenes for their arousal properties. In the test phase, studied and novel scenes were initially presented subliminally, and the exposure duration was gradually increased until a valence categorization was made. The difference in exposure duration required to categorize novel versus studied items was the dependent measure of priming. Aversive content increased the magnitude of priming, an effect that was preserved in healthy aging and AD. Results from an immediate recognition memory test showed that the priming effects could not be attributable to enhanced explicit memory for the aversive scenes. These findings implicate a dissociation between the modulatory effect of emotion across implicit and explicit forms of memory in aging and early-stage AD.     

Preserved conceptual priming in Alzheimer's disease

We assessed Alzheimer's disease (AD) and healthy older adult control (HC) group performance on: (1) a conceptual priming task, in which participants had to make a semantic decision as to whether a degraded picture of an object encountered previously belonged to the category of living or non-living things; and (2) a recognition memory task. The AD group showed a dissociation between impaired performance on the recognition task and preserved priming for semantic decisions to degraded pictures. We argue that it is not whether priming is conceptual or perceptual that is important for the observation of priming in AD, rather it is the nature of the response that is required (c.f., Gabrieli et al., 1999).     

Implicit and explicit memory in Alzheimer's disease and Parkinson's disease

Several tasks examined implicit and explicit memory in demographically matched samples of Alzheimer's (AD) and Parkinson's disease (PD) patients, and healthy elderly subjects. A fragmented pictures test, word stem-completion repetition priming, and a pursuit-rotor tracking task, followed by explicit memory tests, were given. AD patients were impaired on all explicit tests and on word stem-completion priming, but were intact on pursuit-rotor tracking and the skill learning (SL) component of the fragmented pictures test. PD patients were significantly better than AD patients on all explicit memory tests, but were selectively impaired on the SL component of the fragmented pictures test. Finally, a mirror-reading test was given to the PD patients and control subjects, with no significant differences found in performances between the two groups. Results are discussed in terms of hypothetical cognitive processes and brain circuits underlying different implicit and explicit memory domains.     

Priming performance in Alzheimer's disease: the role of task sensitivity.

Studies examining implicit memory performance in Alzheimer's disease (AD) have yielded inconsistent findings, with these patients demonstrating impaired performance within some priming studies and intact performance within others. The present study examined the role of task sensitivity in detecting impaired priming in memory-impaired patients. Twelve healthy older adults and 12 AD patients were administered a picture fragment identification test. Task sensitivity was increased by employing stimulus cues expected to produce larger and more variable priming effects than obtained in previous studies. A simple comparison of priming scores revealed that the AD patients demonstrated significantly impaired priming relative to normal control participants. However, further analysis of priming in relation to certain stimulus characteristics revealed that AD patients often demonstrated impaired priming when overall priming effects were large but relatively intact priming when priming effects were small. These findings suggest that the prevention of ceiling effects in control participants may aid in the detection of impaired priming in patient populations.     

Memory for the September 11, 2001, terrorist attacks one year later in patients with Alzheimer's disease, patients with mild cognitive impairment, and healthy older adults

Although there are many opportunities to study memory in patients with Alzheimer's disease (AD) in the laboratory, there are few opportunities to study memory for real world events in these patients. The September 11, 2001 terrorist attacks provided one such opportunity. Patients with AD, patients with mild cognitive impairment (MCI), and healthy older adults were given a telephone questionnaire in the initial weeks after the event, again three to four months later, and finally one year afterwards to evaluate their memory for the September 11, 2001 terrorist attacks. We were particularly interested in using the attacks as an opportunity to examine the decline of episodic memory in patients with AD, patients with MCI, and older adult controls over a period of months. We found that compared to healthy older adults, patients with AD and MCI showed impaired memory at the initial time point, more rapid forgetting from the initial to the three-month time point, and very similar changes in memory from the three-month to the one-year time point. We speculated that these findings were consistent with patients with AD and MCI showing initial impaired encoding and a more rapid rate of forgetting compared with healthy older adults, but that once the memories had been consolidated, their decay rate became similar to that of healthy older adults. Lastly, although memory distortions were common among all groups, they were greatest in the patients with AD.     

Implicit, explicit, and semantic memory functions in Alzheimer's disease and Huntington's disease.

A priming task involving a word-stem completion paradigm was administered to patients with Alzheimer's disease (AD), patients with Huntington's disease (HD), and normal control subjects. The task was done under conditions of both implicit and explicit recall. Explicit and implicit recall were positively correlated in all three groups. After controlling for explicit recall ability through ANCOVA, AD patients were found to be normally susceptible to the effects of priming on implicit recall. HD patients, however, exhibited significantly increased susceptibility to priming, suggesting that they may have carried out the implicit task in a manner different from that of normals and AD patients. In a second experiment, AD patients were found to supply words of significantly lower association strength than the other two groups in a "free association" task using words from a published list of word association norms. This apparent degradation of semantic memory was found to be strongly correlated with explicit recall performance, suggesting that explicit, implicit, and semantic memory functions decline in parallel in AD. Results are discussed with respect to the difficulties inherent in attempts to demonstrate selective impairments of conceptually distinct forms of memory.     

The underlying mechanisms of semantic memory loss in Alzheimer's disease and semantic dementia

Patients with Alzheimer's disease (AD) and patients with semantic dementia (SD) both exhibit deficits on explicit tasks of semantic memory such as picture naming and category fluency. These deficits have been attributed to a degradation of the stored semantic network. An alternative explanation attributes the semantic deficit in AD to an impaired ability to consciously retrieve items from the semantic network. The present study used an implicit lexical-decision priming task to examine the integrity of the underlying semantic network in AD and SD patients matched for degree of impairment on explicit semantic memory tasks. The AD (n=11) and SD (n=11) patient groups were matched for age, education, level of dementia and impairment on four explicit semantic memory tasks. Healthy elderly participants (n=22) were matched for age and education. Semantic priming effects were evaluated for three types of semantic relationships (attributes, category coordinates, and category superordinates) and compared to lexical associative priming. Healthy controls showed significant priming across all conditions. In contrast, AD patients showed normal superordinate priming, and significant (although somewhat reduced) coordinate priming, but no attribute priming. SD patients showed no priming effect for any semantic relationship. All groups showed significant associative priming. The results indicate that SD patients do indeed have substantial degradation of semantic memory, while AD patients have a partially intact network, accounting for priming in superordinate and coordinate conditions. These findings suggest that AD patients' impairment on explicit semantic tasks is the product of deficient explicit retrieval in combination with a partially degraded semantic network.     

Alzheimer's disease and memory-monitoring impairment: Alzheimer's patients show a monitoring deficit that is greater than their accuracy deficit

We assessed the ability of two groups of patients with mild Alzheimer's disease (AD) and two groups of older adults to monitor the likely accuracy of recognition judgments and source identification judgments about who spoke something earlier. Alzheimer's patients showed worse performance on both memory judgments and were less able to monitor with confidence ratings the likely accuracy of both kinds of memory judgments, as compared to a group of older adults who experienced the identical study and test conditions. Critically, however, when memory performance was made comparable between the AD patients and the older adults (e.g., by giving AD patients extra exposures to the study materials), AD patients were still greatly impaired at monitoring the likely accuracy of their recognition and source judgments. This result indicates that the monitoring impairment in AD patients is actually worse than their memory impairment, as otherwise there would have been no differences between the two groups in monitoring performance when there were no differences in accuracy. We discuss the brain correlates of this memory-monitoring deficit and also propose a Remembrance-Evaluation model of memory-monitoring.     

Implicit and explicit memory for spatial information in Alzheimer's disease

There is abundant evidence that memory impairment in dementia in patients with Alzheimer's disease (AD) is related to explicit, conscious forms of memory, whereas implicit, unconscious forms of memory function remain relatively intact or are less severely affected. Only a few studies have been performed on spatial memory function in AD, showing that AD patients' explicit spatial memory is impaired, possibly related to hippocampal dysfunction. However, studies on implicit spatial memory in AD are lacking. The current study set out to investigate implicit and explicit spatial memory in AD patients (n=18) using an ecologically valid computer task, in which participants had to remember the locations of various objects in common rooms. The contribution of implicit and explicit memory functions was estimated by means of the process dissociation procedure. The results show that explicit spatial memory is impaired in AD patients compared with a control group (n=21). However, no group difference was found on implicit spatial function. This indicates that spared implicit memory in AD extends to the spatial domain, while the explicit spatial memory function deteriorates. Clinically, this finding might be relevant, in that an intact implicit memory function might be helpful in overcoming problems in explicit processing.     

Memory impairment differs in frontotemporal dementia and Alzheimer's disease

The aim of this study was to assess short-term and long-term explicit memory and implicit memory in frontotemporal dementia (FTD; frontal variant) and to compare FTD and Alzheimer's disease (AD) patients with similar severity of dementia. Fifteen FTD patients [mean age: 68 years; Mini-Mental State (MMS): 24], 30 probable AD patients (mean age: 72 years; MMS: 23) and 12 healthy subjects participated in the study. The three groups were comparable in terms of gender and educational level. Short-term memory was assessed with the digit span and Corsi block-tapping tests. Explicit verbal memory was assessed with the Grober and Buschke test, and implicit memory with a verbal priming task and a fragmented picture test. FTD patients demonstrated a genuine memory deficit with impaired digit span, encoding deficit and retrieval strategy difficulties, but preserved implicit verbal and visual priming. Memory patterns differed in AD and FTD: short-term memory and free recall were similarly decreased in FTD and AD but cues provided more benefit to FTD than to AD; encoding was more impaired and the forgetting rate was faster in AD than in FTD; priming was lower in AD than in FTD. AD patients with clinical and imaging frontal lobe dysfunction tended to have lower memory performance and to differ even more from FTD patients than AD patients without frontal lobe dysfunction.     

Impaired production priming and intact identification priming in Alzheimer's disease.

This study examined the distinction between identification and production processes in repetition priming for 16 patients with Alzheimer's disease (AD) and 16 healthy old control participants (NC). Words were read in three study phases. In three test phases, participants (1) reread studied words, along with unstudied words, in a word-naming task (identification priming); (2) completed 3-letter stems of studied and unstudied words into words in a word-stem completion task (production priming); and (3) answered yes or no to having read studied and unstudied words in a recognition task (explicit memory). Explicit memory and word-stem completion priming were impaired in the AD group compared to the NC group. After correcting for baseline slowing, word-naming priming magnitude did not differ between the groups. The results suggest that the distinction between production and identification processes has promise for explaining the pattern of preservation and failure of repetition priming in AD.     

Normal mere exposure effect with impaired recognition in Alzheimer's disease

We investigated the mere exposure effect and the explicit memory in Alzheimer's disease (AD) patients and elderly control subjects, using unfamiliar faces. During the exposure phase, the subjects estimated the age of briefly flashed faces. The mere exposure effect was examined by presenting pairs of faces (old and new) and asking participants to select the face they liked. The participants were then presented with a forced-choice explicit recognition task. Controls subjects exhibited above-chance preference and recognition scores for old faces. The AD patients also showed the mere exposure effect but no explicit recognition. These results suggest that the processes involved in the mere exposure effect are preserved in AD patients despite their impaired explicit recognition. The results are discussed in terms of Seamon et al.'s (1995) proposal that processes involved in the mere exposure effect are equivalent to those subserving perceptual priming. These processes would depend on extrastriate areas which are relatively preserved in AD patients.     

Implicit and explicit memory in Alzheimer's disease and Parkinson's disease

Abstract

Several tasks examined implicit and explicit memory in demographically matched samples of Alzheimer's (AD) and Parkinson's disease (PD) patients, and healthy elderly subjects. A fragmented pictures test, word stem-completion repetition priming, and a pursuit-rotor tracking task, followed by explicit memory tests, were given. AD patients were impaired on all explicit tests and on word stem-completion priming, but were intact on pursuit-rotor tracking and the skill learning (SL) component of the fragmented pictures test. PD patients were significantly better than AD patients on all explicit memory tests, but were selectively impaired on the SL component of the fragmented pictures test. Finally, a mirror-reading test was given to the PD patients and control subjects, with no significant differences found in performances between the two groups. Results are discussed in terms of hypothetical cognitive processes and brain circuits underlying different implicit and explicit memory domains.     

The effect of semantic orientation at encoding on free-recall performance in amnestic mild cognitive impairment and probable Alzheimer's disease

The present study manipulated the nature of orientation provided at encoding in an intentional word memory task. Performance on the memory task was then compared between 23 elderly persons with amnestic mild cognitive impairment (aMCI), 13 patients with probable Alzheimer's disease (AD), and 23 healthy elderly persons. When tested following shallow (reading orientation) encoding, free-recall performance was impaired in AD compared to aMCI and healthy older adults. When tested following deep (categorical semantic orientation) encoding, both AD and aMCI groups were impaired relative to healthy older adults. The latter result was related to larger memory improvement due to semantic orientation in healthy controls than in aMCI and AD participants. Overall, these findings indicate that the encoding put up by aMCI and healthy elderly persons is comparably efficient in situations where shallow supportive cues are provided at encoding, but that healthy controls benefit more than aMCI and AD in situations where supportive cues are strong.     

Learning and forgetting new names and objects in MCI and AD

We studied how subjects with mild cognitive impairment (MCI), early Alzheimer's disease (AD) and age-matched controls learned and maintained the names of unfamiliar objects that were trained with or without semantic support (object definitions). Naming performance, phonological cueing, incidental learning of the definitions and recognition of the objects were tested during follow-up. We found that word learning was significantly impaired in MCI and AD patients, whereas forgetting patterns were similar across groups. Semantic support showed a beneficial effect on object name retrieval in the MCI group 8 weeks after training, suggesting that the MCI patients’ preserved semantic memory can compensate for impaired episodic memory. The MCI group performed equally well as the controls in the tasks measuring incidental learning and recognition memory, whereas the AD group showed impairment in this respect. Both the MCI and the AD group benefited less from phonological cueing than the controls. Our findings indicate that word learning is compromised in both MCI and AD, whereas long-term retention of newly learned words is not affected to the same extent. Incidental learning and recognition memory seem to be well preserved in MCI.     

Functional changes in brain activity during priming in Alzheimer's disease

Patients with Alzheimer's disease (AD) are often impaired on certain forms of implicit memory, such as word-stem completion priming (WSCP). Lesion data suggest that deficient WSCP may be associated with abnormal functioning in the posterior neocortex. Using positron emission tomography (PET), we here provide direct support for this view. Compared with normal old adults, AD patients showed reduced priming on a word-stem completion task. The normal old showed decreased activity in right occipital cortex (area 19), whereas the AD patients showed increased activity in this region during priming. To the extent that decreased activity during priming reflects an experience-dependent reduction of the neuronal population involved, these results indicate that shaping of the relevant neurons is slower in AD, possibly as a result of inadequate initial stimulus-processing.     

Age effects on brain activity during repetition priming of targets and distracters

The effects of age on repetition priming and how such differences were related to intentional learning and working memory status were examined. Fourteen older (age 65-75) and 14 younger (age 18-28) healthy adults performed a modified delayed match-to-sample task consisting of a target object held in mind followed by nine test objects. Sixty four-channel EEGs were recorded as participants indicated whether each test object was the same or different from the target object. Half of all target and distractor objects were intentionally studied prior to the task, and both target and distractor objects were repeatedly presented up to four times in each trial. Although both age groups showed repetition priming effects, speed increases due to repetition were more enhanced for elderly. ERP repetition effects for both younger and older adults were indexed via early (200-550) and late (550-850 ms) components. The early repetition effect was affected by whether a distractor was previously studied or not for younger but not for older adults. In contrast, the late repetition effect was not affected by prior intentional learning, and a marginal age effect suggested that repetitions of distractors likely affected older and younger adults differently. These findings suggest that at least two distinguishable repetition mechanisms differentially affect adult aging.     

The picture superiority effect in patients with Alzheimer's disease and mild cognitive impairment

The fact that pictures are better remembered than words has been reported in the literature for over 30 years. While this picture superiority effect has been consistently found in healthy young and older adults, no study has directly evaluated the presence of the effect in patients with Alzheimer's disease (AD) or mild cognitive impairment (MCI). Clinical observations have indicated that pictures enhance memory in these patients, suggesting that the picture superiority effect may be intact. However, several studies have reported visual processing impairments in AD and MCI patients which might diminish the picture superiority effect. Using a recognition memory paradigm, we tested memory for pictures versus words in these patients. The results showed that the picture superiority effect is intact, and that these patients showed a similar benefit to healthy controls from studying pictures compared to words. The findings are discussed in terms of visual processing and possible clinical importance.