Neuropsychological evidence for multiple implicit memory systems: a comparison of Alzheimer's, Huntington's, and Parkinson's disease patients

The performances of patients with dementia of the Alzheimer type (DAT), patients with Huntington's disease (HD), and demented and nondemented patients with Parkinson's disease (PD) were compared on 2 tests of implicit memory that do not require the conscious recollection of prior study episodes: (1) a pursuit-rotor motor learning task and (2) a lexical priming test. The HD patients were found to be impaired on the motor learning but not the lexical priming task, whereas the DAT patients evidenced the opposite relationship on these tasks. The demented, but not the nondemented, PD patients were found to be impaired on both tests of implicit memory. For both the HD and PD patients, deficits on the motor learning task correlated significantly with severity of dementia but not with level of primary motor dysfunction. The noted double dissociation between HD and DAT patients indicates that different forms of implicit memory, all of which are intact in amnesia, are dependent upon distinct neuroanatomic systems. Motor skill learning may be mediated by a corticostriatal system, whereas verbal priming may depend upon the integrity of the neocortical association areas involved in the storage of semantic knowledge. The results for the PD patients suggest that the demented PD patients have endured damage to the neurologic systems subserving both motor learning and lexical priming.     

Lexical and semantic priming deficits in patients with Alzheimer's disease

Two experiments utilizing priming procedures examined the status of semantic memory in demented and amnesic patients. In the first investigation, lexical priming was assessed in patients with dementia of the Alzheimer type (DAT), Huntington's Disease (HD), alcoholic Korsakoff's syndrome (KS), and in intact control subjects. Subjects were first exposed to a list of words in a rating task and then required to complete three-letter stems with the "first word that comes to mind". Half of the stems could be completed with the previously presented words and the other half were used to assess baseline guessing rates. Recall and recognition of incidentally exposed words was also assessed. Although all three patient groups were impaired on tests of recall and recognition, only the DAT patients exhibited a priming deficit on the stem-completion task. In the second experiment, DAT, HD, and intact control subjects were administered a semantic priming test which required the subject to "free associate" to the first words of previously presented semantically associated word pairs. The results for this association task showed that DAT patients were significantly less likely to produce the second word of the semantically related pair than were the other subject groups. The results of these two experiments suggest that the memory capacities of DAT patients are characterized by a breakdown in the structure of semantic memory and that this impairment is evident on some "automatic" as well as "effortful" processing tasks.     

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.     

INS Workshop program Antwerp,Belguium July 5, 1989

Abstract

While patients with Huntington's disease (HD) and Korsakoff's syndrome (KS) demonstrate “preserved” performance on implicit word-stem completion tasks, patients with Alzheimer's disease (AD) are typically found to be impaired. It has been hypothesized that AD patients do poorly as a result of degenerative changes in posterior cortoil association areas thought to mediate performance on this type of implicit memory task, and that the relative sparing of these areas in KS and HD results in their “preserved” performance. The present study was undertaken to examine the implicit memory performance of AD patients on this task after equating their explicit performance to that of normal controls by manipulating the number of encoding exposures. When this was accomplished, the implicit memory performance of AD patients was equivalent to that of controls. The results are discussed within the context of a critical review of the evidence for the existence of separable neural systems in mediating implicit and explicit memory.     

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.     

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.     

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.     

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.     

Intact haptic priming in normal aging and Alzheimer's disease: evidence for dissociable memory systems

This study is the first to report complete priming in Alzheimer's disease (AD) patients and older control subjects for objects presented haptically. To investigate possible dissociations between implicit and explicit objects representations, young adults, Alzheimer's patients, and older controls performed a speeded object naming task followed by a recognition task. Similar haptic priming was exhibited by the three groups, although young adults responded faster than the two older groups. Furthermore, there was no difference in performance between the two healthy groups. On the other hand, younger and older healthy adults did not differ on explicit recognition while, as expected, AD patients were highly impaired. The double dissociation suggests that different memory systems mediate both types of memory tasks. The preservation of intact haptic priming in AD provides strong support to the idea that object implicit memory is mediated by a memory system that is different from the medial-temporal diencephalic system underlying explicit memory, which is impaired early in AD. Recent imaging and behavioral studies suggest that the implicit memory system may depend on extrastriate areas of the occipital cortex although somatosensory cortical mechanisms may also be involved.     

Long-term retention of implicit learning in Huntington''s disease

Implicit learning was examined in 15 Huntington's disease (HD) patients and 15 control subjects (NC) using a semantic decision-making task. HD patients demonstrated only slightly reduced priming; like NC subjects, their decision times decreased over repeated presentations, though to a somewhat lesser degree. On explicit recognition testing, the HD group made significantly more false positive errors than did the control group, suggesting an impairment of effortful retrieval. The groups displayed equivalent retention of implicitly learned material after 6 months. The striatal neuronal loss of early Huntington's disease does not markedly affect priming or retention of primed stimuli, but may alter explicit memory judgements.     

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.     

The neural substrates of semantic memory deficits in early Alzheimer's disease: clues from semantic priming effects and FDG-PET

The neural substrates responsible for semantic dysfunction during the early stages of AD have yet to be clearly identified. After a brief overview of the literature on normal and pathological semantic memory, we describe a new approach, designed to provide fresh insights into semantic deficits in AD. We mapped the correlations between resting-state brain glucose utilisation measured by FDG-PET and semantic priming scores in a group of 17 AD patients. The priming task, which yields a particularly pure measurement of semantic memory, was composed of related pairs of words sharing an attribute relationship (e.g. tiger-stripe). The priming scores correlated positively with the metabolism of the superior temporal areas on both sides, especially the right side, and this correlation was shown to be specific to the semantic priming effect. This pattern of results is discussed in the light of recent theoretical models of semantic memory, and suggests that a dysfunction of the right superior temporal cortex may contribute to early semantic deficits, characterised by the loss of specific features of concepts in AD.     

Semantic activation and implicit memory in Alzheimer disease

Patients with Alzheimer disease (AD) invariably display pronounced deficits in verbal memory when retention is tested explicitly. The present study examined the possibility that tasks which require memory only implicitly would be performed normally. Moderately demented patients with probable AD were severely impaired in free recall of a word list. On a subsequent word association test, the AD patients were less likely than normals to give items from the recall list as their word associations. The results suggest that implicit verbal memory, as well as explicit memory, is impaired in AD. While the magnitude of the activation effect was significantly reduced in AD patients, it was uncorrelated with recall performance or a measure of global cognitive functioning. Memory activation may thus depend on neural circuitry outside the traditional (i.e. temporo-limbic) memory system.     

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.     

Exploring different routes of recovery from memory in Alzheimer's disease: evidence for preserved long-term priming

Studies investigating implicit memory in Alzheimer's disease suggest that priming abilities disappear over time. This study investigates long-term priming in Alzheimer's disease. A total of 20 patients with Alzheimer's disease and 20 controls underwent the Free and Cued Selective Reminding test. After a 30-minute delay, participants were submitted to a word identification task comprising the studied words and new words. The patients exhibited a long-term priming effect similar to that presented by the comparison group. Therefore, whereas explicit retrieval is definitely impaired in Alzheimer's disease, implicit processes allowing the retrieval of that same information operate relatively normally, including after a long delay.     

Is verbal recognition memory really different in Huntington's and Alzheimer's disease.

Verbal recall and recognition were examined in Huntington's disease (HD) and Alzheimer's disease (AD) patients. Subgroups of HD and AD patients were matched for overall severity of dementia. Subjects were administered the Hopkins Verbal Learning Test, a list-learning task with three free-recall trials followed immediately by one yes/no recognition trial with semantically related and unrelated distractors. The matched AD and HD groups did not differ in the number of words recalled, although the HD patients showed slightly greater improvement over trials. Recognition performance was evaluated with measures of accuracy and response bias that are independent of each other. The matched groups did not differ in overall recognition accuracy, but the AD patients tended to have a more liberal ("yea-saying") response bias than did the HD patients. In addition, only the AD patients were differentially enticed to false-positive responding by semantically related distractors. The results suggest that the rule for making decisions when uncertain, rather than memory strength per se, distinguishes the recognition memory performance of AD and HD patients.     

Face-name association learning in early Alzheimer's disease: a comparison of learning methods and their underlying mechanisms

This study compared the efficacy of five learning methods in the acquisition of face-name associations in early dementia of Alzheimer type (AD). The contribution of error production and implicit memory to the efficacy of each method was also examined. Fifteen participants with early AD and 15 matched controls were exposed to five learning methods: spaced retrieval, vanishing cues, errorless, and two trial-and-error methods, one with explicit and one with implicit memory task instructions. Under each method, participants had to learn a list of five face-name associations, followed by free recall, cued recall and recognition. Delayed recall was also assessed. For AD, results showed that all methods were efficient but there were no significant differences between them. The number of errors produced during the learning phases varied between the five methods but did not influence learning. There were no significant differences between implicit and explicit memory task instructions on test performances. For the control group, there were no differences between the five methods. Finally, no significant correlations were found between the performance of the AD participants in free recall and their cognitive profile, but generally, the best performers had better remaining episodic memory. Also, case study analyses showed that spaced retrieval was the method for which the greatest number of participants (four) obtained results as good as the controls. This study suggests that the five methods are effective for new learning of face-name associations in AD. It appears that early AD patients can learn, even in the context of error production and explicit memory conditions.     

Semantic priming for coordinate distant concepts in Alzheimer's disease patients

Semantic priming paradigms have been used to investigate semantic knowledge in patients with Alzheimer's disease (AD). While priming effects produced by prime-target pairs with associative relatedness reflect processes at both lexical and semantic levels, priming effects produced by words that are semantically related but not associated should reflect only semantic activation processes. This study was aimed at further investigating automatic semantic priming effects in AD patients when semantically related concepts with little to no lexical association are used. Twenty patients with mild to moderate AD and 20 matched controls (NCs) performed a lexical decision task on 30 concept pairs (15 in the living and 15 in the non-living domain) in an automatic semantic priming paradigm. In order to investigate the relationship between priming alteration and semantic damage, we chose concepts from a database. This allowed us to quantify semantic indexes relative to the structural representation at the feature level.No priming was found in NCs or mild AD patients, probably because feature similarity was insufficient in the concept pairs used. Similar to the hyperpriming observed in previous studies, the appearance of priming in the moderate AD group suggests early semantic damage in which attribute knowledge is partially affected. Furthermore, the finding that priming was predicted by the level of sharing (in the semantic system) of features common to the two concepts in the pairs indicates that the level of redundancy of attribute information is the main factor responsible for resiliency to neurological damage in AD.     

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.     

Impaired semantic knowledge underlies the reduced verbal short-term storage capacity in Alzheimer's disease

A decrease in verbal short-term memory (STM) capacity is consistently observed in patients with Alzheimer's disease (AD). Although this impairment has been mainly attributed to attentional deficits during encoding and maintenance, the progressive deterioration of semantic knowledge in early stages of AD may also be an important determinant of poor STM performance. The aim of this study was to examine the influence of semantic knowledge on verbal short-term memory storage capacity in normal aging and in AD by exploring the impact of word imageability on STM performance. Sixteen patients suffering from mild AD, 16 healthy elderly subjects and 16 young subjects performed an immediate serial recall task using word lists containing high or low imageability words. All participant groups recalled more high imageability words than low imageability words, but the effect of word imageability on verbal STM was greater in AD patients than in both the young and the elderly control groups. More precisely, AD patients showed a marked decrease in STM performance when presented with lists of low imageability words, whereas recall of high imageability words was relatively well preserved. Furthermore, AD patients displayed an abnormal proportion of phonological errors in the low imageability condition. Overall, these results indicate that the support of semantic knowledge on STM performance was impaired for lists of low imageability words in AD patients. More generally, these findings suggest that the deterioration of semantic knowledge is partly responsible for the poor verbal short-term storage capacity observed in AD.