Short- and Long-Term Implicit Memory in Aging and Alzheimer's Disease

ABSTRACT

Implicit memory processes were investigated via picture naming in healthy young and older adults and in persons with mild Alzheimer's disease (AD). Repetition priming in picture-naming was intact in all groups over the course of a short retention interval (seconds), and only the AD group revealed a deficit over a longer interval (72 hours). In addition, the AD group showed impaired procedural memory, with no benefit of practice on picture-naming. Impaired long-term priming was related to severity of AD. Both theoretical and methodological implications are discussed.     

Effects of age of acquisition and priming on picture naming

Four experiments examined the interaction of age of acquisition (AoA) and priming on picture naming. Experiment 1 found that initial-letter priming and AoA significantly affected picture-naming latencies, but there was no interaction between them. Experiment 2 found that initial-phoneme priming and AoA significantly affected picture-naming latencies, but again there was no interaction. Experiment 3 repeated Barry, Hirsh, Johnston, and Williams's (2001) priming study using a very short interval between prime and target. Experiment 3 replicated previous findings of a significant interaction between priming and AoA. Experiment 4 repeated this investigation with a procedure that did not require participants to articulate the prime. Once again, there were significant effects of priming, AoA, and the interaction between them. The implications of these findings in relation to accounts of AoA and its locus of effect are discussed.     

Effects of age of acquisition and priming on picture naming

Four experiments examined the interaction of age of acquisition (AoA) and priming on picture naming. Experiment 1 found that initial-letter priming and AoA significantly affected picture-naming latencies, but there was no interaction between them. Experiment 2 found that initial-phoneme priming and AoA significantly affected picture-naming latencies, but again there was no interaction. Experiment 3 repeated Barry, Hirsh, Johnston, and Williams's (2001) priming study using a very short interval between prime and target. Experiment 3 replicated previous findings of a significant interaction between priming and AoA. Experiment 4 repeated this investigation with a procedure that did not require participants to articulate the prime. Once again, there were significant effects of priming, AoA, and the interaction between them. The implications of these findings in relation to accounts of AoA and its locus of effect are discussed.     

Convergent behavioral and neuropsychological evidence for a distinction between identification and production forms of repetition priming

Four experiments examined a distinction between kinds of repetition priming which involve either the identification of the form or meaning of a stimulus or the production of a response on the basis of a cue. Patients with Alzheimer's disease had intact priming on picture-naming and category-exemplar identification tasks and impaired priming on word-stem completion and category-exemplar production tasks. Division of study-phase attention in healthy participants reduced priming on word-stem completion and category-exemplar production tasks but not on picture-naming and category-exemplar identification tasks. The parallel dissociations in normal and abnormal memory cannot be explained by implicit-explicit or perceptual-conceptual distinctions but are explained by an identification-production distinction. There may be separable cognitive and neural bases for implicit modulation of identification and production forms of knowledge.     

The dissociation of repetition priming and recognition memory in language/learning-disabled children.

Recent research has found that the performance of learning-disabled and non-disabled children is dissociated on explicit and implicit tests of memory (Lorsbach & Worman, 1989). The current study further examined this phenomenon by comparing language/learning-disabled (L/LD) and nondisabled children (NLD) on tasks measuring primed picture-naming and item recognition. Included within the design of the experiment was the manipulation of both presentation format (pictures or words) and retention interval (immediate or 1 day). Children were initially presented with pictures and words. Performance was measured both immediately and following a 1-day retention interval on a picture naming task, an item recognition task, and a supplementary measure of memory for presentation format. The magnitude of facilitation associated with primed picture-naming was found to be independent of item recognition performance. In addition, the effects of population (L/LD and NLD) and retention interval (immediate test or 1 day) each produced dissociations between the magnitude of naming facilitation and item recognition performance. Results were discussed in terms of their implications for our understanding of the nature of memory difficulties in L/LD children.     

Transfer of processing in repetition priming: some inappropriate findings.

Transfer effects in repetition priming were found with both picture and word naming, but varied with the type of prime list. Unmixed lists of word or picture primes produced equivalent intra-modal and cross-modal repetition priming in both picture-naming (Experiment 1) and word-naming (Experiment 5) tasks. However, mixing word and picture primes resulted in greater intra-modal than cross-modal priming for both picture-naming (Experiment 2) and word-naming (Experiment 6) tasks. This mixed-list difference between intra-modal and cross-modal priming was reduced by blocking prime types at input (Experiment 3). These findings suggest that differences in priming as a function of prime stimulus format should be cautiously interpreted when mixed prime lists are used.     

Picture priming in normal aging and Alzheimer's disease

The present study investigated age invariance for naming pictures and whether implicit memory is spared in Alzheimer's disease (AD). During the study phase, young adults, AD patients, and older controls were shown outlines of familiar pictures. After a distracter task, implicit memory was assessed incidentally. The results showed similar visual priming for the three groups, although young adults responded faster than the two older groups. Moreover, the number of errors was smaller for studied than for non-studied pictures. This pattern of results was repeated across the three groups, although AD patients produced more errors than young adults and older controls, and there were no differences between these latter groups. These results confirmed previous visual and haptic findings showing unimpaired perceptual priming in normal aging and AD patients when implicit memory is assessed using identification tasks. These results are interpreted from a cognitive neuroscience perspective.     

The attribute priming effect in patients with Alzheimer's disease

Experiments with semantic priming (SP) paradigms have documented early hypopriming in patients with AD when concepts are used as primes and attribute concept features as targets, suggesting that concept attributes are vulnerable to damage very early in the disease course. The aims of this study were to confirm early priming reduction in the attribute condition in patients with AD and to determine which of several semantic indexes (such as the level of distinctiveness, correlation or feature dominance of concept features) best predicts the priming effect size in AD. We administered an SP attribute condition paradigm to 20 mildly demented patients with AD and to 10 NCs. We used concept–attribute pairs for which normative data of semantic indexes relative to both concept primes (i.e., number, type, mean level of dominance, distinctiveness and correlation of features constituting the concepts) and target features (i.e., level of feature dominance, correlation and distinctiveness) were available. Results showed that compared to NCs, the AD group obtained very reduced priming facilitation. Furthermore, the item regression analyses showed that the priming decrement in the AD group was predicted by the feature dominance of the target in the related pairs; that is, the lower the target feature dominance, the lower the priming effect elicited. These results confirmed hypopriming in the attribute condition from the very early phase of AD and support the view that attributes which are more salient for the identification of a given concept are also those most resistant to semantic memory degradation in AD pathology.     

Data-driven and conceptually driven processes in partial-word identification and recognition

Three experiments examined priming in partial-word identification (Warrington & Weiskrantz, 1968) and its relation to recognition memory. The results showed that changes in modality of presentation between study and test reduced performance on both identification and recognition. In contrast, changes in elaborative processing enhanced recognition but had no effect on identification. Furthermore, when explicit memory instructions were given, identification was changed to a cued recall test and was consequently affected by elaborative processing. We also found that the time course of forgetting in priming was different from that in recognition; priming in identification did not change over a 24-hr interval, whereas recognition declined rapidly during this interval. Overall, these results suggest that identification relies primarily on data-driven processing, whereas recognition can rely on both data-driven and conceptually driven processing.     

How many memory systems? Evidence from aging

The present research tested Tulving's (1985) ternary memory theory. Young (ages 19-32) and older (ages 63-80) adults were given procedural, semantic, and episodic memory tasks. Repetition, lag, and codability were manipulated in a picture-naming task, followed by incidental memory tests. Relative to young adults, older adults exhibited lower levels of recall and recognition, but these episodic measures increased similarly as a function of lag and repetition in both age groups. No age-related deficits emerged in either semantic memory (vocabulary, latency slopes, naming errors, and tip-of-the-tongue responses) or procedural memory (repetition priming magnitude and rate of decline). In addition to the age by memory task dissociations, the manipulation of codability produced slower naming latencies and more naming errors (semantic memory), yet promoted better recall and recognition (episodic memory). Finally, a factor analysis of 11 memory measures revealed three distinct factors, providing additional support for a tripartite memory model.     

Memory deficits in Alzheimer's patients: A comprehensive review

Despite considerable experimental work on Alzheimer's disease (AD), the underlying cognitive mechanisms as well as the precise localization of neuropathological changes critical for memory loss remains undefined. A review of the neuropsychological literature on long-term memory deficits in AD patients suggests that AD patients display (a) a pervasive deficit of explicit memory, (b) a partial deficiency of implicit memory for verbal and visuoperceptual material (as measured by repetition priming procedures), and (c) a substantial sparing of implicit memory for visuomotor skills. The explicit memory loss is likely a result of encoding as well as consolidation difficulties. A faulty lexical-semantic knowledge structure appears responsible for deficient repetition priming effects. Since neuropathological changes diffusely affect the brain of AD patients, establishing a clear relationship between localization of cerebral lesions and memory deficits is particularly difficult. Nevertheless, data suggest that extensive involvement of the hippocampal-amygdala complex plays a major role in explicit memory loss. Damage to associative cortical areas likely is involved in repetition priming deficits. The relative integrity of primary motor and sensory cortical areas and of the basal ganglia likely subsume, by contrast, the normal learning of visuomotor skills.     

A longitudinal study of implicit and explicit memory in old persons

Decline in explicit memory with advancing age is a common finding, but it is unclear whether implicit memory (repetition priming) declines or remains stable. Meta-analyses of studies that examined differences between extreme groups (young-old), typically at a single point in time and on a single test, suggest that a mild reduction in priming occurs with advancing age. The authors examined explicit memory and priming, on multiple tests over 4 annual data-collection waves, in a large group of older persons without dementia at baseline. Explicit memory declined significantly, but priming remained stable. Findings indicate that explicit memory and priming are dissociable on the basis of age-related change and that mildly reduced priming is not an inevitable consequence of growing older.     

Lexical but not semantic priming in Alzheimer's disease.

The hypothesis that patients with Alzheimer's disease (AD) have a disturbance in semantic processing was tested using a new lexical-priming task, threshold oral reading. Healthy elderly controls showed significant effects of priming for word pairs that are associatively related (words that reliably co-occur in word association tests) and for word pairs that are semantically related (high-frequency exemplars that belong to the same superordinate category but are not high-frequency associates). AD patients showed effects of priming for associatively related words but not for word pairs that are related only by shared semantic features. These results are consistent with the hypothesis that semantic processing is impaired in AD and suggest that independent networks of relationships among words and among concepts in semantic memory may be differentially disrupted with various forms of brain damage.     

Assessment of associative relations in alzheimer's disease: Evidence for preservation of semantic memory

Abstract

Semantic priming was assessed in Alzheimer's disease (AD), elderly control, and young control subjects with three lexical decision, continuous priming experiments. the stimuli were intracategory, associated pairs in Experiments 1 and 2 and varied types of associated pairs in Experiment 3. AD priming effects were equal to those of elderly control subjects; elderly and young control priming effects were also equal. We interpret this as evidence for the relative preservation of the semantic memory network in early AD, as in normal aging, at least to the extent necessary for normal access of concept nodes and normal automatic spreading activation between concept nodes. In a final study (Experiment 4) knowledge of the associations between the targets and related primes used in Experiments 1 and 2 was explicitly assessed; 20 out of 22 AD subjects showed perfect or close to perfect performance.     

Conceptual implicit memory and environmental context

Changes in environmental context between encoding and retrieval often affect explicit memory but research on implicit memory is equivocal. One proposal is that conceptual but not perceptual priming is influenced by context manipulations. However, findings with conceptual priming may be compromised by explicit contamination. The present study examined the effects of environmental context on conceptual explicit (category-cued recall) and implicit memory (category production). Explicit recall was reduced by context change. The implicit test results depended on test awareness (assessed with a post-test questionnaire). Among test-unaware participants, priming was equivalent for same-context and different-context groups, whereas for the test-aware, the same-context group produced more priming. Thus, when explicit contamination is controlled, changes in environmental context do not impair conceptual priming. Context dependency appears to be a general difference between implicit and explicit memory rather than a difference between conceptual and perceptual implicit memory. Finally, measures of mood indicated no changes in affect across contexts, arguing against mood mediation for the context effects in explicit recall.     

Single and Multiple Test Repetition Priming in Implicit Memory

Using a picture naming task, we compared the magnitude of repetition priming after one prior study episode (single test priming) versus multiple prior study presentations (multiple test priming). Pictures were repeated either one, two, or three times, and the interval between tests was either several minutes (blocked test) or one week (spaced test). Priming increased with additional prior presentations (beyond one) in the multiple test format. In addition, single test priming decreased within one hour after initial exposure, with little change from one hour to two weeks. Priming was unaffected by a simultaneous recognition task, suggesting that picture naming is an implicit task relatively immune from explicit memory contamination.     

Semantic priming and identification of near threshold primes in a lexical decision task

Three experiments examined both the impact of semantic analysis of 50-msec, masked visual primes on a target response and the impact of semantic analysis of the target on a prime response. The first two experiments used a prime-target interval of 1000 msec. In Experiment 1, subjects reported the identity of each prime: (a) after a lexical decision about the target, (b) both before and after a lexical decision, or (c) after a target detection response. Prime report after both types of target response showed retroactive priming in which report was facilitated by related targets and inhibited by unrelated targets. Analyses of lexical decision latency and accuracy conditionalized on prime report showed that semantic priming was restricted to reported related primes. In Experiment 2, subjects made no overt response to the primes. Priming was conditionalized on recognition of the primes on a subsequent test. The pattern was the same as Experiment 1: There was priming only for recognized primes; recognition memory showed a pattern consistent with retroactive priming. Experiment 3 also conditionalized priming on recognition performance but used a prime-target interval of only 250 msec. Again, semantic priming was found only for recognized primes, and recognition memory revealed retroactive priming. Retroactive priming indicates an interdependency between prime and target processing that needs to be incorporated into models of semantic priming.     

Available but unattended conceptual information in working memory: temporarily active semantic content or persistent memory for prior operations?

In 2 experiments, the authors investigated available but unattended information following working memory task demands. The experimental task presented a memory set containing exemplars from 2 conceptual categories. Following instructions to focus attention on only 1 category, priming of both categories was assessed with category comparisons of exemplar pairs. Priming was greatest for the focused category and for exemplars from the memory set (direct priming). Priming also extended to new exemplars of both categories (indirect priming) and showed little decline over more than 1 min of intervening processes. Finally, changing between category exemplars and features across memory set and comparison phases eliminated the indirect priming. These results support a persistent, operation-specific, procedural account of available but unattended conceptual information in working memory.     

Long-term positive and negative identity priming: Evidence for episodic retrieval

An episodic retrieval account of negative priming (Neill, 1997; Neill & Valdes, 1992) was evaluated in three experiments. Duringpractice, regular word pairs were presented to subjects differing numbers of times. The subjects named specific target words while they ignored specific distractor words. Following a 5-min retention interval, memory for practice was revealed:Test responses for target words exhibited positive priming that increased with increases in the number of times that the words had been attended. Test responses for distractor words exhibited either positive priming (Experiment 1) or negative priming (Experiments 2–3) that also increased with increases in the number of times that the words had been ignored. The type of priming that abstractors exhibited was determined by several contextual similarities between the practice environment, in which distractors were ignored initially, and the test environments, in which they were processed subsequently. Negative priming that spanned a 5-min interval, increased with increases in the number of times that a distractor was ignored, and was sensitive to contextual changes indicated that the direction of the effect was temporally backward because the test probe cued memory for earlier processing of the priming stimulus when the distractor had been ignored.     

Semantic priming occurs for word but not location pronunciation in the postcue task

Semantic priming refers to the finding that a word response is facilitated if it is preceded by a related word compared to when it is preceded by an unrelated word. Dallas and Merikle (Can J Psychol 30: 15–21 1976a; Bull Psychon Soc 8: 441–444 1976b) demonstrated that semantic priming occurred under conditions in which a pair of simultaneously displayed words was previewed for over a second prior to the onset of a cue indicating which of the words should be pronounced aloud (postcue task). In contrast, semantic interference effects have been reported for postcue picture-naming tasks (Dean et al. in J Exp Psychol Learn Mem Cogn 27: 733–743, 2001; Humphreys et al. in J Exp Psychol Learn Mem Cogn 21: 961–980, 1995). According to Dean et al., the semantic interference effects in postcue picture naming occur because the integration of the object and the cued attribute in memory is more difficult for categorically related pictures than for unrelated pictures. The aim of this experiment was to determine whether this idea was true for postcue word pronunciation tasks. Participants completed two postcue tasks, one requiring pronunciation of the target word indicated by a locational cue and another requiring pronunciation of the location of a centrally presented word. Results indicated a semantic priming effect only for the locational cue condition suggesting that the integration of the cue and identity information was unaffected by word context. These data suggest that priming in a postcue word pronunciation task may be due to feedback from residual activation within the semantic system facilitating access to the target word’s phonology.