It is well accepted that recognition memory reflects the contribution of two separable memory retrieval processes, namely recollection and familiarity. However, fundamental questions remain regarding the functional nature and neural substrates of these processes. In this article, we describe a simple quantitative model of recognition memory (i.e., the dual-process signal detection model) that has been useful in integrating findings from a broad range of cognitive studies, and that is now being applied in a growing number of neuroscientific investigations of memory. The model makes several strong assumptions about the behavioral nature and neural substrates of recollection and familiarity. A review of the literature indicates that these assumptions are generally well supported, but that there are clear boundary conditions in which these assumptions break down. We argue that these findings provide important insights into the operation of the processes underlying recognition. Finally, we consider how the dual-process approach relates to recent neuroanatomical and computational models and how it might be integrated with recent findings concerning the role of medial temporal lobe regions in other cognitive functions such as novelty detection, perception, implicit memory and short-term memory.
It is well established that healthy aging, amnestic Mild Cognitive Impairment (aMCI), and Alzheimer’s Disease (AD) are associated with substantial declines in episodic memory. However, there is still debate as to how two forms of episodic memory – recollection and familiarity – are affected by healthy and pathological aging. To address this issue we conducted a meta-analytic review of the effect sizes reported in studies using remember/know (RK), receiver operating characteristic (ROC) and process dissociation (PD) methods to examine recollection and familiarity in healthy aging (25 published reports), aMCI (9 published reports), and AD (5 published reports). The results from the meta-analysis revealed that healthy aging is associated with moderate-to-large recollection impairments. Familiarity was not impaired in studies using ROC or PD methods but was impaired in studies that used the RK procedure. aMCI was associated with large decreases in recollection whereas familiarity only tended to show a decrease in studies with a patient sample comprised of both single-domain and multiple-domain aMCI patients. Lastly, AD was associated with large decreases in both recollection and familiarity. The results are consistent with neuroimaging evidence suggesting that the hippocampus is critical for recollection whereas familiarity is dependent on the integrity of the surrounding perirhinal cortex. Moreover, the results highlight the relevance of method selection when examining aging, and suggest that familiarity deficits might be a useful behavioral marker for identifying individuals that will develop dementia.
Many cognitive abilities decline with age even in the absence of detectable pathology. Recent evidence indicates that age-related neural dedifferentiation, operationalized in terms of the neural selectivity, may contribute to this decline. Here, we review work exploring the relationship between neural dedifferentiation, cognition, and age. The evidence for age effects on neural selectivity comes from both non-human animal and human research and is compelling. However, current data suggest that age does not moderate observed relationships between neural dedifferentiation and cognitive performance. We propose that functionally significant variance in measures of neural dedifferentiation reflects both age-dependent and age-independent factors. We further propose that the effects of age on neural dedifferentiation do not exclusively reflect detrimental consequences of aging.
Healthy aging is associated with decreased neural selectivity (dedifferentiation) in category-selective cortical regions. This finding has prompted the suggestion that dedifferentiation contributes to age-related cognitive decline. Consistent with this possibility, dedifferentiation has been reported to negatively correlate with fluid intelligence in older adults. Here, we examined whether dedifferentiation is associated with performance in another cognitive domain-episodic memory-that is also highly vulnerable to aging. Given the proposed role of dedifferentiation in age-related cognitive decline, we predicted there would be a stronger link between dedifferentiation and episodic memory performance in older than in younger adults. Young (18-30 years) and older (64-75 years) male and female humans underwent fMRI scanning while viewing images of objects and scenes before a subsequent recognition memory test. We computed a differentiation index in two regions of interest (ROIs): parahippocampal place area (PPA) and lateral occipital complex (LOC). This index quantified the selectivity of the BOLD response to preferred versus nonpreferred category of an ROI (scenes for PPA, objects for LOC). The differentiation index in the PPA, but not the LOC, was lower in older than in younger adults. Additionally, the PPA differentiation index predicted recognition memory performance for the studied items. This relationship was independent of and not moderated by age. The PPA differentiation index also predicted performance on a latent "fluency" factor derived from a neuropsychological test battery; this relationship was also age invariant. These findings suggest that two independent factors, one associated with age, and the other with cognitive performance, influence neural differentiation.
It is well established that the memory strength of studied items is more variable than the strength of new items on tests of recognition memory, but the reason why this occurs is poorly understood. One account for this old item variance effect is based on single-process theory, which proposes that this effect is due to variability in how well items are initially encoded into memory (i.e., the encoding variability account). In contrast, dual-process theory argues that old items are more variable because they are influenced by both recollection and familiarity, whereas recognition of new items relies primarily on familiarity. The current study shows that increasing encoding variability did not increase old item variance, and that old item variance is directly related to the contribution of recollection. These results indicate that old item memory variability is due to the relative contribution of recollection and familiarity.
Although it is generally accepted that aging is associated with recollection impairments, there is considerable disagreement surrounding how healthy aging influences familiarity-based recognition. One factor that might contribute to the mixed findings regarding age differences in familiarity is the estimation method used to quantify the two mnemonic processes. Here, this issue is examined by having a group of older adults (N = 39) between 40 and 81 years of age complete Remember/Know (RK), receiver operating characteristic (ROC), and process dissociation (PD) recognition tests. Estimates of recollection, but not familiarity, showed a significant negative correlation with chronological age. Inconsistent with previous findings, the estimation method did not moderate the relationship between age and estimations of recollection and familiarity. In a final analysis, recollection and familiarity were estimated as latent factors in a confirmatory factor analysis (CFA) that modeled the covariance between measures of free recall and recognition, and the results converged with the results from the RK, PD, and ROC tasks. These results are consistent with the hypothesis that episodic memory declines in older adults are primary driven by recollection deficits, and also suggest that the estimation method plays little to no role in age-related decreases in familiarity.
Memory reactivation-the reinstatement of processes and representations engaged when an event is initially experienced-is believed to play an important role in strengthening and updating episodic memory. The present study examines how memory reactivation during a potentially interfering event influences memory for a previously experienced event. Participants underwent fMRI during the encoding phase of an AB/AC interference task in which some words were presented twice in association with two different encoding tasks (AB and AC trials) and other words were presented once (DE trials). The later memory test required retrieval of the encoding tasks associated with each of the study words. Retroactive interference was evident for the AB encoding task and was particularly strong when the AC encoding task was remembered rather than forgotten. We used multivariate classification and pattern similarity analysis (PSA) to measure reactivation of the AB encoding task during AC trials. The results demonstrated that reactivation of generic task information measured with multivariate classification predicted subsequent memory for the AB encoding task regardless of whether interference was strong and weak (trials for which the AC encoding task was remembered or forgotten, respectively). In contrast, reactivation of neural patterns idiosyncratic to a given AB trial measured with PSA only predicted memory when the strength of interference was low. These results suggest that reactivation of features of an initial experience shared across numerous events in the same category, but not features idiosyncratic to a particular event, are important in resisting retroactive interference caused by new learning.
Prior studies have indicated that post-encoding stress can protect memories from the effects of forgetting, and this has been taken as evidence that stress facilitates memory consolidation. However, it is not known whether stress acts by directly influencing the strength of the underlying memories or whether it influences the generation process that plays a critical role in tests such as free recall. To address this issue, we examined the effects of stress produced by skydiving on recognition memory for negative and neutral pictures. Relative to a non-stress control condition, post-encoding stress in males was found to increase recognition memory for neutral pictures. However, stress was not found to improve recognition for emotional pictures, nor was it found to influence recognition memory in female participants. Additional analysis of recognition performance suggested that stress increased familiarity-based recognition rather than recollection. The current study indicates that stress can improve familiarity-based recognition, thus showing that that stress directly increases the strength of the underlying memories.
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