Individual differences in forced-choice recognition memory: partitioning contributions of recollection and familiarity.

In forced-choice recognition memory, two different testing formats are possible under conditions of high target-foil similarity: Each target can be presented alongside foils similar to itself (forced-choice corresponding; FCC), or alongside foils similar to other targets (forced-choice noncorresponding; FCNC). Recent behavioural and neuropsychological studies suggest that FCC performance can be supported by familiarity whereas FCNC performance is supported primarily by recollection. In this paper, we corroborate this finding from an individual differences perspective. A group of older adults were given a test of FCC and FCNC recognition for object pictures, as well as standardized tests of recall, recognition, and IQ. Recall measures were found to predict FCNC, but not FCC performance, consistent with a critical role for recollection in FCNC only. After the common influence of recall was removed, standardized tests of recognition predicted FCC, but not FCNC performance. This is consistent with a contribution of only familiarity in FCC. Simulations show that a two-process model, where familiarity and recollection make separate contributions to recognition, is 10 times more likely to give these results than a single-process model. This evidence highlights the importance of recognition memory test design when examining the involvement of recollection and familiarity.

Listening for recollection: a multi-voxel pattern analysis of recognition memory retrieval strategies.

Recent studies of recognition memory indicate that subjects can strategically vary how much they rely on recollection of specific details vs. feelings of familiarity when making recognition judgments. One possible explanation of these results is that subjects can establish an internally directed attentional state ("listening for recollection") that enhances retrieval of studied details; fluctuations in this attentional state over time should be associated with fluctuations in subjects' recognition behavior. In this study, we used multi-voxel pattern analysis of fMRI data to identify brain regions that are involved in listening for recollection. We looked for brain regions that met the following criteria: (1) Distinct neural patterns should be present when subjects are instructed to rely on recollection vs. familiarity, and (2) fluctuations in these neural patterns should be related to recognition behavior in the manner predicted by dual-process theories of recognition: Specifically, the presence of the recollection pattern during the pre-stimulus interval (indicating that subjects are "listening for recollection" at that moment) should be associated with a selective decrease in false alarms to related lures. We found that pre-stimulus activity in the right supramarginal gyrus met all of these criteria, suggesting that this region proactively establishes an internally directed attentional state that fosters recollection. We also found other regions (e.g., left middle temporal gyrus) where the pattern of neural activity was related to subjects' responding to related lures after stimulus onset (but not before), suggesting that these regions implement processes that are engaged in a reactive fashion to boost recollection.

Impaired recollection but spared familiarity in patients with extended hippocampal system damage revealed by 3 convergent methods.

To understand recognition memory, the detection of stimulus repetition, it first is necessary to resolve the debate between 2 fundamentally different models of recognition. Contemporary single-process models assume that recognition memory relies solely on the neural system required for the recall of prior events. Dual-process models assume that recognition comprises 2 independent forms of memory: one supports recall, and the other detects repeated stimuli by signaling their familiarity, the feeling of previous occurrence without the recall of any associated information. These 2 models were contrasted in patients who had undergone surgical removal of a colloid cyst, a condition associated with memory loss when accompanied by fornix and/or mammillary body atrophy. Comparisons were made between 2 groups of 9 patients that differed only with respect to the extent of mammillary body atrophy. Only the more atrophied group was impaired on tests of recall, but both groups showed normal recognition levels on a task that equates recall and recognition performance in normal participants. To explore the nature of this spared recognition, we estimated recall-based recognition and familiarity-based recognition using 3 distinct methods: self-report, receiver operating characteristics, and structural equation modeling. All 3 methods showed impaired recall-based recognition accompanied by intact familiarity in the most atrophied group, as predicted only by dual-process models. When structural equation modeling was applied to all 62 colloid cyst patients, the recall/familiarity dual-process model best explained the patients' memory pattern. The convergent evidence that mammillary body atrophy impairs recall but spares familiarity-based recognition appears irreconcilable with single-process models.

Perirhinal cortex supports encoding and familiarity-based recognition of novel associations.

Results from imaging and lesion studies of item recognition memory have suggested that the hippocampus supports memory for the arbitrary associations that form the basis of episodic recollection, whereas the perirhinal cortex (PRc) supports familiarity for individual items. This view has been challenged, however, by findings showing that PRc may contribute to associative recognition, a task thought to measure relational or recollective memory. Here, using functional magnetic resonance imaging, we demonstrate that PRc activity is increased when pairs of items are processed as a single configuration or unit and that this activity predicts subsequent familiarity-based associative memory. These results explain the discrepancy in the literature by showing that novel associations can be encoded in a unitized manner, thereby allowing PRc to support associative recognition based on familiarity.

Effect of unitization on associative recognition in amnesia.

We examined how associative recognition performance in amnesic patients is mediated by use of a unitized (i.e., holistic) encoding strategy, and the degree to which the unitization effect is related to sparing of familiarity-based recognition. Participants studied word pairs as either separate lexical units in sentences (i.e., nonunitized) or as compounds (unitized). Under standard recognition instructions, normal controls and patients with left-temporal lobe damage (previously determined to have impairments in both recollection and familiarity) showed no difference for unitized and nonunitized pairs, whereas hypoxics (previously determined to have impaired recollection but relatively preserved familiarity) showed an advantage of unitized over nonunitized pairs. This effect was reproduced in normal healthy participants under instructions to restrict responses to judgments of familiarity. The results indicate that unitization may mediate the degree of associative recognition impairment exhibited by some amnesic patients, and that the effect is related to preserved familiarity capacity. The relevance of the results to the debate over the importance of the hippocampus in memory for associations is discussed.

Recall and recognition in mild hypoxia: using covariance structural modeling to test competing theories of explicit memory.

To test theories of explicit memory in amnesia, we examined the effect of hypoxia on memory performance in a group of 56 survivors of sudden cardiac arrest. Structural equation modeling revealed that a single-factor explanation of recall and recognition was insufficient to account for performance, thus contradicting single-process models of explicit memory. A dual-process model of recall in which two processes (e.g., declarative memory and controlled search) contribute to recall performance, whereas only one process (e.g., declarative memory) underlies recognition performance, also failed to explain the results adequately. In contrast, a dual-process model of recognition provided an acceptable account of the data. In this model, two processes--recollection and familiarity--underlie recognition memory, whereas only the recollection process contributes to free recall. The best-fitting model was one in which hypoxia and aging led to deficits in recollection, but left familiarity unaffected. Moreover, a controlled search process was correlated with recollection, but was not associated with familiarity or the severity of hypoxia. The results support models of explicit memory in which recollection depends on the hippocampus and frontal lobes, whereas familiarity-based recognition relies on other brain regions.

Recognition memory for source and occurrence: the importance of recollection.

Previous recognition memory studies indicate that when both recollection and familiarity are expected to contribute to recognition performance (e.g., discriminating studied items from nonstudied items) the dual-process and the unequal-variance signal detection models provide comparable accounts of performance. When familiarity is not expected to be useful (e.g., when items from two equally familiar sources are discriminated between), the dual-process model provides a significantly better account of performance. In the present study, source recognition was tested under conditions in which familiarity could have been used to perform a list-discrimination task; participants were required to discriminate between strong studied items, weak studied items, and new items. The dual-process model provided a better account of performance than did the unequal-variance model. Moreover, the results indicated that the unequal-variance assumption in a single-process signal detection model was not a valid substitution for recollection and that recollection was used to make recognition judgments even when assessments of familiarity were useful.

Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity.

Memory for past events can be based on recollection or on assessments of familiarity. These two forms of human memory have been studied extensively by philosophers and psychologists, but their neuroanatomical substrates are largely unknown. Here we examined the brain regions that are involved in these two forms of memory by studying patients with damage to different temporal lobe regions. Our results come from (i) structural covariance modeling of recall and recognition, (ii) introspective reports during recognition and (iii) analysis of receiver operating characteristics. In sum, we found that the regions disrupted in mild hypoxia, such as the hippocampus, are centrally involved in conscious recollection, whereas the surrounding temporal lobe supports familiarity-based memory discrimination.