Effects of modality on the neural correlates of encoding processes supporting recollection and familiarity

Prior research has demonstrated that the neural correlates of successful encoding ("subsequent memory effects") partially overlap with neural regions selectively engaged by the on-line demands of the study task. The primary goal of the present experiment was to determine whether this overlap is associated solely with encoding processes supporting later recollection, or whether overlapping subsequent memory and study condition effects are also evident when later memory is familiarity-based. Subjects (N = 17) underwent fMRI scanning while studying a series of visually and auditorily presented words. Memory for the words was subsequently tested with a modified Remember/Know procedure. Auditorily selective subsequent familiarity effects were evident in bilateral temporal regions that also responded preferentially to auditory items. Although other interpretations are possible, these findings suggest that overlap between study condition-selective subsequent memory effects and regions selectively sensitive to study demands is not uniquely associated with later recollection. In addition, modality-independent subsequent memory effects were identified in several cortical regions. In every case, the effects were greatest for later recollected items, and smaller for items later recognized on the basis of familiarity. The implications of this quantitative dissociation for dual-process models of recognition memory are discussed.     

Brain potentials of recollection and familiarity

It is widely hypothesized that separate recollection and familiarity processes contribute to recognition memory. The present research measured event-related brain potentials (ERPs) from 128 head locations to identify patterns of brain activity related to recollection and familiarity. In two experiments, subjects performed a recognition memory task requiring discrimination between previously studied words, similar words that changed plurality between study and test, and new words (following Hintzman & Curran, 1994). The FN400 ERP component (300-500 msec) varied with the familiarity of words (new > studied = similar). The parietal component (400-800 msec) was associated with the recollection of plurality (studied > similar = new). Differences in the timing and spatial topography of the FN400 and parietal effects support the view that familiarity and recollection arise from distinct neurocognitive processes.     

Production benefits both recollection and familiarity

In three experiments, we investigated the roles of recollection and familiarity in the production effect—the finding that words read aloud are remembered better than words read silently. Experiment 1, using the remember/know procedure, and Experiment 2, using the receiver operating characteristic procedure, converged in demonstrating that production enhanced both recollection and familiarity. Experiment 3 supported the role of recollection by demonstrating that specific episodic information—that is, whether a word had been studied aloud or silently—was stronger for items studied aloud. These findings fit with an explanation of the production effect as hinging on two factors: greater recollection of distinctive information from the study episode, and more familiarity due to greater attention allocated to the material studied aloud.     

Developmental patterns in priming and familiarity in explicit recollection

Developmental trajectories of two classes of human memory, implicit and explicit memory, appear to diverge. We examined how developmental differences in perceptual and conceptual priming, two types of implicit memory, coincide with differences between familiarity and recollective responses on explicit memory tests that employ the Remember/Know paradigm ( Tulving, 1985 ). Both types of priming were characterized by developmental invariance in 52 children and adolescents ages 8-19 years. Contrary to Komatsu, Naito, and Fuke (1996) results, few age-group differences in perceptual priming were observed following a levels-of-processing encoding manipulation. In contrast, age group differences were found for "Remember" but not "Know" responses. Neither levels of awareness nor strategies influenced priming. Adult levels of performance appear earlier in development on perceptual and conceptual priming tests compared to explicit memory tests. Similar developmental dissociations exist between explicit and implicit memory performance as between "Remember" and "Know" recollective responses.     

Novelty effects on recollection and familiarity in recognition memory

Recognition memory is better for novel or distinctive items than for non-novel items. However, it is not known whether these effects reflect changes in recollection or in familiarity-based recognition judgments. Some previous results have indicated that recollection should be more sensitive to novelty than to familiarity, whereas other results have suggested the opposite. We used avon Restorff paradigm in which a small proportion of studied items were made novel by presenting them in a color different from that of the majority of the study items. Memory was tested using a remember-know procedure. Across two experiments, stimulus novelty was found to benefit both recollection and familiarity. The effects on familiarity were observed under intentional and incidental encoding conditions, whereas the effects on recollection were significantly reduced, and no longer significant, under incidental as compared with intentional encoding conditions. Thus, both processes benefit from stimulus novelty, but the extent to which recollection benefits from novelty depends on the encoding condition.     

Mild hypoxia disrupts recollection,not familiarity

Yonelinas et al. (2002) found that hypoxic patients exhibited deficits in recollection that left familiarity relatively unaffected. In contrast, Manns, Hopkins, Reed, Kitchener, and Squire (2003) studied a group of hypoxic patients who suffered severe and equivalent deficits in recollection and familiarity. We reexamine those studies and argue that the discrepancy in results is likely due to differences in the hypoxic groups that were tested (i.e., differences in amnestic severity, subject sampling methods, and patient etiology). Yonelinas et al. examined memory in 56 cardiac arrest patients who suffered a brief hypoxic event, whereas Manns et al. examined a group of severely amnesic patients that consisted of 2 cardiac arrest patients, 2 heroin overdose patients, 1 carbon monoxide poisoning patient, and 2 patients with unknown etiologies. We also consider an alternative explanation proposed by Wixted and Squire (2004), who argued that the two patient groups suffered similar deficits, but that statistical or methodological artifacts distorted the results of each of Yonelinas et al.'s experiments. A consideration of those results, however, indicates that such an explanation does not account for the existing data. All of the existing evidence indicates that recollection, but not familiarity, is disrupted in mild hypoxic patients. In more severe cases of hypoxia, or those with more complex etiologies such as heroin overdose, more profound deficits may be observed.     

Dissociating familiarity from recollection using rote rehearsal

Recollection-based recognition memory judgments benefit greatly from effortful elaborative encoding, whereas familiarity-based judgments are much less sensitive to such manipulations. In this study, we have examined whether rote rehearsal under divided attention might produce the opposite dissociation, benefiting familiarity more than recollection. Subjects rehearsed word pairs during the "distractor" phase of a working memory span task, and were then given a surprise memory test for the distractor items at the end of the experiment. Experiment 1 demonstrated that increasing rehearsal elevated the recognition rate for intact and rearranged pairs, but neither associative recognition accuracy nor implicit fragment completion benefited from rehearsal. The results suggest that rote rehearsal leads to a greater increase in familiarity than in recollection, and that the increase in observed familiarity cannot be attributed to effects of repetition priming. In Experiment 2, we tested item recognition with the remember/know procedure, and the results supported the conclusions of Experiment 1. Moreover, a signal detection model of remember/know performance systematically overpredicted rehearsal increases in remember rates, and this worsened when high-rehearsal items were assumed to be more variable in strength. The results suggest that rote rehearsal can dissociate familiarity from recollection at the time of encoding and that item recognition cannot be fully accommodated within a one-dimensional signal detection model.     

Differential effects of list strength on recollection and familiarity

Numerous studies have found a null list strength effect (LSE) for recognition sensitivity: Strengthening memory traces associated with some studied items does not impair recognition of nonstrengthened studied items. In Experiment 1, the author found a LSE using receiver operating characteristic-based measures of recognition sensitivity. To account for the discrepancy between this and prior research, the author (a) argues that a LSE occurs for recollection but not for discrimination based on familiarity, and (b) presents self-report data consistent with this hypothesis. Experiment 2 tested the dual-process hypothesis more directly, using switched-plurality (SP) lures to isolate the contribution of recollection. There was a significant LSE for comparisons involving SP lures; the LSE for discrimination of studied items and nominally unrelated lures (which can be supported by familiarity) was not significant.     

Memory conjunction clusters: Influence of familiarity and recollection

In the memory conjunction paradigm, the number of times that constituents of conjunction lures were studied and the method of presentation were varied. In two experiments, participants were presented with eight parent items that could be recombined at test to form a conjunction lure. The constituents that were shared between the parent items and the conjunction lures were either presented in the same words (e.g., blackmail and jailbird presented four times each for the conjunction lure blackbird) or in different words (e.g., the targets footstool, footlocker, foothill, footbridge, baseball, softball, basketball, and golfball for the conjunction lure football). In both experiments, rates of false recognition were higher in the Different condition as opposed to the Same condition. These results provide evidence that participants in the Same condition were able to utilise a recall-to-reject strategy by remembering the repeatedly presented parent word. In the Different condition, participants were not able to utilise that strategy and instead relied on the familiarity of the repeatedly presented constituents which led to higher rates of false recognition.     

Effect of post-encoding emotion on recollection and familiarity for pictures

Although prior studies have examined the effect of post-encoding emotional arousal on recognition memory for words, it is unknown whether the enhancement effect observed on words generalizes to pictures. Furthermore, prior studies using words have showed that the effect of emotional arousal can be modulated by stimuli valence and delay in emotion induction, but it is unclear whether such modulation can extend to pictures and whether other factors such as encoding method (incidental vs. intentional encoding) can be modulatory. Five experiments were conducted to answer these questions. In Experiment 1, participants encoded a list of neutral and negative pictures and then watched a 3-min neutral or negative video. The delayed test showed that negative arousal impaired recollection regardless of picture valence but had no effect on familiarity. Experiment 2 replicated the above findings. Experiment 3 was similar to Experiment 1 except that participants watched a 3-min neutral, negative, or positive video and conducted free recall before the recognition test. Unlike the prior two experiments, the impairment effect of negative arousal disappeared. Experiment 4, where the free recall task was eliminated, replicated the results from Experiment 3. Experiment 5 replicated Experiments 1 and 2 and further showed that the impairment effects of negative arousal could be modulated by delay in emotion induction but not by encoding method or stimuli valence. Taken together, the current study suggests that the enhancement effect observed on words may not generalize to pictures.     

Environmental context and recognition: the role of recollection and familiarity

Evidence for effects of changed environmental context on recognition has been equivocal. Using 3 experiments, the author investigated the role of environmental context from a dual-processing approach. Experiment 1 showed that testing word recognition in a novel context led to a reliable decrement but only for recognition accompanied by conscious recollection, with familiarity-based recognition judgments being unaffected. This was replicated in Experiment 2 using stimuli that were novel to the participants (nonwords). Experiment 3 showed that the decrement in recollection also occurred when the changed-context condition involved presenting items in a different but familiar context. The results suggest that effects of environmental context will only be found when recognition is accompanied by conscious recollection and that this effect is due to a specific item-context association.     

Context effects in recognition memory: the role of familiarity and recollection

A variant of the process dissociation procedure was coupled with a manipulation of response signal lag to assess whether manipulations of context affect one or both of the familiarity and search processes described by the dual process model of recognition. Participants studied a list of word pairs (context+target) followed by a recognition test with target words presented in the same or different context, and in the same or different form as study (singular/plural). Participants were asked to recognize any target word regardless of changes to form (inclusion), or to only recognise words that were presented in the same form (exclusion). The standard context reinstatement effect was evident even at the short response lags. Analyses of the estimates of the contributions of familiarity and search processes suggest that the context effect demonstrated here can be attributed in part to the influence of familiarity on recognition, whereas the effect on recollection was less clear.     

Effects of context on recollection and familiarity experiences are task dependent

The influence of test context on reports of recollection and familiarity depends on how these subjective recognition experiences are conceptualized and measured. Bodner and Lindsay (2003) found that critical items elicited more remember judgments but fewer know judgments in a less (vs. more) memorable context. In contrast, Tousignant and Bodner (2012) found that independent ratings of recollection and familiarity were both higher in a less memorable context. We replicated the dissociative pattern with judgments using recollect/familiar labels (Experiment 1), and in a novel R/F/B task that added a “both” option to eliminate the mutual exclusivity between the recollect and familiar options (Experiment 2). Adding a “guess” option eliminated these context effects (Experiment 3), however whether allowing guesses “cleans up” or “desensitizes” recollection and familiarity judgments remains unclear. Determining which task variants provide appropriate measures of subjective recognition experiences will require an examination of additional dissociations and triangulation with other measures.     

Altering the balance of recollection and familiarity influences the revelation effect

The revelation effect occurs when recognition test probes are more likely to be called "old" if they are preceded by a verbal processing task. Two experiments examined the role of familiarity and recollection in producing this effect. Each experiment tested the hypothesis that decreasing recollection would heighten the magnitude of the revelation effect. In Experiment 1, the revelation effect increased by delaying the recognition test. In Experiment 2, the revelation effect increased when the presentation rate of the study words was reduced. These results are discussed in terms of the variables that produce the revelation effect in episodic and nonepisodic memory judgments.     

Validating neural correlates of familiarity

Familiarity is a pervasive memory phenomenon that occurs in its most basic form when someone recognizes a repeated stimulus without recollecting other aspects of the requisite prior learning episode. Theoretical controversy currently abounds with respect to both the cognitive and neural characteristics of familiarity. Here, we show that the extant data, particularly brain-potential data, are insufficient for validating putative neural correlates of familiarity, and we outline strategies for making progress on this problem. Conceptual priming is an implicit-memory phenomenon that often occurs together with familiarity; experiments that conflate the two phenomena can be misleading. Avoiding this conflation is required to understand familiarity and to determine the extent to which the neurocognitive processes that support priming also drive familiarity.     

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.     

The sensorimotor contributions to implicit memory, familiarity, and recollection

The sensorimotor contributions to memory for prior occurrence were investigated. Previous research has shown that both implicit memory and familiarity draw on gains in stimulus-related processing fluency for old, compared with novel, stimuli, but recollection does not. Recently, it has been demonstrated that processing fluency itself resides in stimulus-specific motor simulations or reenactment (e.g., covert pronouncing simulations for words as stimuli). Combining these lines of evidence, it was predicted that stimulus-specific motor interference preventing simulations should impair both implicit memory and familiarity but leave recollection unaffected. This was tested for words as verbal stimuli associated to pronouncing simulations in the oral muscle system (but also for tunes as vocal stimuli and their associated vocal system, Experiment 2). It was found that oral (e.g., chewing gum), compared with manual (kneading a ball), motor interference prevented mere exposure effects (Experiments 1-2), substantially reduced repetition priming in word fragment completion (Experiment 3), reduced the familiarity estimates in a remember-know task (Experiment 5) and in receiver-operating characteristics (Experiment 6), and completely neutralized familiarity measured by self-reports (Experiment 4) and skin conductance responses (Experiment 7), while leaving recollection and free recall unaffected (across Experiments 1-7). This pattern establishes a rare memory dissociation in healthy participants, that is, explicit without implicit memory or recognizing without feeling familiar. Implications for embodied memory and neuropsychology are discussed.     

Measuring recollection and familiarity: Improving the remember/know procedure

The remember/know (RK) procedure is the most widely used method to investigate recollection and familiarity. It uses trial-by-trial reports to determine how much recollection and familiarity contribute to different kinds of recognition. Few other methods provide information about individual memory judgements and no alternative allows such direct indications of recollection and familiarity influences. Here we review how the RK procedure has been and should be used to help resolve theoretical disagreements about the processing and neural bases of components of recognition memory. Emphasis is placed on procedural weaknesses and a possible confound of recollection and familiarity with recognition memory strength. Recommendations are made about how to minimise these problems including using modified versions of the procedure. The proposals here are important for improving behavioural and lesion research, and vital for brain imaging work.     

Imaging recollection and familiarity in the medial temporal lobe: a three-component model

The medial temporal lobe (MTL) plays a crucial role in supporting memory for events, but the functional organization of regions in the MTL remains controversial, especially regarding the extent to which different subregions support recognition based on familiarity or recollection. Here we review results from functional neuroimaging studies showing that, whereas activity in the hippocampus and posterior parahippocampal gyrus is disproportionately associated with recollection, activity in the anterior parahippocampal gyrus is disproportionately associated with familiarity. The results are consistent with the idea that the parahippocampal cortex (located in the posterior parahippocampal gyrus) supports recollection by encoding and retrieving contextual information, whereas the hippocampus supports recollection by associating item and context information. By contrast, perirhinal cortex (located in the anterior parahippocampal gyrus) supports familiarity by encoding and retrieving specific item information. We discuss the implications of a 'binding of item and context' (BIC) model for studies of recognition memory. This model argues that there is no simple mapping between MTL regions and recollection and familiarity, but rather that the involvement of MTL regions in these processes depends on the specific demands of the task and the type of information involved. We highlight several predictions for future imaging studies that follow from the BIC model.     

一体化促进联结记忆的作用机制：熟悉性和回想加工

当两个或两个以上项目进行一体化编码时, 熟悉性也能够支持联结再认, 这一观点已经得到大量研究证据的支持。然而, 关于一体化如何影响联结再认和构成联结的单个项目再认仍存在分歧。通过回顾现有研究发现：(1)一体化一致性是调节一体化与联结再认关系的重要因素; (2)认知资源有限和新/旧词语义相关性是影响一体化对项目再认作用的重要因素; (3)一体化的发生机制存在“项目假说”、“图式假说”以及“精细加工假说”三种可能的理论解释。未来研究不仅需要控制一体化一致性, 还可以比较不同一体化方式的作用大小以及探索一体化效应的毕生发展规律。