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.     

双加工再认提取中的情绪记忆增强效应

根据双加工理论, 再认提取可以划分为两种不同的加工：熟悉性与回想。以往的研究普遍认为情绪对再认提取具有增强效应, 但是情绪对再认记忆中两种不同加工方式(熟悉性与回想)的增强效应的神经机制尚存争议。本研究以ERP作为测量手段, 采用修正的“记得/知道”范式对情绪图片进行再认测验, 旨在探究在学习?测验间隔较长的条件下, 情绪信息如何对熟悉性与回想产生增强效应。在行为结果中, 对于知道判断, 情绪图片的记忆表现显著高于中性图片, 情绪效价间没有差异; 对于记得判断, 负性情绪图片的记忆表现要显著高于正性与中性图片。在ERP数据上, 对于知道判断, 情绪图片的FN400新旧效应有增强作用。对于记得判断, 负性图片的LPC的新旧效应波幅显著高于中性与负性图片; 而正性图片的LPC新旧效应增强作用不显著。以上证据表明：学习?测验间隔较长的情况下, 熟悉性再认提取中, 情绪记忆增强效应主要体现在情绪唤醒对记忆强度的提高, 而不仅仅体现在情绪效价对熟悉判断反应倾向的影响。在回想的再认提取中, 情绪效价的调节占据主导地位, 负性情绪图片有显著的情绪记忆增强效应; 正性情绪图片则不具有增强效应。     

Recollection can be weak and familiarity can be strong

The remember-know procedure is widely used to investigate recollection and familiarity in recognition memory, but almost all of the results obtained with that procedure can be readily accommodated by a unidimensional model based on signal-detection theory. The unidimensional model holds that remember judgments reflect strong memories (associated with high confidence, high accuracy, and fast reaction times), whereas know judgments reflect weaker memories (associated with lower confidence, lower accuracy, and slower reaction times). Although this is invariably true on average, a new 2-dimensional account (the continuous dual-process model) suggests that remember judgments made with low confidence should be associated with lower old-new accuracy but higher source accuracy than know judgments made with high confidence. We tested this prediction--and found evidence to support it--using a modified remember-know procedure in which participants were first asked to indicate a degree of recollection-based or familiarity-based confidence for each word presented on a recognition test and were then asked to recollect the color (red or blue) and screen location (top or bottom) associated with the word at study. For familiarity-based decisions, old-new accuracy increased with old-new confidence, but source accuracy did not (suggesting that stronger old-new memory was supported by higher degrees of familiarity). For recollection-based decisions, both old-new accuracy and source accuracy increased with old-new confidence (suggesting that stronger old-new memory was supported by higher degrees of recollection). These findings suggest that recollection and familiarity are continuous processes and that participants can indicate which process mainly contributed to their recognition decisions.     

Identifying the Basis for the Word Frequency Effect in Recognition Memory

Abstract

Recent theories of recognition memory have identified two bases on which recognition-memory judgments may be made: recollection, which involves retrieval of contextual information from an earlier episode of stimulus presentation; and familiarity, which is distinguished by a general sense of familiarity in the absence of recollection. Four experiments were conducted to test whether the word frequency effect (WFE) in recognition memory (superior performance with low- in comparison with high-frequency targets) results from recollection-based processes, familiarity-based processes, or both. In two of the experiments, superior memory for aspects of the study context was found for low-frequency in comparison with high-frequency words, suggesting frequency-related differences in recollection. The other two experiments used Jacoby's (1991) inclusion/exclusion paradigm to provide estimates of the contribution of recollection and familiarity to recognition. In both experiments the data suggested that the WFE is primarily a recollection-based phenomenon. These findings suggest that the recognition memory WFE for old items results primarily from the effects of word frequency on recollection. The implications of these findings for theories of recognition memory are discussed.     

Content-specific source encoding in the human medial temporal lobe

Although the medial temporal lobe (MTL) is known to be essential for episodic encoding, the contributions of individual MTL subregions remain unclear. Data from recognition memory studies have provided evidence that the hippocampus supports relational encoding important for later episodic recollection, whereas the perirhinal cortex has been linked with encoding that supports later item familiarity. However, extant data also strongly implicate the perirhinal cortex in object processing and encoding, suggesting that perirhinal processes may contribute to later episodic recollection of object source details. To investigate this possibility, encoding activation in MTL subregions was analyzed on the basis of subsequent memory outcome while participants processed novel scenes paired with 1 of 6 repeating objects. Specifically, encoding activation correlating with later successful scene recognition memory was evaluated against that of source recollection for the object paired with the scene during encoding. In contrast to studies reporting a link between perirhinal cortex and item familiarity, it was found that encoding activation in the right perirhinal cortex correlates with successful recollection of the paired object. Furthermore, other MTL subregions also exhibited content-specific source encoding patterns of activation, suggesting that MTL subsequent memory effects are sensitive to stimulus category.     

Recollection reduces unitised familiarity effect

Two types of encoding tasks have been employed in previous research to investigate the beneficial effect of unitisation on familiarity-based associative recognition (unitised familiarity effect), namely the compound task and the interactive imagery task. Here we show how these two tasks could differentially engage subsequent recollection-based associative recognition and consequently lead to the turn-on or turn-off of the unitised familiarity effect. In the compound task, participants studied unrelated word pairs as newly learned compounds. In the interactive imagery task, participants studied the same word pairs as interactive images. An associative recognition task was used in combination with the Remember/Know procedure to measure recollection-based and familiarity-based associative recognition. The results showed that the unitised familiarity effect was present in the compound task but was absent in the interactive imagery task. A comparison of the compound and the interactive imagery task revealed a dramatic increase in recollection-based associative recognition for the interactive imagery task. These results suggest that unitisation could benefit familiarity-based associative recognition; however, this effect will be eliminated when the memory trace formed is easily accessed by strong recollection without the need for a familiarity assessment.     

Dissociating familiarity from recollection in human recognition memory: Different rates of forgetting over short retention intervals

Two functionally distinct forms of recognition memory have been identified in human and nonhuman species—the ability to recollect qualitative information about previous events, and the ability to differentiate between familiar and novel stimuli. Separate dual-process theories have been developed in the animal and human literatures to account for these findings. However, it is not clear whether these theories describe the same two underlying memory processes. On the basis of animal studies of medial temporal lobe function, familiarity is expected to exhibit disproportionately fast forgetting compared with recollection over short retention intervals. We tested this prediction in healthy human subjects by examining recognition forgetting rates across a range of 8–32 intervening items and found significant forgetting in the accuracy of familiarity-based discriminations and no evidence of forgetting in the accuracy of recollection-based discriminations. In agreement with the results from nonhuman species, the present results indicate that item familiarity decreases more rapidly than recollection over short retention intervals.     

熟悉性与回想分离的新证据

人们常常发现自己对某一情景有些熟悉, 但又想不起以前有关的经历。对这种熟悉感的理论解释, 一种观点认为熟悉感来自一种较弱的记忆形式, 与有回忆情况下的再认属于同一加工过程(single-process models, SPM)。另一种观点则认为, 熟悉感来自一种基于熟悉性的再认, 与基于回想的再认相互独立(dual-process theories, DPT)。在实验室, 评估熟悉性与回想是否相互独立的基本方法是寻找两者分离的证据。本文尝试梳理无线索回忆再认(recognition without cued recall, RWCR)范式的研究, 结果显示：熟悉性对某种特殊的概念加工和整体特征的知觉加工要比回想更加敏感, 并没有支持SPM关于回想和熟悉性各自对意义加工和局部特征的知觉加工更加敏感的推断。而且RWCR研究还观测到熟悉性与回想在行为和神经成像方面的实验性分离, 支持了DPT关于熟悉性与回想相互独立的推断。最后, 本文从熟悉性的深层机制和中英文材料对RWCR的不同影响出发, 对未来研究提出展望。     

Familiarity is related to conceptual implicit memory: An examination of individual differences

Explicit memory is thought to be distinct from implicit memory. However, growing evidence has indicated that explicit familiarity-based recognition memory judgments rely on the same process that supports conceptual implicit memory. We tested this hypothesis by examining individual differences using a paradigm wherein we measured both familiarity and conceptual implicit memory within the same participants. In Experiments 1a and 1b, we examined recognition memory confidence ROCs and remember/know responses, respectively, to estimate recollection and familiarity, and used a free association task to measure conceptual implicit memory. The results demonstrated that, across participants, familiarity, but not recollection, was significantly correlated with conceptual priming. In contrast, in Experiment 2, utilizing a similar paradigm, a comparison of recognition memory ROCs and explicit associative cued-recall performance indicated that cued recall was related to both recollection and familiarity. These results are consistent with models assuming that familiarity-based recognition and conceptual implicit memory rely on similar underlying processes.     

故事情境下真实记忆与虚假记忆的活动差异

以故事情境为实验材料,采用学习再认实验范式,通过操纵再认靶词与故事情境的关联性考察了情境故事对关联虚假记忆和真实再认神经活动的影响。结果发现：在记忆再认的熟悉性加工和回想性加工阶段,虚假记忆与真实记忆所诱发FN400和LPC成分走向一致;在额叶后提取阶段,虚假再认所诱发的晚慢成分波幅大于真实再认。结果说明：情境性关联虚假记忆与真实记忆表现出相似的熟悉性和回想性加工,但在后期需耗费额外的加工资源进行成功的提取。     

The influence of intentional versus incidental retrieval practices on the role of recollection in test-enhanced learning

A testing effect occurs when taking a test leads to more durable memory for tested materials, relative to restudying them during the same period of time. In the current study, we examined whether incidental and intentional restudy/testing practice modes during a practice phase would modulate the contribution of recollection-based and familiarity-based retrieval in a final recognition test. Both practice strategy (restudy versus testing) and practice mode (incidental vs. intentional) were manipulated between participants (N = 160). The restudy and testing groups performed a semantic rating task and a word fragment completion task, respectively, in the incidental condition or in the intentional condition. Only those participants in the intentional condition were instructed to recall or restudy the targets. All participants went through two study–practice cycles that involved two different sets of targets. After the second cycle, participants performed a list-discrimination recognition test that could assess the contributions of recollection-based and familiarity-based retrieval on test-enhanced learning. The testing effect occurred in the intentional condition, but not in the incidental condition. Relative to intentional restudy, intentional testing boosted recollection, but not familiarity, demonstrating the role of recollection in test-enhanced learning.     

An fMRI study of long-term everyday memory using SenseCam

We used a novel automatic camera, SenseCam, to investigate recognition memory for real-life events at a 5-month retention interval. Using fMRI we assessed recollection and familiarity memory using the remember/know procedure. Recollection evoked no medial temporal lobe (MTL) activation compared to familiarity and new responses. Instead, recollection activated diverse regions in neocortex including medial prefrontal cortex. We observed decreased activation in anterior hippocampus/ anterior parahippocampal gyrus (aPHG) at 5 months compared to a 36-hour retention interval. Familiarity was associated with greater activation in aPHG and posterior parahippocampal gyrus (pPHG) than recollection and new responses. Familiarity activation decreased over time in anterior hippocampus/aPHG and posterior hippocampus/pPHG. The engagement of neocortical regions such as medial prefrontal cortex at a 5-month delay, together with the reduced MTL activation at 5 months relative to at 36 hours is in line with the assumptions of Consolidation theory. SenseCam provides a valuable technique for assessing the processes that underlie remote everyday recognition memory.     

ROC in animals: Uncovering the neural substrates of recollection and familiarity in episodic recognition memory

It is a consensus that familiarity and recollection contribute to episodic recognition memory. However, it remains controversial whether familiarity and recollection are qualitatively distinct processes supported by different brain regions, or whether they reflect different strengths of the same process and share the same support. In this review, I discuss how adapting standard human recognition memory paradigms to rats, performing circumscribed brain lesions and using receiver operating characteristic (ROC) methods contributed to solve this controversy. First, I describe the validation of the animal ROC paradigms and report evidence that familiarity and recollection are distinct processes in intact rats. Second, I report results from rats with hippocampal dysfunction which confirm this finding and lead to the conclusion that the hippocampus supports recollection but not familiarity. Finally, I describe a recent study focusing on the medial entorhinal cortex (MEC) that investigates the contribution of areas upstream of the hippocampus to recollection and familiarity.     

Recollective experience, normal aging, and frontal dysfunction.

This study examined the nature of verbal recognition memory in young and old subjects. Following presentation of a word list, subjects undertook a yes-no recognition test and indicated whether their decision was based on explicit recollection or assessment of familiarity. Explicit recollection declined with age, and familiarity-based recognition increased. Furthermore, the extent to which older subjects relied on familiarity-based recognition correlated with neuropsychological indices of frontal lobe dysfunction. A further experiment indicated that the change from explicit recollection to familiarity-based responding was unrelated to changes in older subjects' confidence about their memory. The data indicate the central role of frontal dysfunction in understanding age-related memory loss.     

The relevance of the first two eye fixations for recognition memory processes

ABSTRACT

Stimuli can be recognised based on information from only one or two eye fixations. With only one fixation, item recognition is typically above chance level and performance generally saturates by the second fixation. Thus, the first two eye fixations play an important role for recognition memory performance. However, little is known about the involved processes. Therefore, two experiments were conducted to investigate hypotheses regarding the role of the first two eye fixations for specific recognition memory processes, that is, familiarity and recollection. In addition, we looked in detail at the unique contributions of (a) longer input duration and (b) additional information provided by a second fixation for familiarity- and recollection-based recognition, using a gaze-contingent stimulus presentation technique. The experiments showed that recollection- but not familiarity-based recognition increased with two compared to only one fixation, and that the second fixation boosted recollection both due to longer availability of the input and additional stimulus information gathered.     

Recollection,not familiarity,decreases in healthy ageing: Converging evidence from four estimation methods

Although it is generally accepted that ageing is associated with recollection impairments, there is considerable disagreement surrounding how healthy ageing 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 estimates of recollection and familiarity. In a final analysis, recollection and familiarity were estimated as latent factors in a confirmatory factor analysis that modelled 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.     

Overcoming interference: an fMRI investigation of pattern separation in the medial temporal lobe

The medial temporal lobe (MTL) supports the formation and retrieval of long-term declarative memories, or memories for facts and everyday events. One challenge posed for this type of memory stems from the highly overlapping nature of common episodes. Within cognitive psychology, it is widely accepted that interference between information learned at different times is a major limitation on memory. In spite of several decades of intense research in the fields of interference theory and the neurobiological underpinnings of declarative memory, there is little direct evidence bearing on how the MTL resolves this interference to form accurate memories of everyday facts and events. Computational models of MTL function have proposed a mechanism in which the MTL, specifically the hippocampus, performs pattern separation, whereby overlapping representations are made less similar. However, there is little evidence bearing on how this process is carried out in the intact human MTL. Using high-resolution fMRI, we conducted a set of experiments that taxed behavioral pattern separation by using highly similar, interfering stimuli in a modified continuous recognition task. Regions within the parahippocampal gyrus demonstrated activity consistent with a "recall to reject" strategy. In contrast and critical to performing the task, activity within the hippocampus distinguished between correctly identified true stimulus repetitions, correctly rejected presentations of similar lure stimuli, and false alarms to similar lures. These data support the computational models' assertion that the hippocampus plays a key role in pattern separation.     

Response bias,recollection, and familiarity in individuals with Highly Superior Autobiographical Memory (HSAM)

ABSTRACT

The current study focused on individuals with Highly Superior Autobiographical Memory (HSAM) and had two main objectives: 1) investigate whether HSAMs have increased recollection performance compared to controls, and 2) investigate whether HSAMs have a reliably different response bias than controls. While previous lab-based recognition tests have shown that HSAMs have normal memory performance, these tests were based on a mixture of both recollection and familiarity. Here, we employed recognition tests specifically designed to separate recollected responses from those based on familiarity. Additionally, we were interested in how HSAMs make their memory decisions. Several studies have shown a great deal of variability between individuals in their response bias. Here, individuals with HSAM and age- matched controls completed a remember/know and a source memory test. HSAMs behaved like controls in both overall and recollection-based memory discrimination. However, HSAMs showed a significantly more liberal response bias, endorsing more items as “old” than controls. These findings contribute to our understanding of how memory processes – especially those related to decision-making – function in those with superior memory abilities and may help elucidate how other (non-HSAM) memory experts make decisions.     

Cognitive mechanisms of false facial recognition in older adults

Older adults show elevated false alarm rates on recognition memory tests involving faces in comparison to younger adults. It has been proposed that this age-related increase in false facial recognition reflects a deficit in recollection and a corresponding increase in the use of familiarity when making memory decisions. To test this hypothesis, we examined the performance of 40 older adults and 40 younger adults on a face recognition memory paradigm involving three different types of lures with varying levels of familiarity. A robust age effect was found, with older adults demonstrating a markedly heightened false alarm rate in comparison to younger adults for "familiarized lures" that were exact repetitions of faces encountered earlier in the experiment, but outside the study list, and therefore required accurate recollection of contextual information to reject. By contrast, there were no age differences in false alarms to "conjunction lures" that recombined parts of study list faces, or to entirely new faces. Overall, the pattern of false recognition errors observed in older adults was consistent with excessive reliance on a familiarity-based response strategy. Specifically, in the absence of recollection older adults appeared to base their memory decisions on item familiarity, as evidenced by a linear increase in false alarm rates with increasing familiarity of the lures. These findings support the notion that automatic memory processes such as familiarity remain invariant with age, while more controlled memory processes such as recollection show age-related decline.     

Aging Effects on Recollection and Familiarity: The Role of White Matter Hyperintensities

ABSTRACT

Previous studies have indicated that aging is associated with declines in recollection whereas familiarity-based recognition is left largely unaffected. The brain changes underlying these recollection declines are yet not well understood. In the current study we examined the role of white matter integrity as measured by white matter hyperintensities (WMH) on age-related changes in recollection and familiarity. Recognition was measured using a remember/know procedure (Experiment 1) and a source-memory process-dissociation procedure (Experiment 2). Robust age related declines in recollection were observed, but there was no evidence that white matter damage was related to the observed memory declines. Although future studies with larger samples will be necessary to fully characterize the role of WMH in normal age-related declines in different types of memory, the results suggest that declines in recollection are not strongly related to the brain changes indexed by WMHs.