Pre-experimental Familiarization Increases Hippocampal Activity for Both Targets and Lures in Recognition Memory: An fMRI Study (original) (raw)
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In Search of Recollection and Familiarity Signals in the Hippocampus
Journal of Cognitive Neuroscience, 2010
& fMRI studies of recognition memory have often been interpreted to mean that the hippocampus selectively subserves recollection and that adjacent regions selectively subserve familiarity. Yet, many of these studies have confounded recollection and familiarity with strong and weak memories. In a source memory experiment, we compared correct source judgments (which reflect recollection) and incorrect source judgments (often thought to reflect familiarity) while equating for old-new memory strength by including only high-confidence hits in the analysis. Hippocampal activity associated with both correct source judgments and incorrect source judgments exceeded the activity associated with forgotten items and did so to a similar extent. Further, hippocampal activity was greater for high-confidence old decisions relative to forgotten items even when source decisions were at chance. These results identify a recollection signal in the hippocampus and may identify a familiarity signal as well. Similar results were obtained in the parahippocampal gyrus. Unlike in the medial temporal lobe, activation in prefrontal cortex increased differentially in association with source recollection. &
Learning & Memory, 2010
It has been suggested that the hippocampus selectively supports recollection and that adjacent cortex in the medial temporal lobe can support familiarity. Alternatively, it has been suggested that the hippocampus supports both recollection and familiarity. We tested these suggestions by assessing the performance of patients with hippocampal lesions on recognition memory tests that differ in the extent to which recollection and familiarity contribute to the recognition decision. When targets and foils are highly similar, prior evidence suggests that, on a forced-choice test in which targets are presented together with highly similar, corresponding foils (the FC-C format), performance is supported primarily by familiarity. By contrast, when targets are presented together with foils that are similar to other targets (the FC-NC format) or when memory is tested in a yes/no (Y/N) format, performance is based much more strongly on recollection. Accordingly, a finding that hippocampal damag...
Recollection versus strength as the primary determinant of hippocampal engagement at retrieval
Proceedings of the National Academy of Sciences, 2009
We examined whether hippocampal activity in recognition relates to the strength of the memory or to recollective experience, a subject of considerable current debate. Participants studied word pairs and then made two successive recognition decisions on each item: first on the uncued target and then on the target presented with the studied cue word. We compared recollection and familiarity patterns of activation in fMRI for these decisions. Critically, our analyses attempted in two ways to equate perceived memory strength while varying the associative information available. First, activity for targets judged familiar before cueing was contrasted with activity for the same items in the second decision as a function of whether the targets converted to recollection or remained familiar when the context cues were provided. We found increased hippocampal activity following cueing only with recollective conversion. Second, we investigated whether hippocampal activity was modulated by the r...
A demonstration that the hippocampus supports both recollection and familiarity
Proceedings of the National Academy of Sciences, 2009
Recognition memory is thought to depend on two distinct processes: recollection and familiarity. There is debate as to whether damage to the hippocampus selectively impairs recollection or whether it impairs both recollection and familiarity. If hippocampal damage selectively impairs recollection but leaves familiarity intact, then patients with circumscribed hippocampal lesions should exhibit the full normal range of low-confidence and high-confidence familiarity-based recognition. High-confidence, familiarity-based decisions are ordinarily accompanied by successful recollection (when memory is intact). However, patients with hippocampal lesions, if recollection is impaired, should frequently experience high-confidence, familiarity-based recognition in the absence of recollection, and this circumstance (termed the “butcher-on-the-bus” phenomenon) should occur more often in patients than in healthy controls. We tested five patients with circumscribed hippocampal damage, asking them ...
Recognition memory: opposite effects of hippocampal damage on recollection and familiarity
Nature Neuroscience, 2008
A major controversy in memory research concerns whether recognition is subdivided into distinct cognitive mechanisms of recollection and familiarity that are supported by different neural substrates. Here we developed a new associative recognition protocol for rats that enabled us to show that recollection is reduced, whereas familiarity is increased following hippocampal damage. These results provide strong evidence that these processes are qualitatively different and that the hippocampus supports recollection and not familiarity.
The role of the human hippocampus in familiarity-based and recollection-based recognition memory
Behavioural Brain Research, 2010
The ability to recognize a previously encountered stimulus is dependent on the structures of the medial temporal lobe and is thought to be supported by two processes, recollection and familiarity. A focus of research in recent years concerns the extent to which these two processes depend on the hippocampus and on the other structures of the medial temporal lobe. One view holds that the hippocampus is important for both processes, whereas a different view holds that the hippocampus supports only the recollection process and the perirhinal cortex supports the familiarity process. One approach has been to study patients with hippocampal lesions and to contrast old/new recognition (which can be supported by familiarity) to free recall (which is supported by recollection). Despite some early case studies suggesting otherwise, several group studies have now shown that hippocampal patients exhibit comparable impairments on old/new recognition and free recall. These findings suggest that the hippocampus is important for both recollection and familiarity. Neuroimaging studies and Receiver Operating Characteristic analyses also initially suggested that the hippocampus was specialized for recollection, but these studies involved a strength confound (strong memories have been compared to weak memories). When steps are taken to compare strong recollection-based memories with strong familiarity-based memories, or otherwise control for memory strength, evidence for a familiarity signal (as well as a recollection signal) is evident in the hippocampus. These findings suggest that the functional organization of the medial temporal lobe is probably best understood in terms unrelated to the distinction between recollection and familiarity. The ability to recognize a stimulus as having been previously encountered depends on the structures of the medial temporal lobe (MTL) [61] and is widely assumed to involve two processes, recollection and familiarity [4,28,38]. The familiarity process underlies the almost universal experience of recognizing someone whom you are sure you have met before despite being unable to remember anything about the prior encounter. The recollection process underlies the successful retrieval of the contextual details that
Memory encoding and hippocampally-based novelty/familiarity discrimination networks
Neuropsychologia, 2003
Novelty discrimination refers to the ability to decide whether information is new or has been previously encountered. Recent functional neuroimaging work has demonstrated that the hippocampus plays an important function in novelty discrimination. In the study described here, we explored the idea that novelty discrimination does not depend on the hippocampus alone but involves large-scale functional neural networks consisting of spatially remote brain regions. We measured blood flow with positron emission tomography (PET) while subjects semantically encoded visually and auditorily presented situationally novel and familiar words. Following each PET scan, subjects' memory was tested with a standard yes/no recognition test. Blood flow data were analyzed with the covariance-based seed partial least squares (PLS) method. Behaviorally, subjects' recognition performance was higher for novel than familiar words. Neurally, two large-scale functional networks involving the same region of the hippocampus were identified which showed coherent activity either during the encoding of situationally novel (but not familiar) items or situationally familiar (but not novel) items. These findings indicate that different neural networks are active in the processing of situationally novel and familiar information. The observation that the hippocampus participates in both networks supports the principle of neural context.
Recollection and familiarity in hippocampal amnesia
2008
Currently, there is a general agreement that two distinct cognitive operations, recollection and familiarity, contribute to performance on recognition memory tests. However, there is a controversy about whether recollection and familiarity reflect different memory processes, mediated by distinct neural substrates (dual-process models), or whether they are the expression of memory traces of different strength in the context of a unitary declarative memory system (unitarystrength models). Critical in this debate is the status of recognition memory in hippocampal amnesia and, in particular, whether the various structures in the medial temporal lobe (MTL) contribute differentially to the recollection and familiarity components of recognition. The present study aimed to explore the relative contribution of recollection and familiarity to recognition of words that had been previously read or that had been previously generated in a group of severely amnesic patients with cerebral damage restricted to the hippocampus. A convergent pattern of results emerged when we used a subjective-based (remember/ know; R/K) and an objective-based (process dissociation procedure; PDP) methods to estimate the contribution of recollection and familiarity to recognition performance. In both PDP and R/K procedures, healthy controls disclosed significantly higher recollection estimates for words that had been anagrammed than for words that had been read. Amnesic patients' recollection scores were not different for words that had been generated or that had been read, and the recollection estimate for words that had been generated was significantly reduced as compared to the group of healthy controls. For familiarity, both healthy controls and amnesic patients recognized as familiar more words that had been generated than words that had been read, and there was no difference between the two groups. These data support the hypothesis of a specific role of the hippocampus in recollection processes and suggest that other components of the MTL (e.g., perirhinal cortex) may be more involved in the process of familiarity. V
Hippocampal signals for strong memory when associative memory is available and when it is not
Hippocampus, 2011
The paired-associate task has been used with functional magnetic resonance imaging (fMRI) in studies that assessed the role of the medial temporal lobe (MTL) subserving recollection and familiarity. Some researchers have interpreted their results to mean that the hippocampus selectively subserves recollection and not familiarity [cf., Eichenbaum et al., (2007) Annu Rev Neurosci 30:123-152]. Yet many of these results confound recollection and familiarity with strong and weak memories, and it is not clear whether the conclusions represent differences between memory processes or memory strength. In the current study, participants were scanned with fMRI during retrieval in a paired-associate task, and a new approach separated the analysis of memory strength from the analysis of memory processes. The data were sorted by confidence level in an old/new task, and the high-confidence responses were compared in categories when associative memory was highly accurate and when it was not available. The results show that high-confidence memory produced increased activity in the hippocampus, relative to the level for forgotten pairs, both when associative memory was available and when it was not. Two interpretations are discussed for the behavioral results for when associative memory was not available: one account based on familiarity and the other account based on noncriterial recollection. The conclusion is that recognition of the word-pairs was based on familiarity when associative memory was not available. Together with the fMRI results that activity in two regions associated with cognitive control (left ventrolateral prefrontal cortex and left inferior parietal lobule) was greater when responses were based on associative memory than when based on familiarity, the findings suggest that the hippocampus supports strong memory and that cortical regions make an additional contribution to recollection. V V C
Hippocampus, 2002
The claim that recognition memory is spared relative to recall after focal hippocampal damage has been disputed in the literature. We examined this claim by investigating object and object–location recall and recognition memory in a patient, YR, who has adult-onset selective hippocampal damage. Our aim was to identify the conditions under which recognition was spared relative to recall in this patient. She showed unimpaired forced-choice object recognition but clearly impaired recall, even when her control subjects found the object recognition task to be numerically harder than the object recall task. However, on two other recognition tests, YR's performance was not relatively spared. First, she was clearly impaired at an equivalently difficult yes/no object recognition task, but only when targets and foils were very similar. Second, YR was clearly impaired at forced-choice recognition of object–location associations. This impairment was also unrelated to difficulty because this task was no more difficult than the forced-choice object recognition task for control subjects. The clear impairment of yes/no, but not of forced-choice, object recognition after focal hippocampal damage, when targets and foils are very similar, is predicted by the neural network-based Complementary Learning Systems model of recognition. This model postulates that recognition is mediated by hippocampally dependent recollection and cortically dependent familiarity; thus hippocampal damage should not impair item familiarity. The model postulates that familiarity is ineffective when very similar targets and foils are shown one at a time and subjects have to identify which items are old (yes/no recognition). In contrast, familiarity is effective in discriminating which of similar targets and foils, seen together, is old (forced-choice recognition). Independent evidence from the remember/know procedure also indicates that YR's familiarity is normal. The Complementary Learning Systems model can also accommodate the clear impairment of forced-choice object–location recognition memory if it incorporates the view that the most complete convergence of spatial and object information, represented in different cortical regions, occurs in the hippocampus. Hippocampus 2002;12:341–351. © 2002 Wiley-Liss, Inc.