A demonstration that the hippocampus supports both recollection and familiarity.
ABSTRACT: 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 to recognize recently studied words as well as to remember the context in which the items were studied. Relative to controls, the patients exhibited no increased tendency to experience the butcher-on-the-bus phenomenon. The simplest explanation of the results is that hippocampal damage impairs familiarity as well as recollection. The same conclusion was suggested when two competing models of recognition memory were used to analyze the data.
Project description:Declarative memory is thought to rely on two processes: recollection and familiarity. Recollection involves remembering specific details about the episode in which an item was encountered, and familiarity involves simply knowing that an item was presented even when no information can be recalled about the episode itself. There has been debate whether the hippocampus supports only recollection or whether it supports both processes. We approached this issue in a relatively theory-neutral way by fitting two prominent models that have been used to describe recognition memory: dual process signal detection and unequal variance signal detection. Both models yield two parameters of interest when fit to recognition memory data. The dual process signal detection model yields estimates of recollection (r) and familiarity (d'). The unequal variance signal detection model yields estimates of the ratio of the variance of target and foil memory strength distributions (?target/?foil) and the difference in the means of the two distributions (d). We asked how the two parameters of each model were affected by hippocampal damage. We tested five patients with well-characterized bilateral lesions thought to be limited to the hippocampus and age-matched controls. The patients exhibited a broad memory deficit that markedly reduced the value of both parameters in both models. In addition, the pattern of results exhibited by the patients was recapitulated in healthy controls as the delay between learning and testing was extended. Thus, hippocampal damage impairs both component processes of recognition memory.
Project description: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.
Project description: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.
Project description:Anesthesia in infancy impairs performance in recognition memory tasks in mammalian animals, but it is unknown if this occurs in humans. Successful recognition can be based on stimulus familiarity or recollection of event details. Several brain structures involved in recollection are affected by anesthesia-induced neurodegeneration in animals. Therefore, we hypothesized that anesthesia in infancy impairs recollection later in life in humans and rats. Twenty eight children ages 6-11 who had undergone a procedure requiring general anesthesia before age 1 were compared with 28 age- and gender-matched children who had not undergone anesthesia. Recollection and familiarity were assessed in an object recognition memory test using receiver operator characteristic analysis. In addition, IQ and Child Behavior Checklist scores were assessed. In parallel, thirty three 7-day-old rats were randomized to receive anesthesia or sham anesthesia. Over 10 months, recollection and familiarity were assessed using an odor recognition test. We found that anesthetized children had significantly lower recollection scores and were impaired at recollecting associative information compared with controls. Familiarity, IQ, and Child Behavior Checklist scores were not different between groups. In rats, anesthetized subjects had significantly lower recollection scores than controls while familiarity was unaffected. Rats that had undergone tissue injury during anesthesia had similar recollection indices as rats that had been anesthetized without tissue injury. These findings suggest that general anesthesia in infancy impairs recollection later in life in humans and rats. In rats, this effect is independent of underlying disease or tissue injury.
Project description:The role of the hippocampus in recollection and familiarity remains debated. Using functional magnetic resonance imaging (fMRI), we explored whether hippocampal activity is modulated by increasing recollection confidence, increasing amount of recalled information, or both. We also investigated whether any hippocampal differences between recollection and familiarity relate to processing differences or amount of information in memory. Across two fMRI tasks, we separately compared brain responses to levels of confidence for cued word recall and word familiarity, respectively. Contrary to previous beliefs, increasing confidence/accuracy of cued recall of studied words did not increase hippocampal activity, when unconfounded by amount recollected. In contrast, additional recollection (i.e., recollecting more information than the word alone) increased hippocampal activity, although its accuracy matched that of word recall alone. Unlike cued word recall, increasing word familiarity accuracy did increase hippocampal activity linearly, although at an uncorrected level. This finding occurred although cued word recall and familiarity memory seemed matched with respect to information in memory. The detailed characteristics of these effects do not prove that word familiarity is exceptional in having hippocampal neural correlates. They suggest instead that participants fail to identify some aspects of recollection, misreporting it as familiarity, a problem with word-like items that have strong and recallable semantic associates.
Project description:Recognition memory may be supported by two independent types of retrieval, conscious recollection of a specific experience and a sense of familiarity gained from previous exposure to particular stimuli. In humans, signal detection techniques have been used to distinguish recollection and familiarity, respectively, in asymmetrical and curvilinear components of their receiver operating characteristic (ROC) curves, standard curves that represent item recognition across different levels of confidence or bias. To determine whether animals also employ multiple processes in recognition memory and to explore the anatomical basis of this distinction, we adapted these techniques to examine odour recognition memory in rats. Their ROC curve had asymmetrical and curvilinear components, indicating the existence of both recollection and familiarity in rats. Furthermore, following selective damage to the hippocampus the ROC curve became entirely symmetrical and remained curvilinear, supporting the view that the hippocampus specifically mediates the capacity for recollection.
Project description:Despite a substantial body of work comprising theoretical modeling, the effects of medial temporal lobe lesions, and electrophysiological signal analysis, the role of the hippocampus in recognition memory remains controversial. In particular, it is not known whether the hippocampus exclusively supports recollection or both recollection and familiarity--the two latent cognitive processes theorized to underlie recognition memory. We studied recognition memory in a large group of patients undergoing intracranial electroencephalographic (iEEG) monitoring for epilepsy. By measuring high-frequency activity (HFA)--a signal associated with precise spatiotemporal properties--we show that hippocampal activity during recognition predicted recognition memory performance and tracked both recollection and familiarity. Through the lens of dual-process models, these results indicate that the hippocampus supports both the recollection and familiarity processes.
Project description:A major controversy in the study of memory concerns whether there are distinct medial temporal lobe (MTL) substrates of recollection and familiarity. Studies using receiver operating characteristics analyses of recognition memory indicate that the hippocampus is essential for recollection, but not for familiarity. We found the converse pattern in the amygdala, wherein damage impaired familiarity while sparing recollection. Combined with previous findings, these results dissociate recollection and familiarity by selective MTL damage.
Project description:There is continuing controversy about the extent to which the rodent medial prefrontal cortical area (mPFC) is functionally homologous to the dorsolateral prefrontal cortex in humans and nonhuman primates. Previous studies have compared the effects of mPFC lesions in rats to those of dorsolateral prefrontal lesions in working memory, strategy switching, and temporal ordering. None, however, has examined the role of the rodent mPFC in recognition memory, wherein, in humans, dorsolateral prefrontal damage results in a deficit in source monitoring resulting in impaired recollection. In the present study, we examined recognition memory in rats with bilateral mPFC lesions (prelimbic/infralimbic regions; ibotenic acid) using a variant of a non-match-to-sample task with manipulations of response bias that allowed for a signal detection analysis that distinguishes recollection and familiarity contributions to recognition memory. Animals with medial prefrontal lesions had a modest overall deficit in recognition with no general change in their tendency to elicit "old" or "new" responses. Signal detection analyses indicated that rats with mPFC damage had a curvilinear and symmetrical receiver operating characteristic (ROC) curve, compared with a curvilinear and asymmetrical ROC curve in control subjects, indicating that mPFC damage severely reduced recollection-based performance, while sparing familiarity. The recollection failure was associated with an impaired ability to reject new items (increased false alarm rate), whereas the identification of old items (hit rate) was normal. This pattern of findings is similar to that observed in humans with dorsolateral prefrontal damage and is complementary to the selective deficit in hit rate observed after hippocampal damage.
Project description: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 rated familiarity strength of cued items or whether it increased uniquely in recollection. Hippocampal activation was not modulated parametrically by familiarity strength and recollected items were associated with greater activity relative to highly familiar items. Together, our results support the notion that it is recollection of context, rather than memory strength, that underlies hippocampal engagement at retrieval.