In search of recollection and familiarity signals in the hippocampus.
ABSTRACT: 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:Recollection is typically associated with high recognition confidence and accurate source memory. However, subjects sometimes make accurate source memory judgments even for items that are not confidently recognized, and it is not known whether these responses are based on recollection or some other memory process. In the current study, we measured event related potentials (ERPs) while subjects made item and source memory confidence judgments in order to determine whether recollection supported accurate source recognition responses for items that were not confidently recognized. In line with previous studies, we found that recognition memory was associated with two ERP effects: an early on-setting FN400 effect, and a later parietal old-new effect [late positive component (LPC)], which have been associated with familiarity and recollection, respectively. The FN400 increased gradually with item recognition confidence, whereas the LPC was only observed for highly confident recognition responses. The LPC was also related to source accuracy, but only for items that had received a high confidence item recognition response; accurate source judgments to items that were less confidently recognized did not exhibit the typical ERP correlate of recollection or familiarity, but rather showed a late, broadly distributed negative ERP difference. The results indicate that accurate source judgments of episodic context can occur even when recollection fails.
Project description: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: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:The sense of familiarity for events is crucial for successful recognition memory. However, the neural substrate and mechanisms supporting familiarity remain unclear. A major controversy in memory research is whether the parahippocampal areas, especially the lateral entorhinal (LEC) and the perirhinal (PER) cortices, support familiarity or whether the hippocampus (HIP) does. In addition, it is unclear if LEC, PER and HIP interact within this frame. Here, we especially investigate if LEC and PER's contribution to familiarity depends on hippocampal integrity. To do so, we compare LEC and PER neural activity between rats with intact hippocampus performing on a human to rat translational task relying on both recollection and familiarity and rats with hippocampal lesions that have been shown to then rely on familiarity to perform the same task. Using high resolution Immediate Early Gene imaging, we report that hippocampal lesions enhance activity in LEC during familiarity judgments but not PER's. These findings suggest that different mechanisms support familiarity in LEC and PER and led to the hypothesis that HIP might exert a tonic inhibition on LEC during recognition memory that is released when HIP is compromised, possibly constituting a compensatory mechanism in aging and amnesic patients.
Project description:fMRI was employed to assess whether the neural correlates of accurate source memory are modulated by the reward value of recollected information. Study items comprised pictures of objects, each paired with a depiction of 1 of 2 coins. The reward value of the coins ($2.00 vs. $0.02) was disclosed after study. At test, a source memory procedure was employed in which subjects discriminated between studied and unstudied objects and, for objects judged studied, indicated the identity of the coin paired with the object at study. Correct judgments earned a reward corresponding to the value of the coin, whereas incorrect judgments were penalized. No regions were identified where the magnitude of recollection effects was modulated by reward. Exclusive effects of source accuracy were evident in the hippocampus. Different striatal sub-regions demonstrated exclusive recollection effects, exclusive reward effects, and overlap between the 2 effects. The left angular gyrus and medial prefrontal cortex were additively responsive to source accuracy and the reward. The findings suggest that reward value and recollection success are conjointly but independently represented in at least 2 cortical regions and that striatal retrieval success effects cannot be accounted for in terms of a single construct, such as goal satisfaction.
Project description:We used event-related fMRI to investigate whether recollection- and familiarity-based memory judgments are modulated by the degree of visual similarity between old and new art paintings. Subjects performed a flower detection task, followed by a Remember/Know/New surprise memory test. The old paintings were randomly presented with new paintings, which were either visually similar or visually different. Consistent with our prediction, subjects were significantly faster and more accurate to reject new, visually different paintings than new, visually similar ones. The proportion of false alarms, namely remember and know responses to new paintings, was significantly reduced with decreased visual similarity. The retrieval task evoked activation in multiple visual, parietal and prefrontal regions, within which remember judgments elicited stronger activation than know judgments. New, visually different paintings evoked weaker activation than new, visually similar items in the intraparietal sulcus. Contrasting recollection with familiarity revealed activation predominantly within the precuneus, where the BOLD response elicited by recollection peaked significantly earlier than the BOLD response evoked by familiarity judgments. These findings suggest that successful memory retrieval of pictures is mediated by activation in a distributed cortical network, where memory strength is manifested by differential hemodynamic profiles. Recollection- and familiarity-based memory decisions may therefore reflect strong memories and weak memories, respectively.
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:People tend to show better memory for information that is deemed valuable or important. By one mechanism, individuals selectively engage deeper, semantic encoding strategies for high value items (Cohen, Rissman, Suthana, Castel, & Knowlton, 2014). By another mechanism, information paired with value or reward is automatically strengthened in memory via dopaminergic projections from midbrain to hippocampus (Shohamy & Adcock, 2010). We hypothesized that the latter mechanism would primarily enhance recollection-based memory, while the former mechanism would strengthen both recollection and familiarity. We also hypothesized that providing interspersed tests during study is a key to encouraging selective engagement of strategies. To test these hypotheses, we presented participants with sets of words, and each word was associated with a high or low point value. In some experiments, free recall tests were given after each list. In all experiments, a recognition test was administered 5 minutes after the final word list. Process dissociation was accomplished via remember/know judgments at recognition, a recall test probing both item memory and memory for a contextual detail (word plurality), and a task dissociation combining a recognition test for plurality (intended to probe recollection) with a speeded item recognition test (to probe familiarity). When recall tests were administered after study lists, high value strengthened both recollection and familiarity. When memory was not tested after each study list, but rather only at the end, value increased recollection but not familiarity. These dual process dissociations suggest that interspersed recall tests guide learners' use of metacognitive control to selectively apply effective encoding strategies. (PsycINFO Database Record
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.
Project description:We examined the effects of value on recognition by assessing its contribution to recollection and familiarity. In three experiments, participants studied English words, each associated with a point-value they would earn for correct recognition, with the goal of maximizing their score. In Experiment 1, participants provided Remember/Know judgments. In Experiment 2 participants indicated whether items were recollected or if not, their degree of familiarity along a 6-point scale. In Experiment 3, recognition of words was accompanied by a test of memory for incidental details. Across all experiments, participants were more likely to recognize items with higher point-value. Furthermore, value appeared to primarily enhance recollection, as effects on familiarity were small and not consistent across experiments. Recollection of high-value items appears to be accompanied by fewer incidental details, suggesting that value increases focus on items at the expense of irrelevant information.