How We Transmit Memories to Other Brains: Constructing Shared Neural Representations Via Communication.

Humans are able to mentally construct an episode when listening to another person's recollection, even though they themselves did not experience the events. However, it is unknown how strongly the neural patterns elicited by mental construction resemble those found in the brain of the individual who experienced the original events. Using fMRI and a verbal communication task, we traced how neural patterns associated with viewing specific scenes in a movie are encoded, recalled, and then transferred to a group of naïve listeners. By comparing neural patterns across the 3 conditions, we report, for the first time, that event-specific neural patterns observed in the default mode network are shared across the encoding, recall, and construction of the same real-life episode. This study uncovers the intimate correspondences between memory encoding and event construction, and highlights the essential role our common language plays in the process of transmitting one's memories to other brains.

Accessing Real-Life Episodic Information from Minutes versus Hours Earlier Modulates Hippocampal and High-Order Cortical Dynamics.

It is well known that formation of new episodic memories depends on hippocampus, but in real-life settings (e.g., conversation), hippocampal amnesics can utilize information from several minutes earlier. What neural systems outside hippocampus might support this minutes-long retention? In this study, subjects viewed an audiovisual movie continuously for 25 min; another group viewed the movie in 2 parts separated by a 1-day delay. Understanding Part 2 depended on retrieving information from Part 1, and thus hippocampus was required in the day-delay condition. But is hippocampus equally recruited to access the same information from minutes earlier? We show that accessing memories from a few minutes prior elicited less interaction between hippocampus and default mode network (DMN) cortical regions than accessing day-old memories of identical events, suggesting that recent information was available with less reliance on hippocampal retrieval. Moreover, the 2 groups evinced reliable but distinct DMN activity timecourses, reflecting differences in information carried in these regions when Part 1 was recent versus distant. The timecourses converged after 4 min, suggesting a time frame over which the continuous-viewing group may have relied less on hippocampal retrieval. We propose that cortical default mode regions can intrinsically retain real-life episodic information for several minutes.

Neural Differentiation Tracks Improved Recall of Competing Memories Following Interleaved Study and Retrieval Practice.

Selective retrieval of overlapping memories can generate competition. How does the brain adaptively resolve this competition? One possibility is that competing memories are inhibited; in support of this view, numerous studies have found that selective retrieval leads to forgetting of memories that are related to the just-retrieved memory. However, this retrieval-induced forgetting (RIF) effect can be eliminated or even reversed if participants are given opportunities to restudy the materials between retrieval attempts. Here, we outline an explanation for such a reversal, rooted in a neural network model of RIF that predicts representational differentiation when restudy is interleaved with selective retrieval. To test this hypothesis, we measured changes in pattern similarity of the BOLD fMRI signal elicited by related memories after undergoing interleaved competitive retrieval and restudy. Reduced pattern similarity within the hippocampus positively correlated with retrieval-induced facilitation of competing memories. This result is consistent with an adaptive differentiation process that allows individuals to learn to distinguish between once-confusable memories.

Can cognitive neuroscience illuminate the nature of traumatic childhood memories?

Recent findings from cognitive neuroscience and cognitive psychology may help explain why recovered memories of trauma are sometimes illusory. In particular, the notion of defective source monitoring has been used to explain a wide range of recently established memory distortions and illusions. Conversely, the results of a number of studies may potentially be relevant to forgetting and recovery of accurate memories, including studies demonstrating reduced hippocampal volume in survivors of sexual abuse, and recovery from functional and organic retrograde amnesia. Other recent findings of interest include the possibility that state-dependent memory could be induced by stress-related hormones, new pharmacological models of dissociative states, and evidence for 'repression' in patients with right parietal brain damage.

False memories and aging.

Although memory processes and systems usually operate reliably, they are sometimes prone to distortions and illusions. Here we review evidence indicating that cognitive aging is often associated with increased susceptibility to various kinds of false recollections. Accumulating data indicate that older adults frequently have special difficulties recollecting the source of information, which in turn renders them vulnerable to confusing perceived and imagined experiences, and to related kinds of memory distortions. Evidence from studies of false recall and recognition indicate that older adults are sometimes more likely than younger adults to remember events that never happened, reflecting the influence of indistinct encoding of events and the use of lenient criteria during retrieval. Neuroimaging studies suggest that age-related changes in medial temporal and frontal regions may play a role in the altered functioning of specific encoding and retrieval processes that give rise to memory distortions. Future studies of aging and false memories are likely to provide a promising avenue for illuminating basic mechanisms of memory distortion.

False recognition after a right frontal lobe infarction: memory for general and specific information.

We previously reported a case study of a man with right frontal lobe damage, BG, who showed extraordinarily high false alarm rates on remember-know recognition tests (Schacter, D. L. et al., Neuropsychologia, 1996, Vol. 34, pp. 793-808). Experiment 1 extends his high false alarm rate to yes-no recognition tests. BG typically gives false 'remember' responses on remember-know tests, and this pattern was uninfluenced when he was asked to explain the basis for his 'remember' responses (Experiments 2 and 3). When BG was given a semantic encoding task, he stopped giving 'remember'-based false alarms (Experiment 4). Signal detection analyses revealed that BG had a discrimination deficit and an abnormally liberal response bias (especially for 'remember' responses) in most conditions. Overall, BG's high false alarm rate is interpreted as reflecting an over-reliance on the general similarity between a test item and the study episode.

False recognition in younger and older adults: exploring the characteristics of illusory memories.

Roediger and McDermott (1995) demonstrated that when subjects hear a list of associates to a "theme word" that has itself not been presented, they frequently claim to recollect having heard the nonpresented theme word on the study list. In Experiment 1, we found that asking subjects to explain their remember responses, by writing down exactly what they remembered about the item's presentation at study, did not significantly diminish the rate of remember false alarms to nonpresented theme words. We also found that older adults were relatively more susceptible than younger adults to this false-recognition effect. Subjects' explanations suggested that both veridical and illusory memories were predominantly composed of associative information as opposed to sensory and contextual detail. In Experiment 2, we obtained quantitative evidence for this conclusion, using a paradigm in which subjects were asked focused questions about the contents of their recollective experience. Lastly, we found that both younger and older adults recalled more sensory and contextual detail in conjunction with studied items than with nonpresented theme words, although these differences were less pronounced in older adults.

The cognitive neuroscience of constructive memory.

Numerous empirical and theoretical observations point to the constructive nature of human memory. This paper reviews contemporary research pertaining to two major types of memory distortions that illustrate such constructive processes: (a) false recognition and (b) intrusions and confabulations. A general integrative framework that outlines the types of problems that the human memory system must solve in order to produce mainly accurate representations of past experience is first described. This constructive memory framework (CMF) emphasizes processes that operate at encoding (initially binding distributed features of an episode together as a coherent trace; ensuring sufficient pattern separation of similar episodes) and also at retrieval (formation of a sufficiently focused retrieval description with which to query memory; postretrieval monitoring and verification). The framework is applied to findings from four different areas of research: cognitive studies of young adults, neuropsychological investigations of brain-damaged patients, neuroimaging studies, and studies of cognitive aging.

Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans?

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.

Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition.

Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced-choice recognition of both intra-item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter-item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra-item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined.