Hippocampal activity predicts contextual misattribution of false memories.

Failure of contextual retrieval can lead to false recall, wherein people retrieve an item or experience that occurred in a different context or did not occur at all. Whereas the hippocampus is thought to play a crucial role in memory retrieval, we lack understanding of how the hippocampus supports retrieval of items related to a target context while disregarding related but irrelevant information. Using direct electrical recordings from the human hippocampus, we investigate the neural process underlying contextual misattribution of false memories. In two large datasets, we characterize key physiological differences between correct and false recalls that emerge immediately prior to vocalization. By differentiating between false recalls that share high or low contextual similarity with the target context, we show that low-frequency activity (6 to 18 Hz) in the hippocampus tracks similarity between the current and retrieved context. Applying multivariate decoding methods, we were able to reliably predict the contextual source of the to-be-recalled item. Our findings elucidate one of the hallmark features of episodic memory: our ability to distinguish between memories that were formed on different occasions.

Temporal organization of narrative recall is present but attenuated in adults with hippocampal amnesia.

Studies of the impact of brain injury on memory processes often focus on the quantity and episodic richness of those recollections. Here, we argue that the organization of one's recollections offers critical insights into the impact of brain injury on functional memory. It is well-established in studies of word list memory that free recall of unrelated words exhibits a clear temporal organization. This temporal contiguity effect refers to the fact that the order in which word lists are recalled reflects the original presentation order. Little is known, however, about the organization of recall for semantically rich materials, nor how recall organization is impacted by hippocampal damage and memory impairment. The present research is the first study, to our knowledge, of temporal organization in semantically rich narratives in three groups: (1) Adults with bilateral hippocampal damage and severe declarative memory impairment, (2) adults with bilateral ventromedial prefrontal cortex (vmPFC) damage and no memory impairment, and (3) demographically matched non-brain-injured comparison participants. We find that although the narrative recall of adults with bilateral hippocampal damage reflected the temporal order in which those narratives were experienced above chance levels, their temporal contiguity effect was significantly attenuated relative to comparison groups. In contrast, individuals with vmPFC damage did not differ from non-brain-injured comparison participants in temporal contiguity. This pattern of group differences yields insights into the cognitive and neural systems that support the use of temporal organization in recall. These data provide evidence that the retrieval of temporal context in narrative recall is hippocampal-dependent, whereas damage to the vmPFC does not impair the temporal organization of narrative recall. This evidence of limited but demonstrable organization of memory in participants with hippocampal damage and amnesia speaks to the power of narrative structures in supporting meaningfully organized recall despite memory impairment.

Improving Memory Search Through Model-Based Cue Selection.

We often use cues from our environment when we get stuck searching our memories, but prior research has failed to show benefits of cuing with other, randomly selected list items during memory search. What accounts for this discrepancy? We proposed that cues' content critically determines their effectiveness and sought to select the right cues by building a computational model of how cues affect memory search. Participants (N = 195 young adults from the United States) recalled significantly more items when receiving our model's best (vs. worst) cue. Our model provides an account of why some cues better aid recall: Effective cues activate contexts most similar to the remaining items' contexts, facilitating recall in an unsearched area of memory. We discuss our contributions in relation to prominent theories about the effect of external cues.

Direct brain recordings suggest a causal subsequent-memory effect.

Endogenous variation in brain state and stimulus-specific evoked activity can both contribute to successful encoding. Previous studies, however, have not clearly distinguished among these components. We address this question by analysing intracranial EEG recorded from epilepsy patients as they studied and subsequently recalled lists of words. We first trained classifiers to predict recall of either single items or entire lists and found that both classifiers exhibited similar performance. We found that list-level classifier output-a biomarker of successful encoding-tracked item presentation and recall events, despite having no information about the trial structure. Across widespread brain regions, decreased low- and increased high-frequency activity (HFA) marked successful encoding of both items and lists. We found regional differences in the hippocampus and prefrontal cortex, where in the hippocampus HFA correlated more strongly with item recall, whereas, in the prefrontal cortex, HFA correlated more strongly with list performance. Despite subtle differences in item- and list-level features, the similarity in overall classification performance, spectral signatures of successful recall and fluctuations of spectral activity across the encoding period argue for a shared endogenous process that causally impacts the brain's ability to learn new information.

The precuneus as a central node in declarative memory retrieval.

Both, the hippocampal formation and the neocortex are contributing to declarative memory, but their functional specialization remains unclear. We investigated the differential contribution of both memory systems during free recall of word lists. In total, 21 women and 17 men studied the same list but with the help of different encoding associations. Participants associated the words either sequentially with the previous word on the list, with spatial locations on a well-known path, or with unique autobiographical events. After intensive rehearsal, subjects recalled the words during functional magnetic resonance imaging (fMRI). Common activity to all three types of encoding associations was identified in the posterior parietal cortex, in particular in the precuneus. Additionally, when associating spatial or autobiographical material, retrosplenial cortex activity was elicited during word list recall, while hippocampal activity emerged only for autobiographically associated words. These findings support a general, critical function of the precuneus in episodic memory storage and retrieval. The encoding-retrieval repetitions during learning seem to have accelerated hippocampus-independence and lead to direct neocortical integration in the sequentially associated and spatially associated word list tasks. During recall of words associated with autobiographical memories, the hippocampus might add spatiotemporal information supporting detailed scenic and contextual memories.

Variability across subjects in free recall versus cued recall.

Memory scientists usually compare mean performance on some measure(s) (accuracy, confidence, latency) as a function of experimental condition. Some researchers have made within-subject variability in task performance a focal outcome measure (e.g., Yao et al., Journal of Clinical and Experimental Neuropsychology, 38, 227-237, 2016). Here, we explored between-subject variability in accuracy as a function of experimental conditions. This work was inspired by an incidental finding in a previous study, in which we observed greater variability in accuracy of memory performance on cued recall (CR) versus free recall (FR) of English animal/object nouns (Mah et al., Frontiers in Psychology, 14, 1146200, 2023). Here we report experiments designed to assess the reliability of that pattern and to explore its causes (e.g., differential interpretation of instructions, [un]relatedness of CR word pairs, encoding time). In Experiment 1 (N = 120 undergraduates), we replicated the CR:FR variability difference with a more representative set of English nouns. In Experiments 2A (N = 117 Prolific participants) and 2B (N = 127 undergraduates), we found that the CR:FR variability difference persisted in a forced-recall procedure. In Experiment 3 (N = 260 Prolific participants), we used meaningfully related word pairs and still found greater variability in CR than in FR performance. In Experiment 4 (N = 360 Prolific participants), we equated CR and FR study phases by having all participants study pairs and, again, observed greater variability in CR than FR. The same was true in Experiment 5 (N = 120 undergraduates), in which study time was self-paced. Comparisons of variability across subjects can yield insights into the mechanisms underlying task performance.

PEPPR: A post-encoding pre-production reinstatement model of dual-list free recall.

Recent events are easy to recall, but they also interfere with the recall of more distant, non-recent events. In many computational models, non-recent memories are recalled by using the context associated with those events as a cue. Some models, however, do little to explain how people initially activate non-recent contexts in the service of accurate recall. We addressed this limitation by evaluating two candidate mechanisms within the Context-Maintenance and Retrieval model. The first is a Backward-Walk mechanism that iteratively applies a generate/recognize process to covertly retrieve progressively less recent items. The second is a Post-Encoding Pre-Production Reinstatement (PEPPR) mechanism that formally implements a metacognitive control process that reinstates non-recent contexts prior to retrieval. Models including these mechanisms make divergent predictions about the dynamics of response production and monitoring when recalling non-recent items. Before producing non-recent items, Backward-Walk cues covert retrievals of several recent items, whereas PEPPR cues few, if any, covert retrievals of that sort. We tested these predictions using archival data from a dual-list externalized free recall paradigm that required subjects to report all items that came to mind while recalling from the non-recent list. Simulations showed that only the model including PEPPR accurately predicted covert recall patterns. That same model fit the behavioral data well. These findings suggest that self-initiated context reinstatement plays an important role in recall of non-recent memories and provides a formal model that uses a parsimonious non-hierarchical context representation of how such reinstatement might occur.

Effects of lexical skills and orthographic neighborhood size in word memory.

Two experiments were designed to investigate the relationship between individual lexical skills in young adults and memory performance on words varying by their orthographic neighborhood size. In Experiment 1, a sample of 100 university students were administrated a set of spelling, reading, and vocabulary tests to assess their lexical skills. Then, they had to learn mixed lists of words from high and low neighborhood size and perform free recall and memory recognition tasks. Importantly, high lexical skills were found to enhance free recall and, to a lesser extent, recognition. In addition, a typical mirror effect of neighborhood size was found in recognition as words were better recognized and also produced less false alarms when they had a low neighborhood size. In Experiment 2, pure lists of words were designed and a new sample of 90 university students was assessed. We replicated the effect of lexical skills in free recall and the effect of neighborhood size for hits in recognition. Spelling skills were found to interact with neighborhood size in free recall in that low spelling skills were associated with a facilitatory effect of neighborhood size. In recognition, a relation between reading skills and neighborhood size was found such that the higher the reading skills, the higher was the inhibitory effect of neighborhood size. These results provide new evidence of an influence of lexical skills in word memory performance and underline the role of orthographic neighborhood size in episodic memory tasks.

On the cost and benefits of restudying: exploring the list strength effect in self-guided learning.

Across five experiments we examined whether restudying a self-selected subset of items impairs memory for the remaining non-restudied items, and enhances memory for the restudied items. This question was inspired by research on the list strength effect, in which re-presentation of only a subset of items from a list impairs recall for items presented only once, and enhances memory for items presented twice. We found that following initial encoding of all items, honouring participants' restudy selections did indeed impair recall for the non-restudied items relative to when no items were restudied. Additionally, we found that memory for the subset of restudied items was enhanced relative to when all items were restudied. These findings expand previous research on the LSE to self-regulated learning and provide important new insights on how some learning strategies may in part be detrimental, but also beneficial, to future memory performance.

Free recall scaling laws and short-term memory effects in a latching attractor network.

Despite the complexity of human memory, paradigms like free recall have revealed robust qualitative and quantitative characteristics, such as power laws governing recall capacity. Although abstract random matrix models could explain such laws, the possibility of their implementation in large networks of interacting neurons has so far remained underexplored. We study an attractor network model of long-term memory endowed with firing rate adaptation and global inhibition. Under appropriate conditions, the transitioning behavior of the network from memory to memory is constrained by limit cycles that prevent the network from recalling all memories, with scaling similar to what has been found in experiments. When the model is supplemented with a heteroassociative learning rule, complementing the standard autoassociative learning rule, as well as short-term synaptic facilitation, our model reproduces other key findings in the free recall literature, namely, serial position effects, contiguity and forward asymmetry effects, and the semantic effects found to guide memory recall. The model is consistent with a broad series of manipulations aimed at gaining a better understanding of the variables that affect recall, such as the role of rehearsal, presentation rates, and continuous and/or end-of-list distractor conditions. We predict that recall capacity may be increased with the addition of small amounts of noise, for example, in the form of weak random stimuli during recall. Finally, we predict that, although the statistics of the encoded memories has a strong effect on the recall capacity, the power laws governing recall capacity may still be expected to hold.

The influence of emotion on temporal context models.

Temporal context models (TCMs) have been influential in understanding episodic memory and its neural underpinnings. Recently, TCMs have been extended to explain emotional memory effects, one of the most clinically important findings in the field of memory research. This review covers recent advances in hypotheses for the neural representation of spatiotemporal context through the lens of TCMs, including their ability to explain the influence of emotion on episodic and temporal memory. In recent years, simplifying assumptions of "classical" TCMs - with exponential trace decay and the mechanism by which temporal context is recovered - have become increasingly clear. The review also outlines how recent advances could be incorporated into a future TCM, beyond classical assumptions, to integrate emotional modulation.

A comment on the order of report in two-pair dichotic digit testing in children assessed for auditory processing.

OBJECTIVE: This clinical note aimed to 1) describe the order-of-report (OoR) strategies used by a large sample of children who completed 2pDD testing in the free-recall condition as part of an audiological assessment of auditory processing (AP), and 2) determine if use of OoR correlated with 2pDD test performance. DESIGN: A retrospective (case-review), single observation design. STUDY SAMPLE: A convenient sample of 77 children (50 males and 27 females aged 7.0 to 17.4 years [median = 8.8 years]) referred to audiology for an AP assessment. RESULTS: The participating children used temporal more than ear or sequential OoR and showed decreased test scores with increased use of ear OoR. CONCLUSIONS: These findings suggest children referred for an AP assessment could favour a temporal OoR when completing 2pDD testing for its opportunity to rehearse the first digit pair (possibly strengthening its memory trace) prior to processing the second digit pair, while their use of an ear OoR could come at the cost detrimental ear dominance effects that reduce their test performance. Future research could consider if similar results are observed in other child populations and if preferred dichotic processing strategy could inform auditory training for children with dichotic listening deficits.

The role of rehearsal and reminding in the recall of categorized word lists.

Most theories of free recall emphasize the importance of retrieval in explaining temporal and semantic regularities in recall; rehearsal mechanisms are often absent or limit rehearsal to a subset of what was last rehearsed. However, in three experiments using the overt rehearsal method, we show clear evidence that just-presented items act as retrieval cues during encoding (study-phase retrieval) with prior related items rehearsed despite well over a dozen intervening items. Experiment 1 examined free recall of categorized and uncategorized lists of 32 words. In Experiments 2 and 3, we presented categorized lists of 24, 48, and 64 words for free recall or cued recall, with the category exemplars blocked in successive list positions (Experiment 2) or randomized throughout the list (Experiment 3). The probability of rehearsing a prior word was affected by its semantic similarity to the just-presented item, and the frequency and recency of its prior rehearsals. These rehearsal data suggest alternative interpretations to well-known recall phenomena. With randomized designs, the serial position curves were reinterpreted by when words were last rehearsed (which contributed to the list length effects), and semantic clustering and temporal contiguity effects at output were reinterpreted by whether words were co-rehearsed during study. The contrast with the blocked designs suggests that recall is sensitive to the relative (not absolute) recency of targeted list items. We discuss the benefits of incorporating rehearsal machinery into computational models of episodic memory, and suggest that the same retrieval processes that generate the recalls are used to generate the rehearsals.

Survival processing advantage demonstrated with virtual reality-based survival environment: A promising tool for survival processing research.

Many studies have been conducted to demonstrate the survival processing advantage (SPA) as an evolutionary-oriented memory effect. But few studies were conducted to demonstrate this effect in real-life or simulated survival environments. This study tested whether the SPA could be replicated in a survival virtual reality environment (VRE). In Experiment 1, the SPAs were measured in VREs (survival grasslands, survival battlefield, nonsurvival moving) in which Experiment 1A used the standard long instructions and Experiment 1B used the modified short instructions. In Experiment 2, the SPAs were measured again with the scenarios corresponding to the VREs used in Experiment 1A. All experiments demonstrated typical SPAs, suggesting that the survival VRE is a reliable tool in designing and delivering a survival situation. The potential problems of applying survival VRE to survival processing research are discussed at the end.

Adult age differences in subjective context retrieval in dual-list free recall.

Age-related episodic memory deficits imply that older and younger adults differentially retrieve and monitor contextual features that indicate the source of studied information. Such differences have been shown in subjective reports during recognition and cued recall as well as process estimates derived from computational models of free recall organisation. The present study extends the subject report method to free recall to characterise age differences in context retrieval and monitoring, and to test assumptions from a context-based computational model. Older and younger adults studied two lists of semantically related words and then recalled from only the first or second list. After each recall, participants indicated their subjective context retrieval using remember/know judgments. Compared to younger adults, older adults showed lower recall accuracy and subjective reports of context retrieval (i.e., remember judgments) that were less specific to correct recalls. These differences appeared after first-recall attempts. Recall functions conditioned on serial positions were more continual across correct recalls from target lists and intrusions from non-target lists for older than younger adults. Together with other analyses of context retrieval and monitoring reported here, these findings suggest that older adults retrieved context less distinctively across the recall period, leading to greater perceived similarity for temporally contiguous lists.

Great minds think alike: New measures to quantify the similarity of recalls.

Given the recent interest in how memory operates in social contexts, it is more important than ever to meaningfully measure the similarity between recall sequences of different individuals. Similarity of recall sequences of different individuals has been quantified using primarily order-agnostic and some order-sensitive measures specific to memory research without agreement on any one preferred measure. However, edit distance measures have not been used to quantify the similarity of recall sequences in collaborative memory studies. In the current study, we review a broad range of similarity measures, highlighting commonalities and differences. Using simulations and behavioral data, we show that edit distances do measure a memory-relevant factor of similarity and capture information distinct from that captured by order-agnostic measures. We answer illustrative research questions which demonstrate potential applications of edit distances in collaborative and individual memory settings and reveal the unique impact collaboration has on similarity.

Face-Selective Units in Human Ventral Temporal Cortex Reactivate during Free Recall.

Research in functional neuroimaging has suggested that category-selective regions of visual cortex, including the ventral temporal cortex (VTC), can be reactivated endogenously through imagery and recall. Face representation in the monkey face-patch system has been well studied and is an attractive domain in which to explore these processes in humans. The VTCs of 8 human subjects (4 female) undergoing invasive monitoring for epilepsy surgery were implanted with microelectrodes. Most (26 of 33) category-selective units showed specificity for face stimuli. Different face exemplars evoked consistent and discriminable responses in the population of units sampled. During free recall, face-selective units preferentially reactivated in the absence of visual stimulation during a 2 s window preceding face recall events. Furthermore, we show that in at least 1 subject, the identity of the recalled face could be predicted by comparing activity preceding recall events to activity evoked by visual stimulation. We show that face-selective units in the human VTC are reactivated endogenously, and present initial evidence that consistent representations of individual face exemplars are specifically reactivated in this manner.SIGNIFICANCE STATEMENT The role of "top-down" endogenous reactivation of native representations in higher sensory areas is poorly understood in humans. We conducted the first detailed single-unit survey of ventral temporal cortex (VTC) in human subjects, showing that, similarly to nonhuman primates, humans encode different faces using different rate codes. Then, we demonstrated that, when subjects recalled and imagined a given face, VTC neurons reactivated with the same rate codes as when subjects initially viewed that face. This suggests that the VTC units not only carry durable representations of faces, but that those representations can be endogenously reactivated via "top-down" mechanisms.

Accelerated long-term forgetting in adult patients with genetic generalized epilepsy.

OBJECTIVE: Accelerated long-term forgetting (ALF) has been demonstrated among children but not adults with genetic generalized epilepsy (GGE). We investigated (1) how forgetting patterns of verbal and visuospatial material differ between patients with GGE and healthy controls (HCs) and (2) whether ALF is associated with ictal or interictal epileptic activity. METHODS: Forty-two patients with GGE (39, 92.9% experiencing seizures) were compared to 57 HCs in word, logical story, and Rey-Osterrieth complex figure recall tasks by testing after intervals of 30 min and 4 weeks. Ambulatory electroencephalography (EEG) was performed before testing to detect generalized epileptic activity, and patients were asked to document the number of seizures during the 4-week interval. RESULTS: A two-way repeated measures ANOVA indicated that individuals with GGE have different forgetting patterns in comparison to HCs in tasks of word (delay by group interaction F1.5, 142.5  = 4.5, p = .02, ηp2  = .04) and figure (F2, 194  = 15.9, p < .001, ηp2  = .14) but not story (F1.6 151.1  = .5, p = .58, ηp2  = .005) recall. Last learning trial-adjusted scores of word recall were comparable between HCs and patients with epilepsy (PWEs) at 30 min (p = .21) but not at 4 weeks (p = .006). Individuals with GGE performed worse than HCs in figure recall at 30 min and 4 weeks (p < .001), with lower performance after the 4-week interval present only among seizure-positive and EEG-positive individuals (p < .001) during subgroup analysis. Performance on memory tests was unrelated to overall seizure frequency, the number of antiseizure drugs used, and epilepsy duration. SIGNIFICANCE: Our study supports the presence of ALF in a task of word recall among adult patients with GGE. The pattern of forgetting visuospatial information suggests greater forgetting of material before the first delay and ongoing deficits among PWEs with epileptic activity. Future studies should confirm our findings and investigate the functional or pathological mechanisms of memory dysfunction in GGE.

Enhancing memory using enactment: does meaning matter in action production?

ABSTRACTEnactment is an encoding strategy in which performing an action related to a target item enhances memory for that word, relative to verbal encoding. Precisely how this motor activity aids recall is unclear. We examined whether the action created during encoding needed to be semantically relevant to the to-be-remembered word, to enhance memory. In Experiment 1, participants were asked to either (a) enact, (b) perform unrelated motoric gestures, or (c) read forty-five action verbs. On a subsequent free-recall test, memory for enacted words was significantly higher relative to words read, or encoded with unrelated gestures. In Experiment 2, to reduce the ambiguity associated with initiating an unrelated gesture, participants were instructed to write target words in the air. Results were similar to Experiment 1. In Experiment 3, we replicated the results of Experiment 2 using video conferencing to record the onset time of action initiation for enacted, unrelated gesture, and read trials. Results showed that planning of meaningful actions may also contribute to the memory performance as evidenced by a longer onset time to initiate an action on enactment relative to gesturing and reading trials. These findings suggest that planning and executing meaningful actions drive the enactment benefit.

Do Mandatory Health Warning Labels on Consumer Products Increase Recall of the Health Risks of Cannabis?

INTRODUCTION: Warning labels are an important source of health information. This study examined awareness of health warnings on cannabis packages over time in Canada-where large rotating messages are mandated-versus US states with legal adult-use cannabis, which have less comprehensive regulations. METHODS: Repeat cross-sectional data were collected from the International Cannabis Policy Study online surveys among past 12-month cannabis consumers in Canada and the US (n = 38,448). Free recall of warning messages was assessed in 2018-2020, followed by a prompted recognition task (2020 only). Adjusted logistic regression models tested differences in free recall and recognition of warnings between Canada and US states with and without legal adult-use cannabis ("legal" and "illegal" states, respectively). RESULTS: Free recall of ≥1 warning increased to a greater extent in Canada from 2018 (5%; pre-legalization) to 2019 (13%; post-legalization) compared to US "legal" (AOR = 1.93, p < 0.001) and "illegal" states (AOR = 1.80, p = 0.007), and from 2018 to 2020 (5% vs. 15%) compared to US "legal" states (AOR = 2.23, p = 0.027). In all jurisdictions, free recall of warnings was higher among more frequent consumers (p < 0.001) and those who purchased products from legal retail stores/websites (p < 0.001). With few exceptions, when a specific message was mandated (e.g., impaired driving), consumers were more likely to both freely recall and recognize that message (all p < 0.05). CONCLUSIONS: Cannabis legalization is associated with greater recall of health warning messages. Awareness of specific warning messages was higher in jurisdictions where the associated warning was mandated on packages, suggesting that warning labels may improve knowledge of cannabis-related health risks.Supplemental data for this article is available online at.