Subsequent Memory Research Articles

Time after Time: Preserving Temporal Memories When Experiences Repeat.

Remembering when events occur in time is fundamental to episodic memory. Yet, many experiences repeat over time creating the potential for interference when attempting to recall temporally specific memories. Here, we argue that temporal memories are protected, in part, by reinstatement of temporal context information that is triggered by stimulus repetitions. We motivate this argument by integrating seminal findings across several distinct literatures and methodologies. Specifically, we consider key insights from foundational behavioral studies of temporal memory, recent electrophysiological and neuroimaging approaches to measuring memory reinstatement, and computational models that describe how temporal context representations shape memory processes. We also note several open questions concerning how temporal context reinstatement might influence subsequent temporal memory, including potential mediating effects of event spacing and event boundaries. These ideas and questions have the potential to guide future research and, ultimately, to advance theoretical accounts of how we preserve temporal memories.

Limited carry-over effects of socioemotional manipulations on subsequent unrelated memory tasks.

Although age is typically associated with significant impairments in memory performance, several domains exist in which these impairments are reduced or even eliminated. These "pockets of preservation" in older adults' memory can be seen in tasks involving socioemotional processing and may be supported by distinct encoding or retrieval modes relative to neutral content. The current study examines whether engaging in socioemotional tasks prior to encoding or retrieval allows older adults to enter an encoding or retrieval mode that better supports memory performance. In two online studies, adults across the lifespan were asked to complete a memory task where they incidentally encoded and retrieved neutral (Experiment 1, N = 1621) or emotional (Experiment 2, N = 409) word-image pairs. Participants were randomly assigned to a control (i.e., no manipulation), pre-encoding, or pre-retrieval socioemotional manipulation condition. There were no main effects of manipulation condition, suggesting that such manipulations may not reliably enhance memory. However, future research is needed to follow up on exploratory analyses that highlighted particular conditions under which these manipulations may convey benefits. There were also no age-by-manipulation interactions. While these null effects may suggest that these manipulations are not better suited to older adults, this may also be a result of the unexpected age-related increases (Experiment 1) and age invariance (Experiment 2) in overall memory accuracy in the current study. Socioemotional manipulations should also be examined in older adults who underperform younger adults.

A default mode network subsystem supports both item and associative word encoding: Insights from a meta-analysis

Abstract Recent meta-analytic evidence has underscored the significant role of the default mode network (DMN) in facilitating item word encoding. This study builds on this finding through a comprehensive meta-analysis of fMRI-based subsequent memory studies that use words as stimuli. The results highlight several key functions within the DMN. Firstly, the dorsomedial prefrontal cortex (dmPFC) subsystem of the DMN plays a pivotal role in enhancing successful word encoding, suggesting its vital involvement in the semantic processing of incoming verbal information. Secondly, the utility of the dmPFC subsystem extends beyond item word encoding to associative word encoding tasks, demonstrating its broad applicability in verbal information encoding. Thirdly, regions within the left inferior frontal cortex, a core component of the dmPFC subsystem, show increased activity during associative compared to item word encoding, emphasizing their role in integrating verbal information with contextual details. Contrary to previous research that linked the DMN with encoding interference—often attributed to the core subsystem’s tendency for mind-wandering—this study highlights the facilitative role of the dmPFC subsystem in memory encoding. The contrasting roles of the DMN subsystems, both interfering and facilitating, challenge traditional views and advocate for a more nuanced understanding of the network’s role in memory encoding.

Pattern separation during encoding and Subsequent Memory Effect

Memory retrieval has been extensively studied in relation to the encoding processes that precede access to stored information. Event related potentials (ERP) research has compared brain potentials elicited during the study phase of successful and unsuccessful retrieval, finding greater activation for the subsequent retrieval information. In this work we were interested in exploring the neural markers associated to subsequent recognition when similar memories are subsequently encoded. We used a Subsequent Memory paradigm in which we manipulated the number of similar items within a category (2 or 6) that participants encoded. Manipulating the number of similar encoded items within a category allowed us to test whether encoding markers of subsequent recognition depend solely on memory trace strength or, on the contrary, successful recognition is influenced by subsequently presented similar memories, and consequently may not be reflected in higher activation in such cases. After a 20-minute period, participants performed a recognition task providing one of a three-option judgement: “old”, “similar” and “new”, which allowed us to test if the amplitude of ERP waveforms varied based on the similarity judgement of the unrecognized encoded item. We did not observe a significant parietal subsequent memory effect, however, old hits and similar false alarms were both significantly different from similar correct rejections and old false alarms in ERP retrieval. These findings suggest that differences in brain responses between conditions are specifically related to the retrieval process and not the encoding process, indicating potential differential effects on memory during retrieval. Moreover, it is also possible that differences in brain responses develop or change over the rest time between phases, influencing how these conditions manifest across different stages of information processing.

Emotional future simulations: neural and cognitive perspectives.

LeDoux's work on the emotional brain has had broad impact in neuroscience and psychology. Here, we discuss an aspect of the emotional brain that we have examined in our laboratory during the past two decades: emotional future simulations or constructed mental representations of positive and negative future experiences. Specifically, we consider research concerning (i) neural correlates of emotional future simulations, (ii) how emotional future simulations impact subsequent cognition and memory, (iii) the role of emotional future simulations in worry and anxiety, and (iv) individual differences in emotional future simulation related to narcissistic grandiosity. The intersection of emotion and future simulation is closely linked to some of LeDoux's primary scientific concerns.

Long-term retention of real-world experiences in a patient with profound amnesia

The medial temporal lobe (MTL) is known to be critical for healthy memory function, but patients with MTL damage can, under certain circumstances, demonstrate successful learning of novel information encountered outside the laboratory. Here, we describe a patient, D.C., with extensive but focal bilateral MTL damage centering primarily on his hippocampus, whose memory for real-world experiences was assessed. Tests of remote memory indicated at least some capacity to retrieve specific details. To test his anterograde memory, he was taken on a tour of the NIH Clinical Center, with unique events occurring at each of ten specific locations. His memory for these events was tested after 1 h, and again after fifteen months. Initially, D.C. could not recall having participated in the tour, even when cued with photographs of specific places he had visited. However, he achieved 90% accuracy on a forced choice recognition test of old and new objects he encountered on the tour, and his recognition of these objects remained intact over a year later when he was tested once again. Subsequent recognition memory tests using novel picture stimuli in a standard laboratory-style computer task resulted in chance-level performance across multiple test formats and stimulus categories. These findings suggest a potentially privileged role for natural learning for long-term retention in a patient with severely damaged medial temporal lobes.

Transient susceptibility to interference at event boundaries impacts long-term memory of naturalistic episodes

ABSTRACT During ongoing narratives, event boundaries trigger processes relevant for subsequent memory. Previous work has shown that novel, unrelated input presented at an event boundary can retroactively interfere with short-term retention of the preceding event. This interference was attributed to a perturbation of offset-related processes taking place within seconds after encoding and supporting the binding of elements into a coherent event memory. However, the temporal specificity of this memory interference and whether its impact extends to longer retention delays has not been addressed. Here, participants viewed either individual or pairs of short narrative movie clips. Susceptibility to interference at event boundaries was probed by presenting the second clip either immediately after the first, or with a 2s encoding delay. In free and cued recall, after 20 min and 24 h, only memory for movie clips that were immediately followed by a second clip was reduced compared to clips shown in isolation. Intact offset-related processes (as indexed by successful recall of the first movie) did not negatively affect encoding of the subsequent clip. Together, these results indicate that the 2s time-window immediately after an event is relevant for successful consolidation and long-term retention of memory.

Polysomnographically mediated cognitive improvements in individuals with insomnia symptoms following continuous theta-burst stimulation of the default mode network

IntroductionInsomnia is associated with mild cognitive impairment, although the mechanisms of this impairment are not well-understood. Timing of slow-wave and rapid eye movement sleep may help explain cognitive impairments common in insomnia. This investigation aimed to determine whether cognitive changes following continuous theta-burst stimulation (cTBS) are attributable to active stimulation, polysomnographic parameters of sleep, or both.MethodData presented here are part of a pilot clinical trial aiming to treat insomnia by targeting a node in the default mode network using an inhibitory 40-s (cTBS). A double-blind counterbalanced sham-controlled crossover design was conducted. Participants (N = 20) served as their own controls on two separate in-laboratory visits—one with active cTBS and the other with sham cTBS. Each visit included cognitive assessments before and after stimulation and following a night of sleep in the lab monitored with polysomnography.ResultsSlow wave sleep duration influenced working memory in the active cTBS condition, with shorter duration predicting improvements in working memory post sleep (B = −0.003, p = 0.095). Onset latency to rapid eye movement sleep predicted subsequent working memory, regardless of treatment condition (B = −0.001, p = 0.040). Results suggest that changes in attention and processing speed were primarily due to slow wave sleep onset (B = −0.001, p = 0.017) and marginally predicted by slow wave sleep duration (B = 0.002, p = 0.081) and sleep efficiency (B = 0.006, p = 0.090).ConclusionsFindings emphasize the important role that timing of slow-wave and rapid eye movement sleep have on information processing. Future work using larger sample sizes and more stimulation sessions is needed to determine optimal interactions between timing and duration of slow wave and rapid eye movement throughout the sleep period.Clinical trial registrationThis study is registered on ClinicalTrials.gov (NCT04953559). https://clinicaltrials.gov/study/NCT04953559?locStr=Arizona&country=United%20States&state=Arizona&cond=insomnia&intr=tms%20&rank=1

Persistent activity during working memory maintenance predicts long-term memory formation in the human hippocampus.

Working memory (WM) and long-term memory (LTM) are often viewed as separate cognitive systems. Little is known about how these systems interact when forming memories. We recorded single neurons in the human medial temporal lobe while patients maintained novel items in WM and completed a subsequent recognition memory test for the same items. In the hippocampus, but not in the amygdala, the level of WM content-selective persistent activity during WM maintenance was predictive of whether the item was later recognized with high confidence or forgotten. By contrast, visually evoked activity in the same cells was not predictive of LTM formation. During LTM retrieval, memory-selective neurons responded more strongly to familiar stimuli for which persistent activity was high while they were maintained in WM. Our study suggests that hippocampal persistent activity of the same cells supports both WM maintenance and LTM encoding, thereby revealing a common single-neuron component of these two memory systems.

Radiosensitivity-related Variation in MicroRNA-34a-5p Levels and Subsequent Neuronal Loss in the Hilus of the Dentate Gyrus after Irradiation at Postnatal Days 10 and 21 in Mice.

The radiosensitivity of mice differs between postnatal days 10 (P10) and 21(P21); these days mark different stages of brain development. In the present study, Ki67 and doublecotin (DCX) immunostaining and hematoxylin staining was performed, which showed that acute radiation exposure at postnatal day 10 induced higher cell apoptosis and loss in the hilus of the dentate gyrus at day 1 postirradiation than postnatal day 21. MicroRNA (miRNA) sequencing and real-time quantitative reverse transcription PCR (qRT-PCR) analysis indicated the upregulation of miRNA-34a-5p at days 1 and 7 after irradiation at postnatal day 10, but not at postnatal day 21. Down-regulation of T-cell intracytoplasmic antigen-1 pathway (Tia1) was indicated by qRT-PCR at day 1 day but not day 7 after irradiation at postnatal day 10. Neurobehavioral testing in mature mice irradiated at postnatal day 10 demonstrated the impairment of short-term memory in novel object recognition and spatial memory, compared to those irradiated at postnatal day 21. Combined with our previous luciferase assay showing the direct interaction of miRNA34a-5p and Tia1, these findings suggest that radiation-induced abnormal miR-34a-5p/Tial interaction at day 1 after irradiation at postnatal day 10 may be involved in apoptosis of the dentate gyrus hilar, impairment of neurogenesis and subsequent short-term memory loss as observed in the novel object recognition and Barnes maze tests.

Predicting the effectiveness of binaural beats on working memory.

Working memory is vital for short-term information processing. Binaural beats can enhance working memory by improving attention and memory consolidation through neural synchronization. However, individual differences in cognitive and neuronal functioning affect effectiveness of binaural beats, necessitating personalized approaches. This study aimed to develop a machine learning model to predict binaural beats's effectiveness on working memory using electroencephalography. Sixty healthy participants underwent a 5-min electroencephalography recording, an initial working memory evaluation, 15 min of binaural beats stimulation, and a subsequent working memory evaluation using digit span tests of increasing difficulty. Recall accuracy and response times were measured. Differential scores from pre-evaluation and post-evaluation labeled participants as active or inactive to binaural beats stimulation. electroencephalography data, recorded using 14 electrodes, provided brain activity estimates across theta, alpha, beta, and gamma frequency bands, resulting in 56 features (14 channels × 4 bands) for the machine learning model. Several classifiers were tested to identify the most effective model. The weighted K-nearest neighbors model achieved the highest accuracy (90.0%) and area under the receiver operating characteristic curve (92.24%). Frontal and parietal electroencephalography channels in theta and alpha bands were crucial for classification. This study's findings offer significant clinical insights, enabling informed interventions and preventing resource inefficiency.

Rhythmic Temporal Cues Coordinate Cross-frequency Phase-amplitude Coupling during Memory Encoding.

Accumulating evidence suggests that rhythmic temporal cues in the environment influence the encoding of information into long-term memory. Here, we test the hypothesis that these mnemonic effects of rhythm reflect the coupling of high-frequency (gamma) oscillations to entrained lower-frequency oscillations synchronized to the beat of the rhythm. In Study 1, we first test this hypothesis in the context of global effects of rhythm on memory, when memory is superior for visual stimuli presented in rhythmic compared with arrhythmic patterns at encoding [Jones, A., & Ward, E. V. Rhythmic temporal structure at encoding enhances recognition memory, Journal of Cognitive Neuroscience, 31, 1549-1562, 2019]. We found that rhythmic presentation of visual stimuli during encoding was associated with greater phase-amplitude coupling (PAC) between entrained low-frequency (delta) oscillations and higher-frequency (gamma) oscillations. In Study 2, we next investigated cross-frequency PAC in the context of local effects of rhythm on memory encoding, when memory is superior for visual stimuli presented in-synchrony compared with out-of-synchrony with a background auditory beat (Hickey et al., 2020). We found that the mnemonic effect of rhythm in this context was again associated with increased cross-frequency PAC between entrained low-frequency (delta) oscillations and higher-frequency (gamma) oscillations. Furthermore, the magnitude of gamma power modulations positively scaled with the subsequent memory benefit for in- versus out-of-synchrony stimuli. Together, these results suggest that the influence of rhythm on memory encoding may reflect the temporal coordination of higher-frequency gamma activity by entrained low-frequency oscillations.

The impact of threat of shock on memory for threat-irrelevant information: Evidence for a role of reduced semantic organization

Research into the effects of acute anxiety on episodic memory has produced inconsistent findings, particularly for threat-neutral information. In two experiments, we tested the hypothesis that anxiety induced by threat of shock can interfere with the use of semantic-organizational processes that benefit memory. In Experiment 1, participants viewed and freely recalled two lists of semantically unrelated neutral words, one encoded in a threatening context (threat blocks) and one encoded without threat (safe blocks). As predicted, significantly fewer words were recalled during threat than safe blocks. Moreover, free recall patterns following threat blocks showed lower levels of semantic organization as assessed using a “path length” measurement that considers the semantic distance between pairs of consecutively recalled words. Both effects unexpectedly interacted with block order, such that they primarily reflected improved recall and increased semantic organization from the first to the second block in participants who received the threat block first. Experiment 2 used semantically related word lists to reduce potential impacts of task experience on semantic organization. Free recall was again less accurate and showed longer (less organized) path lengths for threat than safe blocks, and the path length effect no longer interacted with block order. Moreover, threat-induced changes to path lengths emerged as a mediator of the relation between physiological effects of threat (increased skin conductance) and reduced subsequent memory. These data point to semantic control processes as an understudied determinant of when and how acute anxiety impacts episodic memory.

Cortico-hippocampal interactions underlie schema-supported memory encoding in older adults.

Although episodic memory is typically impaired in older adults (OAs) compared to young adults (YAs), this deficit is attenuated when OAs can leverage their rich semantic knowledge, such as their knowledge of schemas. Memory is better for items consistent with pre-existing schemas and this effect is larger in OAs. Neuroimaging studies have associated schema use with the ventromedial prefrontal cortex (vmPFC) and hippocampus (HPC), but most of this research has been limited to YAs. This fMRI study investigated the neural mechanisms underlying how schemas boost episodic memory in OAs. Participants encoded scene-object pairs with varying congruency, and memory for the objects was tested the following day. Congruency with schemas enhanced object memory for YAs and, more substantially, for OAs. FMRI analyses examined how cortical modulation of HPC predicted subsequent memory. Congruency-related vmPFC modulation of left HPC enhanced subsequent memory in both age groups, while congruency-related modulation from angular gyrus (AG) boosted subsequent memory only in OAs. Individual differences in cortico-hippocampal modulations indicated that OAs preferentially used their semantic knowledge to facilitate encoding via an AG-HPC interaction, suggesting a compensatory mechanism. Collectively, our findings illustrate age-related differences in how schemas influence episodic memory encoding via distinct routes of cortico-hippocampal interactions.

Microglia mediate memory dysfunction via excitatory synaptic elimination in a fracture surgery mouse model

Cognitive impairment is a common issue among human patients undergoing surgery, yet the neural mechanism causing this impairment remains unidentified. Surgical procedures often lead to glial cell activation and neuronal hypoexcitability, both of which are known to contribute to postoperative cognitive dysfunction (POCD). However, the role of neuron-glia crosstalk in the pathology of POCD is still unclear. Through integrated transcriptomics and proteomics analyses, we found that the complement cascades and microglial phagocytotic signaling pathways are activated in a mouse model of POCD. Following surgery, there is a significant increase in the presence of complement C3, but not C1q, in conjunction with presynaptic elements. This triggers a reduction in excitatory synapses, a decline in excitatory synaptic transmission, and subsequent memory deficits in the mouse model. By genetically knockout out C3ar1 or inhibiting p-STAT3 signaling, we successfully prevented neuronal hypoexcitability and alleviated cognitive impairment in the mouse model. Therefore, targeting the C3aR and downstream p-STAT3 signaling pathways could serve as potential therapeutic approaches for mitigating POCD.

Imitation-inhibition training can reduce the observation-inflation effect in face-to-face scenarios.

Observing others performing an action can lead to false memories of self-performance-the observation-inflation effect. Previous research has indicated that this phenomenon might impact the memory of actions in real-world interactions. However, whether direct observation without interaction can lead to observation inflation remains unclear. In Experiment 1, participants passively observed the experimenter performing actions live. In subsequent memory tests, they indeed reported false memories regarding their performances. Building on this, Experiment 2 investigated the causes of the observation-inflation effect induced by "real" actions. Participants underwent imitation-inhibition training with the individuals they observed previously. The results revealed that participants who completed imitation-inhibition training reported fewer false memories in memory tests than those who completed imitation training. These findings suggest that even passive observation of "real" actions can lead to observation inflation, and the simulation of others' actions by individuals may be a potential underlying cause of their occurrence in real-life situations.

Offline hippocampal reactivation during dentate spikes supports flexible memory.

Stabilizing new memories requires coordinated neuronal spiking activity during sleep. Hippocampal sharp-wave ripples (SWRs) in the cornu ammonis (CA) region and dentate spikes (DSs) in the dentate gyrus (DG) are prime candidate network events for supporting this offline process. SWRs have been studied extensively, but the contribution of DSs remains unclear. By combining triple-ensemble (DG-CA3-CA1) recordings and closed-loop optogenetics in mice, we show that, like SWRs, DSs synchronize spiking across DG and CA principal cells to reactivate population-level patterns of neuronal coactivity expressed during prior waking experience. Notably, the population coactivity structure in DSs is more diverse and higher dimensional than that seen during SWRs. Importantly, suppressing DG granule cell spiking selectively during DSs impairs subsequent flexible memory performance during multi-object recognition tasks and associated hippocampal patterns of neuronal coactivity. We conclude that DSs constitute a second offline network event central to hippocampal population dynamics serving memory-guided behavior.

Correcting fake news headlines after repeated exposure: memory and belief accuracy in younger and older adults

The efficacy of fake news corrections in improving memory and belief accuracy may depend on how often adults see false information before it is corrected. Two experiments tested the competing predictions that repeating fake news before corrections will either impair or improve memory and belief accuracy. These experiments also examined whether fake news exposure effects would differ for younger and older adults due to age-related differences in the recollection of contextual details. Younger and older adults read real and fake news headlines that appeared once or thrice. Next, they identified fake news corrections among real news headlines. Later, recognition and cued recall tests assessed memory for real news, fake news, if corrections occurred, and beliefs in retrieved details. Repeating fake news increased detection and remembering of corrections, correct real news retrieval, and erroneous fake news retrieval. No age differences emerged for detection of corrections, but younger adults remembered corrections better than older adults. At test, correct fake news retrieval for earlier-detected corrections was associated with better real news retrieval. This benefit did not differ between age groups in recognition but was greater for younger than older adults in cued recall. When detected corrections were not remembered at test, repeated fake news increased memory errors. Overall, both age groups believed correctly retrieved real news more than erroneously retrieved fake news to a similar degree. These findings suggest that fake news repetition effects on subsequent memory accuracy depended on age differences in recollection-based retrieval of fake news and that it was corrected.

Reduced expression of fMRI subsequent memory effects with increasing severity across the Alzheimer’s disease risk spectrum

Abstract In functional magnetic resonance imaging (fMRI) studies, episodic memory is commonly investigated with the subsequent memory paradigm in which brain activity is recorded during encoding and analyzed as a function of subsequent remembering and forgetting. Impaired episodic memory is common in individuals with or at risk for Alzheimer’s disease (AD), but only few studies have reported subsequent memory effects in AD or its risk states like mild cognitive impairment (MCI). One reason for this might be that subsequent memory responses may be blunted in AD or MCI and thus less likely to manifest in fMRI signal differences. Here, we used Bayesian model selection of single-subject fMRI general linear models (GLMs) for a visual novelty and memory encoding experiment to compare the model performance of categorical and parametric subsequent memory models as well as memory-invariant models in a clinical cohort (N = 468) comprising healthy controls (HC) as well as individuals with subjective cognitive decline (SCD), MCI, and AD, plus healthy relatives of AD patients (AD-rel). We could replicate the previously reported superiority of parametric subsequent memory models over categorical models (Soch, Richter, Schütze, Kizilirmak, Assmann, Knopf, et al., 2021) in the HC and also in the SCD and AD-rel groups. However, memory-invariant models outperformed any model assuming subsequent memory effects in the MCI and AD groups. In the AD group, we additionally found substantially lower model preference for models assuming novelty compared to models not differentiating between novel and familiar stimuli. Our results suggest that voxel-wise memory-related fMRI activity patterns in AD and also MCI should be interpreted with caution and point to the need for additional or alternative approaches to investigate memory function.

Subsequent Memory Effects in Cortical Pattern Similarity Differ by Semantic Class.

Although living and nonliving stimuli are known to rely on distinct brain regions during perception, it is largely unknown if their episodic memory encoding mechanisms differ as well. To investigate this issue, we asked participants to encode object pictures (e.g., a picture of a tiger) and to retrieve them later in response to their names (e.g., word "tiger"). For each of four semantic classes (living-animate, living-inanimate, nonliving-large, and nonliving-small), we examined differences in the similarity in activation patterns (neural pattern similarity [NPS]) for subsequently remembered versus forgotten items. Higher NPS for remembered items suggests an advantage of within-class item similarity, whereas lower NPS for remembered items indicates an advantage for item distinctiveness. We expect NPS within class-specific regions to be higher for remembered than for forgotten items. For example, the parahippocampal cortex has a well-known role in scene processing [Aminoff, E. M., Kveraga, K., & Bar, M. The role of the parahippocampal cortex in cognition. Trends in Cognitive Sciences, 17, 379-390, 2013], and the anterior temporal and inferior frontal gyrus have well-known roles in object processing [Clarke, A., & Tyler, L. K. Object-specific semantic coding in human perirhinal cortex. Journal of Neuroscience, 34, 4766-4775, 2014]. As such, we expect to see higher NPS for remembered items in these regions pertaining to scenes and objects, respectively. Consistent with this hypothesis, in fusiform, parahippocampal, and retrosplenial regions, higher NPS predicted memory for subclasses of nonliving objects, whereas in the left inferior frontal and left retrosplenial regions, lower NPS predicted memory for subclasses of living objects. Taken together, the results support the idea that subsequent memory depends on a balance of similarity and distinctiveness and demonstrate that the neural mechanisms of episodic encoding differ across semantic categories.