Eye tracking evidence for the reinstatement of emotionally negative and neutral memories.

Recent eye tracking studies have linked gaze reinstatement-when eye movements from encoding are reinstated during retrieval-with memory performance. In this study, we investigated whether gaze reinstatement is influenced by the affective salience of information stored in memory, using an adaptation of the emotion-induced memory trade-off paradigm. Participants learned word-scene pairs, where scenes were composed of negative or neutral objects located on the left or right side of neutral backgrounds. This allowed us to measure gaze reinstatement during scene memory tests based on whether people looked at the side of the screen where the object had been located. Across two experiments, we behaviorally replicated the emotion-induced memory trade-off effect, in that negative object memory was better than neutral object memory at the expense of background memory. Furthermore, we found evidence that gaze reinstatement was related to recognition memory for the object and background scene components. This effect was generally comparable for negative and neutral memories, although the effects of valence varied somewhat between the two experiments. Together, these findings suggest that gaze reinstatement occurs independently of the processes contributing to the emotion-induced memory trade-off effect.

Intrinsic functional connectivity among memory networks does not predict individual differences in narrative recall.

Individuals differ greatly in their ability to remember the details of past events, yet little is known about the brain processes that explain such individual differences in a healthy young population. Previous research suggests that episodic memory relies on functional communication among ventral regions of the default mode network ("DMN-C") that are strongly interconnected with the medial temporal lobes. In this study, we investigated whether the intrinsic functional connectivity of the DMN-C subnetwork is related to individual differences in memory ability, examining this relationship across 243 individuals (ages 18-50 years) from the openly available Cambridge Center for Aging and Neuroscience (Cam-CAN) dataset. We first estimated each participant's whole-brain intrinsic functional brain connectivity by combining data from resting-state, movie-watching, and sensorimotor task scans to increase statistical power. We then examined whether intrinsic functional connectivity predicted performance on a narrative recall task. We found no evidence that functional connectivity of the DMN-C, with itself, with other related DMN subnetworks, or with the rest of the brain, was related to narrative recall. Exploratory connectome-based predictive modeling (CBPM) analyses of the entire connectome revealed a whole-brain multivariate pattern that predicted performance, although these changes were largely outside of known memory networks. These results add to emerging evidence suggesting that individual differences in memory cannot be easily explained by brain differences in areas typically associated with episodic memory function.

Hippocampal Functions Modulate Transfer-Appropriate Cortical Representations Supporting Subsequent Memory.

The hippocampus plays a central role as a coordinate system or index of information stored in neocortical loci. Nonetheless, it remains unclear how hippocampal processes integrate with cortical information to facilitate successful memory encoding. Thus, the goal of the current study was to identify specific hippocampal-cortical interactions that support object encoding. We collected fMRI data while 19 human participants (7 female and 12 male) encoded images of real-world objects and tested their memory for object concepts and image exemplars (i.e., conceptual and perceptual memory). Representational similarity analysis revealed robust representations of visual and semantic information in canonical visual (e.g., occipital cortex) and semantic (e.g., angular gyrus) regions in the cortex, but not in the hippocampus. Critically, hippocampal functions modulated the mnemonic impact of cortical representations that are most pertinent to future memory demands, or transfer-appropriate representations Subsequent perceptual memory was best predicted by the strength of visual representations in ventromedial occipital cortex in coordination with hippocampal activity and pattern information during encoding. In parallel, subsequent conceptual memory was best predicted by the strength of semantic representations in left inferior frontal gyrus and angular gyrus in coordination with either hippocampal activity or semantic representational strength during encoding. We found no evidence for transfer-incongruent hippocampal-cortical interactions supporting subsequent memory (i.e., no hippocampal interactions with cortical visual/semantic representations supported conceptual/perceptual memory). Collectively, these results suggest that diverse hippocampal functions flexibly modulate cortical representations of object properties to satisfy distinct future memory demands.Significance Statement The hippocampus is theorized to index pieces of information stored throughout the cortex to support episodic memory. Yet how hippocampal processes integrate with cortical representation of stimulus information remains unclear. Using fMRI, we examined various forms of hippocampal-cortical interactions during object encoding in relation to subsequent performance on conceptual and perceptual memory tests. Our results revealed novel hippocampal-cortical interactions that utilize semantic and visual representations in transfer-appropriate manners: conceptual memory supported by hippocampal modulation of frontoparietal semantic representations, and perceptual memory supported by hippocampal modulation of occipital visual representations. These findings provide important insights into the neural mechanisms underlying the formation of information-rich episodic memory and underscore the value of studying the flexible interplay between brain regions for complex cognition.

How list composition affects the emotional enhancement of memory in younger and older adults.

Young adults show an immediate emotional enhancement of memory (EEM) when emotional and non-emotional information are presented in mixed lists but not pure lists, but it is unclear whether older adults' memories also benefit from the cognitive factors producing the list-composition effect. The present study examined whether the list-composition effect extended to older adults (55+), testing the following alternatives: (1) younger and older adults could show the list-composition effect, (2) due to age-related decreases in cognitive resources, older adults may show weaker effects of list-composition, or (3) due to age-related positivity effects, older adults' list-composition effect may vary by valence. Results supported the first alternative: the list-composition effect occurred for older as well as younger adults, when testing memory for pictures (Experiment 1) or words (Experiment 2). In a third experiment, we explored whether mixing information at only encoding or retrieval (and blocking in the other phase) would suffice for the list composition effect to occur. Results revealed that mixed encoding/blocked retrieval did not elicit the EEM in either age group. Overall, the results suggest age-related stability in the cognitive processes that give rise to the immediate EEM.

Integrating Region- and Network-level Contributions to Episodic Recollection Using Multilevel Structural Equation Modeling.

The brain is composed of networks of interacting brain regions that support higher-order cognition. Among these, a core network of regions has been associated with recollection and other forms of episodic construction. Past research has focused largely on the roles of individual brain regions in recollection or on their mutual engagement as part of an integrated network. However, the relationship between these region- and network-level contributions remains poorly understood. Here, we applied multilevel structural equation modeling to examine the functional organization of the posterior medial (PM) network and its relationship to episodic memory outcomes. We evaluated two aspects of functional heterogeneity in the PM network: first, the organization of individual regions into subnetworks, and second, the presence of regionally specific contributions while accounting for network-level effects. Our results suggest that the PM network is composed of ventral and dorsal subnetworks, with the ventral subnetwork making a unique contribution to recollection, especially to recollection of spatial information, and that memory-related activity in individual regions is well accounted for by these network-level effects. These findings highlight the importance of considering the functions of individual brain regions within the context of their affiliated networks.

Summary metrics of memory subnetwork functional connectivity alterations in multiple sclerosis.

BACKGROUND: Memory dysfunction is common in multiple sclerosis (MS); mechanistic understanding of its causes is lacking. Large-scale network resting-state functional connectivity (RSFC) is sensitive to memory dysfunction. OBJECTIVE: We derived and tested summary metrics of memory network RSFC. METHODS: Cognitive data and 3T magnetic resonance imaging (MRI) scans were collected from 235 MS patients and 35 healthy controls (HCs). Index scores were calculated as RSFC within (anteriority index, AntI) and between (integration index, IntI) dorsomedial anterior temporal and medial temporal memory subnetworks. Group differences in index expression were evaluated. Associations between index scores and memory/non-memory cognition were evaluated; relationships between T2 lesion volume (T2LV) and index scores were assessed. RESULTS: Index scores were related to memory and T2LV in MS patients, who showed marginally elevated AntI relative to HC (p = 0.06); no group differences were found for IntI. Better memory was associated with higher AntI (ß = 0.15, p = 0.018) and IntI (ß = 0.16, p = 0.014). No associations were found for non-memory cognition. Higher T2LV was associated with higher AntI and IntI; exploratory mediation analysis revealed significant inconsistent mediation, that is, higher index scores partially suppressed the negative association between T2LV and memory. CONCLUSION: Summary, within-subject metrics permit replication and circumvent challenges of traditional (incommensurate) RSFC variables to advance development of mechanistic models of memory dysfunction in MS.

Patterns of episodic content and specificity predicting subjective memory vividness.

The ability to remember and internally represent events is often accompanied by a subjective sense of "vividness". Vividness measures are frequently used to evaluate the experience of remembering and imagining events, yet little research has considered the objective attributes of event memories that underlie this subjective judgment, and individual differences in this mapping. Here, we tested how the content and specificity of event memories support subjectively vivid recollection. Over three experiments, participants encoded events containing a theme word and three distinct elements - a person, a place, and an object. In a memory test, memory for event elements was assessed at two levels of specificity - semantic gist (names) and perceptual details (lure discrimination). We found a strong correspondence between memory vividness and memory for gist information that did not vary by which elements were contained in memory. There was a smaller, additive benefit of remembering specific perceptual details on vividness, which, in one study, was driven by memory for place details. Moreover, we found individual differences in the relationship between memory vividness and objective memory attributes primarily along the specificity dimension, such that one cluster of participants used perceptual detail to inform memory vividness whereas another cluster was more driven by gist information. Therefore, while gist memory appears to drive vividness on average, there were idiosyncrasies in this pattern across participants. When assessing subjective ratings of memory and imagination, research should consider how these ratings map onto objective memory attributes in the context of their study design and population.

A new look at memory retention and forgetting.

The forgetting curve is one of the most well known and established findings in memory research. Knowing the pattern of memory change over time can provide insight into underlying cognitive mechanisms. The default understanding is that forgetting follows a continuous, negatively accelerating function, such as a power function. We show that this understanding is incorrect. We first consider whether forgetting rates vary across different intervals of time reported in the literature. We found that there were different patterns of forgetting across different time periods. Next, we consider evidence that complex memories, such as those derived from event cognition, show different patterns, such as linear forgetting. Based on these findings, we argue that forgetting cannot be adequately explained by a single continuous function. As an alternative, we propose a Memory Phases Framework, through which the progress of memory can be divided into phases that parallel changes associated with neurological memory consolidation. These phases include (a) Working Memory (WM) during the first minute of retention, (b) Early Long-Term Memory (e-LTM) during the 12 hr following encoding, (c) a period of Transitional Long-Term Memory (t-LTM) during the following week or so, and (d) Long-Lasting Memory (LLM) memory beyond this. These findings are of significance for any field of study where being able to predict retention and forgetting is important, such as training, eyewitness memory, or clinical treatment. They are also important for evaluating behavioral or neuroscientific manipulations targeting memories over longer periods of time when different processes may be involved. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Distinct medial-tempora lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear.

Current models of episodic memory posit that retrieval involves the reenactment of encoding processes. Recent evidence has shown that this reinstatement process - indexed by subsequent encoding-retrieval similarity of brain activity patterns - is related to the activity in the hippocampus during encoding. However, we tend to re-experience emotional events in memory more richly than dull events. The role of amygdala - a critical hub of emotion processing - in reinstatement of emotional events was poorly understood. To investigate it, we leveraged a previously overlooked divergence in the role of amygdala in memory modulation by distinct emotions - disgust and fear. Here we used a novel paradigm in which participants encoded complex events (word pairs) and their memory was tested after 3 weeks, both phases during fMRI scanning. Using representational similarity analysis and univariate analyses, we show that the strength of amygdala activation during encoding was correlated with memory reinstatement of individual event representations in emotion-specific regions. Critically, amygdala modulated reinstatement more for disgust than fear. This was in line with other differences observed at the level of memory performance and neural mechanisms of encoding. Specifically, amygdala and perirhinal cortex were more involved during encoding of disgust-related events, whereas hippocampus and parahippocampal gyrus during encoding of fear-related events. Together, these findings shed a new light on the role of the amygdala and medial temporal lobe regions in encoding and reinstatement of specific emotional memories.

Brain Mechanisms Underlying the Subjective Experience of Remembering.

The ability to remember events in vivid, multisensory detail is a significant part of human experience, allowing us to relive previous encounters and providing us with the store of memories that shape our identity. Recent research has sought to understand the subjective experience of remembering, that is, what it feels like to have a memory. Such remembering involves reactivating sensory-perceptual features of an event and the thoughts and feelings we had when the event occurred, integrating them into a conscious first-person experience. It allows us to reflect on the content of our memories and to understand and make judgments about them, such as distinguishing events that actually occurred from those we might have imagined or been told about. In this review, we consider recent evidence from functional neuroimaging in healthy participants and studies of neurological and psychiatric conditions, which is shedding new light on how we subjectively experience remembering.

Mapping the organization and dynamics of the posterior medial network during movie watching.

Brain regions within a posterior medial network (PMN) are characterized by sensitivity to episodic tasks, and they also demonstrate strong functional connectivity as part of the default network. Despite its cohesive structure, delineating the intranetwork organization and functional diversity of the PMN is crucial for understanding its contributions to multidimensional event cognition. Here, we probed functional connectivity of the PMN during movie watching to identify its pattern of connections and subnetwork functions in a split-sample replication of 136 participants. Consistent with prior findings of default network fractionation, we identified distinct PMN subsystems: a Ventral PM subsystem (retrosplenial cortex, parahippocampal cortex, posterior angular gyrus) and a Dorsal PM subsystem (medial prefrontal cortex, hippocampus, precuneus, posterior cingulate cortex, anterior angular gyrus). Ventral and Dorsal PM subsystems were differentiated by functional connectivity with parahippocampal cortex and precuneus and integrated by retrosplenial cortex and posterior cingulate cortex, respectively. Finally, the distinction between PMN subsystems is functionally relevant: whereas both Dorsal and Ventral PM connectivity tracked the movie content, only Ventral PM connections increased in strength at event transitions and appeared sensitive to episodic memory. Overall, these findings reveal PMN functional pathways and the distinct functional roles of intranetwork subsystems during event cognition.

Amygdala and ventral tegmental area differentially interact with hippocampus and cortical medial temporal lobe during rest in humans.

Neuromodulatory regions that detect salience, such as amygdala and ventral tegmental area (VTA), have distinct effects on memory. Yet, questions remain about how these modulatory regions target subregions across the hippocampus and medial temporal lobe (MTL) cortex. Here, we sought to characterize how VTA and amygdala subregions (i.e., basolateral amygdala and central-medial amygdala) interact with hippocampus head, body, and tail, as well as cortical MTL areas of perirhinal cortex and parahippocampal cortex in a task-free state. To quantify these interactions, we used high-resolution resting state fMRI and characterized pair-wise, partial correlations across regions-of-interest. We found that basolateral amygdala showed greater functional coupling with hippocampus head, hippocampus tail, and perirhinal cortex when compared to either VTA or central-medial amygdala. Furthermore, the VTA showed greater functional coupling with hippocampus tail when compared to central-medial amygdala. There were no significant differences in functional coupling with hippocampus body and parahippocampal cortex. These results support a framework by which neuromodulatory regions do not indiscriminately influence all MTL subregions equally, but rather bias information processing to discrete MTL targets. These findings provide a more specified model of the intrinsic properties of systems underlying MTL neuromodulation. This emphasizes the need to consider heterogeneity both across and within neuromodulatory systems to better understand affective memory.

Deconstructing the Posterior Medial Episodic Network.

Our ability to remember or imagine specific events involves the construction of complex mental representations, a process that engages cortical and hippocampal regions in a core posterior medial (PM) brain network. Existing theoretical approaches have described the overarching contributions of the PM network, but less is known about how episodic content is represented and transformed throughout this system. Here, we review evidence of key functional interactions among PM regions and their relation to the core cognitive operations and representations supporting episodic construction. Recent demonstrations of intranetwork functional diversity are integrated with existing accounts to inform a network-based model of episodic construction, in which PM regions flexibly share and manipulate event information to support the variable phenomenology of episodic memory and simulation.

A database of news videos for investigating the dynamics of emotion and memory.

Emotional experiences are known to be both perceived and remembered differently from nonemotional experiences, often leading to heightened encoding of salient visual details and subjectively vivid recollection. The vast majority of previous studies have used static images to investigate how emotional event content modulates cognition, yet natural events unfold over time. Therefore, little is known about how emotion dynamically modulates continuous experience. Here we report a norming study wherein we developed a new stimulus set of 126 emotionally negative, positive, and neutral videos depicting real-life news events. Participants continuously rated the valence of each video during its presentation and judged the overall emotional intensity and valence at the end of each video. In a subsequent memory test, participants reported how vividly they could recall the video details and estimated each video's duration. We report data on the affective qualities and subjective memorability of each video. The results replicate the well-established effect that emotional experiences are remembered more vividly than nonemotional experiences. Importantly, this novel stimulus set will facilitate research into the temporal dynamics of emotional processing and memory.

Progression from Feature-Specific Brain Activity to Hippocampal Binding during Episodic Encoding.

The hallmark of episodic memory is recollecting multiple perceptual details tied to a specific spatial-temporal context. To remember an event, it is therefore necessary to integrate such details into a coherent representation during initial encoding. Here we tested how the brain encodes and binds multiple, distinct kinds of features in parallel, and how this process evolves over time during the event itself. We analyzed data from 27 human subjects (16 females, 11 males) who learned a series of objects uniquely associated with a color, a panoramic scene location, and an emotional sound while fMRI data were collected. By modeling how brain activity relates to memory for upcoming or just-viewed information, we were able to test how the neural signatures of individual features as well as the integrated event changed over the course of encoding. We observed a striking dissociation between early and late encoding processes: left inferior frontal and visuo-perceptual signals at the onset of an event tracked the amount of detail subsequently recalled and were dissociable based on distinct remembered features. In contrast, memory-related brain activity shifted to the left hippocampus toward the end of an event, which was particularly sensitive to binding item color and sound associations with spatial information. These results provide evidence of early, simultaneous feature-specific neural responses during episodic encoding that predict later remembering and suggest that the hippocampus integrates these features into a coherent experience at an event transition.SIGNIFICANCE STATEMENT Understanding and remembering complex experiences are crucial for many socio-cognitive abilities, including being able to navigate our environment, predict the future, and share experiences with others. Probing the neural mechanisms by which features become bound into meaningful episodes is a vital part of understanding how we view and reconstruct the rich detail of our environment. By testing memory for multimodal events, our findings show a functional dissociation between early encoding processes that engage lateral frontal and sensory regions to successfully encode event features, and later encoding processes that recruit hippocampus to bind these features together. These results highlight the importance of considering the temporal dynamics of encoding processes supporting multimodal event representations.

Stress and the medial temporal lobe at rest: Functional connectivity is associated with both memory and cortisol.

When acute stress is experienced immediately after memory encoding (i.e., post-encoding stress) it can significantly impact subsequent memory for that event. For example, recent work has suggested that post-encoding stress occurring in a different context from encoding impairs memory. However, the neural processes underlying these effects are poorly understood. We aimed to expand this understanding by conducting an analysis of resting functional connectivity in the period following post-encoding stress that occurred in a different context than encoding, using seed regions in the medial temporal lobes known for their roles in memory. In the current study of 44 males randomized to stress (n = 23) or control (n = 21) groups, we found that stress increased cortisol, impaired recollection of neutral materials, and altered functional connectivity with medial temporal lobe regions. Although stress did not significantly alter hippocampus-amygdala functional connectivity, relative to participants in the control group, participants in the post-encoding stress group showed lower functional connectivity between the hippocampus and a region with a peak in the superior temporal gyrus. Across participants in both groups, functional connectivity between these regions was related to greater increases in cortisol, and it was also inversely related to recollection of neutral materials. In contrast, the stress group showed greater parahippocampal cortex functional connectivity with a region in the left middle temporal gyrus than the control group. Moreover, greater functional connectivity between the parahippocampal cortex and the observed cluster in the middle temporal gyrus was associated with greater cortisol changes from pre- to post-manipulation, but was not related to differences in memory. The results show that post-encoding stress can alter the resting-state functional connectivity between the medial temporal lobe and neocortex, which may help explain how stress impacts memory.

Memories Fade: The Relationship Between Memory Vividness and Remembered Visual Salience.

Past events, particularly emotional experiences, are often vividly recollected. However, it remains unclear how qualitative information, such as low-level visual salience, is reconstructed and how the precision and bias of this information relate to subjective memory vividness. Here, we tested whether remembered visual salience contributes to vivid recollection. In three experiments, participants studied emotionally negative and neutral images that varied in luminance and color saturation, and they reconstructed the visual salience of each image in a subsequent test. Results revealed, unexpectedly, that memories were recollected as less visually salient than they were encoded, demonstrating a novel memory-fading effect, whereas negative emotion increased subjective memory vividness and the precision with which visual features were encoded. Finally, memory vividness tracked both the precision and remembered salience (bias) of visual information. These findings provide evidence that low-level visual information fades in memory and contributes to the experience of vivid recollection.

Cortico-hippocampal network connections support the multidimensional quality of episodic memory.

Episodic memories reflect a bound representation of multimodal features that can be reinstated with varying precision. Yet little is known about how brain networks involved in memory, including the hippocampus and posterior-medial (PM) and anterior-temporal (AT) systems, interact to support the quality and content of recollection. Participants learned color, spatial, and emotion associations of objects, later reconstructing the visual features using a continuous color spectrum and 360-degree panorama scenes. Behaviorally, dependencies in memory were observed for the gist but not precision of event associations. Supporting this integration, hippocampus, AT, and PM regions showed increased connectivity and reduced modularity during retrieval compared to encoding. These inter-network connections tracked a multidimensional, objective measure of memory quality. Moreover, distinct patterns of connectivity tracked item color and spatial memory precision. These findings demonstrate how hippocampal-cortical connections reconfigure during episodic retrieval, and how such dynamic interactions might flexibly support the multidimensional quality of remembered events.

Dissociable medial temporal pathways for encoding emotional item and context information.

Emotional experiences are typically remembered with a greater sense of recollection than neutral experiences, but memory benefits for emotional items do not typically extend to their source contexts. Item and source memory have been attributed to different subregions of the medial temporal lobes (MTL), but it is unclear how emotional item recollection fits into existing models of MTL function and, in particular, what is the role of the hippocampus. To address these issues, we used high-resolution functional magnetic resonance imaging (fMRI) to examine MTL contributions to successful emotional item and context encoding. The results showed that emotional items were recollected more often than neutral items. Whereas amygdala and perirhinal cortex (PRC) activity supported the recollection advantage for emotional items, hippocampal and parahippocampal cortex activity predicted subsequent source memory for both types of items, reflecting a double dissociation between anterior and posterior MTL regions. In addition, amygdala activity during encoding modulated the relationships of PRC activity and hippocampal activity to subsequent item recollection and source memory, respectively. Specifically, whereas PRC activity best predicted subsequent item recollection when amygdala activity was relatively low, hippocampal activity best predicted source memory when amygdala activity was relatively high. We interpret these findings in terms of complementary compared to synergistic amygdala-MTL interactions. The results suggest that emotion-related enhancements in item recollection are supported by an amygdala-PRC pathway, which is separable from the hippocampal pathway that binds items to their source context.

Neural reactivation in parietal cortex enhances memory for episodically linked information.

Remembering is a complex process that involves recalling specific details, such as who you were with when you celebrated your last birthday, as well as contextual information, such as the place where you celebrated. It is well established that the act of remembering enhances long-term retention of the retrieved information, but the neural and cognitive mechanisms that drive memory enhancement are not yet understood. One possibility is that the process of remembering results in reactivation of the broader episodic context. Consistent with this idea, in two experiments, we found that multiple retrieval attempts enhanced long-term retention of both the retrieved object and the nontarget object that shared scene context, compared with a restudy control. Using representational similarity analysis of fMRI data in experiment 2, we found that retrieval resulted in greater neural reactivation of both the target objects and contextually linked objects compared with restudy. Furthermore, this reactivation occurred in a network of medial and lateral parietal lobe regions that have been linked to episodic recollection. The results demonstrate that retrieving a memory can enhance retention of information that is linked in the broader event context and the hippocampus and a posterior medial network of parietal cortical areas (also known as the Default Network) play complementary roles in supporting the reactivation of episodically linked information during retrieval.