A contextual binding theory of episodic memory: systems consolidation reconsidered.

Episodic memory reflects the ability to recollect the temporal and spatial context of past experiences. Episodic memories depend on the hippocampus but have been proposed to undergo rapid forgetting unless consolidated during offline periods such as sleep to neocortical areas for long-term storage. Here, we propose an alternative to this standard systems consolidation theory (SSCT) - a contextual binding account - in which the hippocampus binds item-related and context-related information. We compare these accounts in light of behavioural, lesion, neuroimaging and sleep studies of episodic memory and contend that forgetting is largely due to contextual interference, episodic memory remains dependent on the hippocampus across time, contextual drift produces post-encoding activity and sleep benefits memory by reducing contextual interference.

Multisensory processing impacts memory for objects and their sources.

Multisensory object processing improves recognition memory for individual objects, but its impact on memory for neighboring visual objects and scene context remains largely unknown. It is therefore unclear how multisensory processing impacts episodic memory for information outside of the object itself. We conducted three experiments to test the prediction that the presence of audiovisual objects at encoding would improve memory for nearby visual objects, and improve memory for the environmental context in which they occurred. In Experiments 1a and 1b, participants viewed audiovisual-visual object pairs or visual-visual object pairs with a control sound during encoding and were subsequently tested on their memory for each object individually. In Experiment 2, objects were paired with semantically congruent or meaningless control sounds and appeared within four different scene environments. Memory for the environment was tested. Results from Experiments 1a and 1b showed that encoding a congruent audiovisual object did not significantly benefit memory for neighboring visual objects, but Experiment 2 showed that encoding a congruent audiovisual object did improve memory for the environments in which those objects were encoded. These findings suggest that multisensory processing can influence memory beyond the objects themselves and that it has a unique role in episodic memory formation. This is particularly important for understanding how memories and associations are formed in real-world situations, in which objects and their surroundings are often multimodal.

When stress enhances memory encoding: The beneficial effects of changing context.

The effects of acute stress on memory encoding are complex, and we do not yet know all of the conditions that can determine whether stress at encoding improves or impairs memory. Recent work has found that changing contexts between encoding and stress can abolish the effects of post-encoding stress on memory, suggesting that context may play an important role in the effects of stress on memory. However, the role of context in the effects of stress on memory encoding is not yet known. We addressed this gap by examining the effects of context on the influence of acute stress on memory encoding. In a 2 × 2 experimental design, participants (N = 103) completed either a stressor (i.e., Socially Evaluated Cold Presser Test) or control task (i.e., warm water control) before completing a memory encoding task, which occurred in either in the same room as or a different room from the stressor or control task. Memory retrieval was tested for each participant within the context that they completed the encoding task. We found that, relative to nonstressed (i.e., control) participants, stressed participants who switched contexts prior to encoding showed better memory for both negative and neutral images. In contrast, when the stressor or control task occurred in the same room as memory encoding, stress had no beneficial effect on memory. These results highlight the importance of the ongoing context as a determinant of the effects of stress on memory encoding and present a challenge to current theoretical accounts of stress and memory.

Stress and memory encoding: What are the roles of the stress-encoding delay and stress relevance?

The effects of acute stress on memory encoding are complex. Recent work has suggested that both the delay between stress and encoding and the relevance of the information learned to the stressor may modulate the effects of stress on memory encoding, but the relative contribution of each of these two factors is unclear. Therefore, in the present study, we manipulated (1) acute stress, (2) the delay between stress and encoding, and (3) the relevance of the information learned to the stressor. The results indicated that stress during encoding led to better memory for study materials that were related to the stressor relative to memory for study materials that were unrelated to the stressor. This effect was numerically reduced for materials that were encoded 40 min after stressor onset (23 min after the stressor had ended) compared with items encoded at the time of the stressor, but this difference was not significant. These results suggest that the relevance of the information learned to the stressor may play a particularly important role in the effects of stress on memory encoding, which has important implications for theories of stress and memory.

The hippocampus supports high-precision binding in visual working memory.

It is well established that the hippocampus is critical for long-term episodic memory, but a growing body of research suggests that it also plays a critical role in supporting memory over very brief delays as measured in tests of working memory (WM). However, the circumstances under which the hippocampus is necessary for WM and the specific processes that it supports remain controversial. We propose that the hippocampus supports WM by binding together high-precision properties of an event, and we test this claim by examining the precision of color-location bindings in a visual WM task in which participants report the precise color of studied items using a continuous color wheel. Amnestic patients with hippocampal damage were significantly impaired at retrieving these colors after a 1-s delay, and these impairments reflected a reduction in the precision of those memories rather than increases in total memory failures or binding errors. Moreover, a parallel fMRI study in healthy subjects revealed that neural activity in the head and body of the hippocampus was directly related to the precision of visual WM decisions. Together, these results indicate that the hippocampus is critical in complex high-precision binding that supports memory over brief delays.

Markers of a plant-based diet relate to memory and executive function in older adults.

BACKGROUND: Although it is known that plant-based foods are important for physical health, little is known about the relationship between plant-based foods and cognitive health. Emerging evidence suggests that some macronutrients may influence cognition, but it is unclear which domains of cognition are involved; more importantly, it is unknown how a plant-based diet relates to cognition. OBJECTIVE: To examine associations between a plant-based dietary pattern and cognitive functioning. METHODS: Participants were 3,039 older adults who participated in the 2011-2014 waves of the National Health and Nutrition Examination Survey (NHANES). The present cross-sectional study used data on macronutrient intake from 24-hour dietary interviews, as well as performance on tests of long-term memory and executive function (i.e., delayed word recall, digit symbol substitution test, and animal fluency). Principal component analysis was used to extract a dietary pattern consistent with a plant-based diet. RESULTS: Greater adherence to a dietary pattern consistent with a plant-based diet was related to better performance on all cognitive tasks. Secondary analyses indicated that the associations between a plant-based dietary pattern and executive function accounted for the association between a plant-based dietary pattern and memory. Furthermore, this same plant-based dietary pattern was associated with reduced baseline inflammation in a separate dataset. CONCLUSIONS: Experimental manipulations are needed to determine the potential causal relations of these associations, but these results suggest that a plant-based diet relates to better cognition, especially through improved executive control. Future work should also attempt to extend these results by examining potential mechanisms underlying these associations, such as reduced inflammation.

Narratives bridge the divide between distant events in episodic memory.

Many studies suggest that information about past experience, or episodic memory, is divided into discrete units called "events." Yet we can often remember experiences that span multiple events. Events that occur in close succession might simply be linked because of their proximity to one another, but we can also build links between events that occur farther apart in time. Intuitively, some kind of organizing principle should enable temporally distant events to become bridged in memory. We tested the hypothesis that episodic memory exhibits a narrative-level organization, enabling temporally distant events to be better remembered if they form a coherent narrative. Furthermore, we tested whether post-encoding memory consolidation is necessary to integrate temporally distant events. In three experiments, participants learned and subsequently recalled events from fictional stories, in which pairs of temporally distant events involving side characters ("sideplots") either formed one coherent narrative or two unrelated narratives. Across participants, we varied whether recall was assessed immediately after learning, or after a delay: 24 hours, 12 hours between morning and evening ("wake"), or 12 hours between evening and morning ("sleep"). Participants recalled more information about coherent than unrelated narrative events, in most delay conditions, including immediate recall and wake conditions, suggesting that post-encoding consolidation was not necessary to integrate temporally distant events into a larger narrative. Furthermore, post hoc modeling across experiments suggested that narrative coherence facilitated recall over and above any effects of sentence-level semantic similarity. This reliable memory benefit for coherent narrative events supports theoretical accounts which propose that narratives provide a high-level architecture for episodic memory.

Temporal proximity to the elicitation of curiosity is key for enhancing memory for incidental information.

Curiosity states benefit memory for target information, but also incidental information presented during curiosity states. However, it is not known whether incidental curiosity-enhanced memory depends on when incidental information during curiosity states is encountered. Here, participants incidentally encoded unrelated face images at different time points while they anticipated answers to trivia questions. Across two experiments, we found memory enhancements for unrelated faces presented during high-curiosity compared with low-curiosity states, but only when presented shortly after a trivia question. This suggests processes associated with the elicitation of curiosity-but not sustained anticipation or the satisfaction of curiosity-enhance memory for incidental information.

Why do we retrace our visual steps? Semantic and episodic memory in gaze reinstatement.

When we look at repeated scenes, we tend to visit similar regions each time-a phenomenon known as resampling Resampling has long been attributed to episodic memory, but the relationship between resampling and episodic memory has recently been found to be less consistent than assumed. A possibility that has yet to be fully considered is that factors unrelated to episodic memory may generate resampling: for example, other factors such as semantic memory and visual salience that are consistently present each time an image is viewed and are independent of specific prior viewing instances. We addressed this possibility by tracking participants' eyes during scene viewing to examine how semantic memory, indexed by the semantic informativeness of scene regions (i.e., meaning), is involved in resampling. We found that viewing more meaningful regions predicted resampling, as did episodic familiarity strength. Furthermore, we found that meaning interacted with familiarity strength to predict resampling. Specifically, the effect of meaning on resampling was attenuated in the presence of strong episodic memory, and vice versa. These results suggest that episodic and semantic memory are each involved in resampling behavior and are in competition rather than synergistically increasing resampling. More generally, this suggests that episodic and semantic memory may compete to guide attention.

Using acute stress to improve episodic memory: The critical role of contextual binding.

Previous research has shown that encountering a brief stressor shortly after learning can be beneficial for memory. Recent studies, however, have shown that post-encoding stress does not benefit all recently encoded memories, and an adequate theoretical account of these effects remains elusive. The current study tested a contextual binding account of post encoding stress by examining the effect of varying the context in which the stressor was experienced. Participants encoded a mixture of negative and neutral images, immediately followed by a stressor (i.e., socially evaluated cold pressor) or a non-stress control task. Half of the participants received the stress/control manipulation in the same context as the study materials and half were moved to another context (i.e., a different room with a different experimenter). Two days later all participants returned to the original study room and received a recognition memory test. The results indicated that stress increased recognition memory only when the stressor occurred in the same context as the study materials, whereas stress did not benefit memory if the stressor occurred in a different context. Moreover, stress related increases in salivary cortisol were related to increases in memory when the stressor occurred in the same context as the study materials but not when the context changed. Similar effects were observed for negative and neutral materials and for males and females. These results are consistent with a contextual binding account and suggest that stress acts on memory by enhancing the encoding of the ongoing context of the stressor which benefits memory for the immediately preceding events that share the same context.

Determining the biological associates of acute cold pressor post-encoding stress effects on human memory: The role of salivary interleukin-1ß.

Stress generally hurts many aspects of memory, but an interesting finding to emerge from the stress and memory literature is that stress that occurs shortly after learning (i.e., post-encoding stress) usually benefits memory. Although this effect is well established, the biological mechanisms underpinning this effect are not-especially in humans. We addressed this gap in the present study by collecting saliva samples from 80 participants who were randomized to a post-encoding stress (i.e., cold pressor for 3 min) or control task (i.e., warm water for 3 min) and 48 h later completed a recognition memory task. Saliva was collected both prior to and 15 min after the offset of (18 min after the onset of) the stress/control manipulation. Drawing on animal and human work, we examined how five stress-responsive biomarkers-cortisol, salivary α-amylase, progesterone, estradiol, and the proinflammatory cytokine interleukin (IL)-1ß, all assessed in saliva-related to the effects of stress on memory. We found that stress enhanced recollection of negative images and that these effects were selectively related to salivary IL-1ß. Moreover, we found that the beneficial effects of stress on memory were statistically mediated by salivary IL-1ß. We found no robust associations-either linear or quadratic-between memory and any other biomarker, nor did we find significant interactions between biomarkers in predicting memory. These results suggest that immune system activity indexed by salivary IL-1ß may play an important role in contributing to post-encoding stress effects on human memory.

Determining the mechanisms through which recent life stress predicts working memory impairments: precision or capacity?

Prior research has found that recent life stress exposure is related to poorer working memory performance, but it remains unclear which aspects of working memory are related to stress. To address this important issue, we examined the extent to which recent life stress exposure was associated with working memory capacity (i.e., the number of items that can be held in working memory) and working memory precision (i.e., the quality of representations of items held within working memory) in a sample of 260 healthy young adults (Mage = 19.95 years old; range = 18-33). Recent life stress exposure and working memory were assessed with the Stress and Adversity Inventory for Daily Stress (Daily STRAIN) and color wheel task, respectively. We found that recent life stress was selectively associated with lower working memory capacity; moreover, the association of recent life stress with capacity was significantly stronger in magnitude than the non-significant association of recent life stress with precision. These associations were robust while controlling for potential confounds, including demographic factors, negative affect, and cumulative lifetime stress exposure. These results thus suggest that stress-related degradations in working memory capacity may help explain how recent life stress exposure affects working memory performance.

The effects of post-encoding stress and glucocorticoids on episodic memory in humans and rodents.

It is now well established that acute stress shortly after encoding (i.e., post-encoding stress) can benefit episodic memory. In the current paper, we briefly review the human literature examining the effects of post-encoding stress on episodic memory, and we relate that literature to studies of post-encoding manipulations of cortisol in humans, as well as studies of post-encoding stress and administration of corticosterone on analogous memory tasks in rodents. An examination of the literature reveals several important gaps in our understanding of stress and memory. For example, although the human literature shows that post-encoding stress generally improves memory, these effects are not observed if stress occurs in a different context from learning. Moreover, the rodent literature shows that post-encoding stress generally impairs memory instead of improving it, and these effects depend on whether the animal is habituated to the learning context prior to encoding. Although many aspects of the results support a cellular consolidation account of post-encoding stress, we present possible modifications, such as a network reset, to better account for the data. We also suggest that it is important to incorporate ideas of contextual binding in order to understanding the effects of post-encoding stress and glucocorticoids on memory.

Pre-encoding stress induced changes in perceived stress, blood pressure and cortisol are differentially associated with recollection and familiarity.

Stress before encoding is often linked to impaired memory. Further influences of stress on memory are arousal of the to be learned material and memory retrieval type (free recall vs. recognition). In the current study we tested the influence of stress on memory encoding for neutral and negative arousing pictures in healthy young adults. A total of 80 participants (40 men) were subjected either to the socially evaluated cold pressure test or a control condition before encoding of arousing and neutral pictures. One day later participants underwent a recognition test. Results show different relationships between the obtained stress markers and recognition memory. Higher perceived stress ratings predicted poorer overall accuracy for arousing material. Lower perceived stress ratings and larger blood pressure increase predicted higher recollection values for arousing material. In contrast, a larger cortisol increase predicted lower familiarity values for arousing material. Concluding, activity of the sympathetic nervous system (SNS) and a lower feeling of perceived stress predict better recollection. HPA axis activity predicts lower familiarity. Pre-encoding induced changes in the perceived feeling of stress, activity of the SNS, and activity of the HPA axis show specific and distinct relationships to recognition memory.

Close but no cigar: Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory.

Increasing evidence suggests that the human hippocampus contributes to a range of different behaviors, including episodic memory, language, short-term memory, and navigation. A novel theoretical framework, the Precision and Binding Model, accounts for these phenomenon by describing a role for the hippocampus in high-resolution, complex binding. Other theories like Cognitive Map Theory, in contrast, predict a specific role for the hippocampus in allocentric navigation, while Declarative Memory Theory predicts a specific role in delay-dependent conscious memory. Navigation provides a unique venue for testing these predictions, with past results from research with humans providing inconsistent findings regarding the role of the human hippocampus in spatial navigation. Here, we tested five patients with lesions primarily restricted to the hippocampus and those extending out into the surrounding medial temporal lobe cortex on a virtual water maze task. Consistent with the Precision and Binding Model, we found partially intact allocentric memory in all patients, with impairments in the spatial precision of their searches for a hidden target. We found similar impairments at both immediate and delayed testing. Our findings are consistent with the Precision and Binding Model of hippocampal function, arguing for its role across domains in high-resolution, complex binding. SIGNIFICANCE STATEMENT: Remembering goal locations in one's environment is a critical skill for survival. How this information is represented in the brain is still not fully understood, but is believed to rely in some capacity on structures in the medial temporal lobe. Contradictory findings from studies of both humans and animals have been difficult to reconcile with regard to the role of the MTL, specifically the hippocampus. By assessing impairments observed during navigation to a goal in patients with medial temporal lobe damage we can better understand the role these structures play in such behavior. Utilizing virtual reality and novel analysis techniques, we have more precisely assessed the impact that medial temporal lobe damage has on spatial memory and navigation.

Reward anticipation modulates the effect of stress-related increases in cortisol on episodic memory.

When acute stress is experienced shortly after an event is encoded into memory, this can slow the forgetting of the study event, which is thought to reflect the effect of cortisol on consolidation. In addition, when events are encoded under conditions of high reward they tend to be remembered better than those encoded under non-rewarding conditions, and these effects are thought to reflect the operation of the dopaminergic reward system. Although both modulatory systems are believed to impact the medial temporal lobe regions critical for episodic memory, the manner, and even the extent, to which these two systems interact is currently unknown. To address this question in the current study, participants encoded words under reward or non-reward conditions, then one half of the participants were stressed using the social evaluation cold pressor task and the other half completed a non-stress control task. After a two-hour delay, all participants received a free recall and recognition memory test. There were no significant effects of stress or reward on overall memory performance. However, for the non-reward items, increases in stress-related cortisol in stressed participants were related to increases in recall and increases in recollection-based recognition responses. In contrast, for the reward items, increases in stress-related cortisol were not related to increases in memory performance. The results indicate that the stress and the reward systems interact in the way they impact episodic memory. The results are consistent with tag and capture models in the sense that cortisol reactivity can only affect non-reward items because plasticity-related products are already provided by reward anticipation.

Stress as a mnemonic filter: Interactions between medial temporal lobe encoding processes and post-encoding stress.

Acute stress has been shown to modulate memory for recently learned information, an effect attributed to the influence of stress hormones on medial temporal lobe (MTL) consolidation processes. However, little is known about which memories will be affected when stress follows encoding. One possibility is that stress interacts with encoding processes to selectively protect memories that had elicited responses in the hippocampus and amygdala, two MTL structures important for memory formation. There is limited evidence for interactions between encoding processes and consolidation effects in humans, but recent studies of consolidation in rodents have emphasized the importance of encoding "tags" for determining the impact of consolidation manipulations on memory. Here, we used functional magnetic resonance imaging in humans to test the hypothesis that the effects of post-encoding stress depend on MTL processes observed during encoding. We found that changes in stress hormone levels were associated with an increase in the contingency of memory outcomes on hippocampal and amygdala encoding responses. That is, for participants showing high cortisol reactivity, memories became more dependent on MTL activity observed during encoding, thereby shifting the distribution of recollected events toward those that had elicited relatively high activation. Surprisingly, this effect was generally larger for neutral, compared to emotionally negative, memories. The results suggest that stress does not uniformly enhance memory, but instead selectively preserves memories tagged during encoding, effectively acting as mnemonic filter. © 2016 Wiley Periodicals, Inc.

Visual short-term memory for high resolution associations is impaired in patients with medial temporal lobe damage.

The medial temporal lobe (MTL) plays a critical role in episodic long-term memory, but whether the MTL is necessary for visual short-term memory is controversial. Some studies have indicated that MTL damage disrupts visual short-term memory performance whereas other studies have failed to find such evidence. To account for these mixed results, it has been proposed that the hippocampus is critical in supporting short-term memory for high resolution complex bindings, while the cortex is sufficient to support simple, low resolution bindings. This hypothesis was tested in the current study by assessing visual short-term memory in patients with damage to the MTL and controls for high resolution and low resolution object-location and object-color associations. In the location tests, participants encoded sets of two or four objects in different locations on the screen. After each set, participants performed a two-alternative forced-choice task in which they were required to discriminate the object in the target location from the object in a high or low resolution lure location (i.e., the object locations were very close or far away from the target location, respectively). Similarly, in the color tests, participants were presented with sets of two or four objects in a different color and, after each set, were required to discriminate the object in the target color from the object in a high or low resolution lure color (i.e., the lure color was very similar or very different, respectively, to the studied color). The patients were significantly impaired in visual short-term memory, but importantly, they were more impaired for high resolution object-location and object-color bindings. The results are consistent with the proposal that the hippocampus plays a critical role in forming and maintaining complex, high resolution bindings. © 2016 Wiley Periodicals, Inc.

Recent life stress exposure is associated with poorer long-term memory, working memory, and self-reported memory.

Although substantial research has examined the effects of stress on cognition, much of this research has focused on acute stress (e.g. manipulated in the laboratory) or chronic stress (e.g. persistent interpersonal or financial difficulties). In contrast, the effects of recent life stress on cognition have been relatively understudied. To address this issue, we examined how recent life stress is associated with long-term, working memory, and self-reported memory in a sample of 142 healthy young adults who were assessed at two time points over a two-week period. Recent life stress was measured using the newly-developed Stress and Adversity Inventory for Daily Stress (Daily STRAIN), which assesses the frequency of relatively common stressful life events and difficulties over the preceding two weeks. To assess memory performance, participants completed both long-term and working memory tasks. Participants also provided self-reports of memory problems. As hypothesized, greater recent life stress exposure was associated with worse performance on measures of long-term and working memory, as well as more self-reported memory problems. These associations were largely robust while controlling for possible confounds, including participants' age, sex, and negative affect. The findings indicate that recent life stress exposure is broadly associated with worse memory. Future studies should thus consider assessing recent life stress as a potential predictor, moderator, or covariate of memory performance.