Mnemonic Content and Hippocampal Patterns Shape Judgments of Time.

Our experience of time can feel dilated or compressed, rather than reflecting true "clock time." Although many contextual factors influence the subjective perception of time, it is unclear how memory accessibility plays a role in constructing our experience of and memory for time. Here, we used a combination of behavioral and functional MRI measures in healthy young adults (N = 147) to ask the question of how memory is incorporated into temporal duration judgments. Behaviorally, we found that event boundaries, which have been shown to disrupt ongoing memory integration processes, result in the temporal compression of duration judgments. Additionally, using a multivoxel pattern similarity analysis of functional MRI data, we found that greater temporal pattern change in the left hippocampus within individual trials was associated with longer duration judgments. Together, these data suggest that mnemonic processes play a role in constructing representations of time.

Decision-making Increases Episodic Memory via Postencoding Consolidation.

The ability for individuals to actively make decisions engages regions within the mesolimbic system and enhances memory for chosen items. In other behavioral contexts, mesolimbic engagement has been shown to enhance episodic memory by supporting consolidation. However, research has yet to investigate how consolidation may support interactions between decision-making and episodic memory. Across two studies, participants encoded items that were covered by occluder screens and could either actively decide which of two items to uncover or an item was preselected by the experimenter. In Study 1, we show that active decision-making reduces forgetting rates across an immediate and 24-hr memory test, a behavioral marker of consolidation. In Study 2, we use functional neuroimaging to characterize putative neural markers of memory consolidation by measuring interactions between the hippocampus and perirhinal cortex (PRC) during a postencoding period that reexposed participants to elements of the decision-making context without exposing them to memoranda. We show that choice-related striatal engagement is associated with increased postencoding hippocampal-PRC interactions. Finally, we show that a previous reported relationship between choice-related striatal engagement and long-term memory is accounted for by these postencoding hippocampal-PRC interactions. Together, these findings support a model by which actively deciding to encode information enhances memory consolidation to preserve episodic memory for outcomes, a process that may be facilitated by reexposure to the original decision-making context.

Transcending time in the brain: How event memories are constructed from experience.

Our daily lives unfold continuously, yet when we reflect on the past, we remember those experiences as distinct and cohesive events. To understand this phenomenon, early investigations focused on how and when individuals perceive natural breakpoints, or boundaries, in ongoing experience. More recent research has examined how these boundaries modulate brain mechanisms that support long-term episodic memory. This work has revealed that a complex interplay between hippocampus and prefrontal cortex promotes the integration and separation of sequential information to help organize our experiences into mnemonic events. Here, we discuss how both temporal stability and change in one's thoughts, goals, and surroundings may provide scaffolding for these neural processes to link and separate memories across time. When learning novel or familiar sequences of information, dynamic hippocampal processes may work both independently from and in concert with other brain regions to bind sequential representations together in memory. The formation and storage of discrete episodic memories may occur both proactively as an experience unfolds. They may also occur retroactively, either during a context shift or when reactivation mechanisms bring the past into the present to allow integration. We also describe conditions and factors that shape the construction and integration of event memories across different timescales. Together these findings shed new light on how the brain transcends time to transform everyday experiences into meaningful memory representations.

The simple act of choosing influences declarative memory.

Individuals value the opportunity to make choices and exert control over their environment. This perceived sense of agency has been shown to have broad influences on cognition, including preference, decision-making, and valuation. However, it is unclear whether perceived control influences memory. Using a combined behavioral and functional magnetic resonance imaging approach, we investigated whether imbuing individuals with a sense of agency over their learning experience influences novel memory encoding. Participants encoded objects during a task that manipulated the opportunity to choose. Critically, unlike previous work on active learning, there was no relationship between individuals' choices and the content of memoranda. Despite this, we found that the opportunity to choose resulted in robust, reliable enhancements in declarative memory. Neuroimaging results revealed that anticipatory activation of the striatum, a region associated with decision-making, valuation, and exploration, correlated with choice-induced memory enhancements in behavior. These memory enhancements were further associated with interactions between the striatum and hippocampus. Specifically, anticipatory signals in the striatum when participants are alerted to the fact that they will have to choose one of two memoranda were associated with encoding success effects in the hippocampus on a trial-by-trial basis. The precedence of the striatal signal in these interactions suggests a modulatory relationship of the striatum over the hippocampus. These findings not only demonstrate enhanced declarative memory when individuals have perceived control over their learning but also support a novel mechanism by which these enhancements emerge. Furthermore, they demonstrate a novel context in which mesolimbic and declarative memory systems interact.

Temporal binding within and across events.

Remembering the order in which events occur is a fundamental component of episodic memory. However, the neural mechanisms supporting serial recall remain unclear. Behaviorally, serial recall is greater for information encountered within the same event compared to across event boundaries, raising the possibility that contextual stability may modulate the cognitive and neural processes supporting serial encoding. In the present study, we used fMRI during the encoding of consecutive face and object stimuli to elucidate the neural encoding signatures supporting subsequent serial recall behavior both within and across events. We found that univariate BOLD activation in both the middle hippocampus and left ventrolateral prefrontal cortex (PFC) was associated with subsequent serial recall of items that occur across event boundaries. By contrast, successful serial encoding within events was associated with increased functional connectivity between the hippocampus and ventromedial PFC, but not with univariate activation in these or other regions. These findings build on evidence implicating hippocampal and PFC processes in encoding temporal aspects of memory. They further suggest that these encoding processes are influenced by whether binding occurs within a stable context or bridges two adjacent but distinct events.

Temporal memory is shaped by encoding stability and intervening item reactivation.

Making sense of previous experience requires remembering the order in which events unfolded in time. Prior work has implicated the hippocampus and medial temporal lobe cortex in memory for temporal information associated with individual episodes. However, the processes involved in encoding and retrieving temporal information across extended sequences is relatively poorly understood. Here we used fMRI during the encoding and retrieval of extended sequences to test specific predictions about the type of information used to resolve temporal order and the role of the hippocampus in this process. Participants studied sequences of images of celebrity faces and common objects followed by a recency discrimination test. The main conditions of interest were pairs of items that had been presented with three intervening items, half of which included an intervening category shift. During encoding, hippocampal pattern similarity across intervening items was associated with subsequent successful order memory. To test for evidence of associative retrieval, we trained a classifier to discriminate encoding patterns associated with faces versus objects and applied the classifier on fMRI patterns during recency discrimination. We found evidence that the category content of intervening items was reactivated during recency judgments, and this was related to hippocampal encoding-retrieval similarity. A follow-up behavioral priming experiment revealed additional evidence for intervening item reinstatement during temporal order judgments. Reinstatement did not differ according to whether the items occurred within a single context or across context boundaries. Thus, these data suggest that inter-item associative encoding and retrieval mediated by the hippocampus contribute to temporal order memory.

Deconstructing the effect of self-directed study on episodic memory.

Self-directed learning is often associated with better long-term memory retention; however, the mechanisms that underlie this advantage remain poorly understood. This series of experiments was designed to "deconstruct" the notion of self-directed learning, in order to better identify the factors most responsible for these improvements to memory. In particular, we isolated the memory advantage that comes from controlling the content of study episodes from the advantage that comes from controlling the timing of those episodes. Across four experiments, self-directed learning significantly enhanced recognition memory, relative to passive observation. However, the advantage for self-directed learning was found to be present even under extremely minimal conditions of volitional control (simply pressing a button when a participant was ready to advance to the next item). Our results suggest that improvements to memory following self-directed encoding may be related to the ability to coordinate stimulus presentation with the learner's current preparatory or attentional state, and they highlight the need to consider the range of cognitive control processes involved in and influenced by self-directed study.

Benefits of spaced learning are predicted by re-encoding of past experience in ventromedial prefrontal cortex.

More than a century of research shows that spaced learning improves long-term memory. Yet, there remains debate concerning why. A major limitation to resolving theoretical debates is the lack of evidence for how neural representations change as a function of spacing. Here, leveraging a massive-scale 7T human fMRI dataset, we tracked neural representations and behavioral expressions of memory as participants viewed thousands of natural scene images that repeated at lags ranging from seconds to many months. We show that spaced learning increases the similarity of human ventromedial prefrontal cortex representations across stimulus encounters and, critically, these increases parallel and predict the behavioral benefits of spacing. Additionally, we show that these spacing benefits critically depend on remembering and, in turn, 're-encoding' past experience. Collectively, our findings provide fundamental insight into how spaced learning influences neural representations and why spacing is beneficial.

Agency as a bridge to form associative memories.

The perception of agency can influence memory when individuals feel their decisions exert control over their environment. While perceived agency has been shown to increase memory for items, most real-life situations are much more complex. Here, we examined how an individual's agency to influence the outcome of a situation affects their ability to learn associations between items that occur prior to and after a decision is made. In our paradigm, participants were told they were playing a game show where they had to help a trial unique cue, a "contestant," choose between three doors. On "agency" trials, participants were allowed to pick any door they wanted. On "forced-choice" trials, participants were instructed to select a door that was highlighted. They then saw the outcome, a "prize" that was behind the selected door. Across multiple studies, we find evidence for agency-related memory enhancements for contestants, a pattern that extended to contestant-prize, contestant-door, and door-prize associations. Additionally, we found that agency benefits for inferred cue-outcome relationships (i.e., door-prize) were limited to situations when choices were motivated by an explicit goal. Finally, we found that agency acts indirectly to influence cue-outcome binding by enhancing processes akin to inferential reasoning which associate information across item pairs containing overlapping information. Together, these data suggest having agency over a situation leads to enhanced memory for all items in that situation. This enhanced binding for items may be occurring by the formation of causal links when an individual has agency over their learning environment. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Contextual familiarity rescues the cost of switching.

Changes in context influence the way we form and structure memories. Yet, little is known about how qualitatively different types of context switches shape memory organization. The current experiments characterize how different features of context change influence the structure and organization of free recall. Participants completed a context switching paradigm in which we manipulated the rate of switches and prior experience with the contexts participants were switching between (repeated vs. novel). We measured free-recall performance and determined the extent to which participants organized items by the order in which they were encoded or the type of context with which they were originally presented. Across two experiments, we found and replicated that rapidly switching to novel, but not repeated contexts, impaired memory recall performance and biased memory towards a greater reliance on temporal information. Critically, we observed that these differences in performance may be due to distinctions in how participants organize their recalls when rapidly switching contexts. Results indicated that participants were less likely to only cluster their responses by the same context when the contexts were repeating at a high rate, as compared to when the contexts were novel. Overall, our findings support a model in which contextual familiarity rescues the costs associated with rapidly switching to new tasks or contexts.

Value restructures the organization of free recall.

A large body of research illustrates the prioritization of goal-relevant information in memory; however, it is unclear how reward-related memories are organized. Using a rewarded free recall paradigm, we investigated how reward motivation structures the organization of memory around temporal and higher-order contexts. To better understand these processes, we simulated our findings using a reward-modulated variant of the Context Maintenance and Retrieval Model (CMR; Polyn et al., 2009). In the first study, we found that reward did not influence temporal clustering, but instead shifted the organization of memory based on reward category. Further, we showed that a reward-modulated learning rate and source features of CMR most accurately depict reward's enhancement on memory and clustering by value. In a second study, we showed that reward-memory effects can exist in both extended periods of sustained motivation and frequent changes in motivation, by showing equivalent reward effects using mixed- and pure-list motivation manipulations. However, we showed that a reward-modulated learning rate in isolation can support reward's enhancement of memory in pure-list contexts. Overall, we conclude that reward-related memories are adaptively organized by higher-order value information, and contextual binding to value contexts may only be necessary when rewards are intermittent versus sustained.

Re-expression of CA1 and entorhinal activity patterns preserves temporal context memory at long timescales.

Converging, cross-species evidence indicates that memory for time is supported by hippocampal area CA1 and entorhinal cortex. However, limited evidence characterizes how these regions preserve temporal memories over long timescales (e.g., months). At long timescales, memoranda may be encountered in multiple temporal contexts, potentially creating interference. Here, using 7T fMRI, we measured CA1 and entorhinal activity patterns as human participants viewed thousands of natural scene images distributed, and repeated, across many months. We show that memory for an image's original temporal context was predicted by the degree to which CA1/entorhinal activity patterns from the first encounter with an image were re-expressed during re-encounters occurring minutes to months later. Critically, temporal memory signals were dissociable from predictors of recognition confidence, which were carried by distinct medial temporal lobe expressions. These findings suggest that CA1 and entorhinal cortex preserve temporal memories across long timescales by coding for and reinstating temporal context information.

Structuring Memory Through Inference-Based Event Segmentation.

Although the stream of information we encounter is continuous, our experiences tend to be discretized into meaningful clusters, altering how we represent our past. Event segmentation theory proposes that clustering ongoing experience in this way is adaptive in that it promotes efficient online processing as well as later reconstruction of relevant information. A growing literature supports this theory by demonstrating its important behavioral consequences. Yet the exact mechanisms of segmentation remain elusive. Here, we provide a brief overview of how event segmentation influences ongoing processing, subsequent memory retrieval, and decision making as well as some proposed underlying mechanisms. We then explore how beliefs, or inferences, about what generates our experience may be the foundation of event cognition. In this inference-based framework, experiences are grouped together according to what is inferred to have generated them. Segmentation then occurs when the inference changes, creating an event boundary. This offers an alternative to dominant theories of event segmentation, allowing boundaries to occur independent of perceptual change and even when transitions are predictable. We describe how this framework can reconcile seemingly contradictory empirical findings (e.g., memory can be biased toward both extreme episodes and the average of episodes). Finally, we discuss open questions regarding how time is incorporated into the inference process.

A common mechanism underlying choice's influence on preference and memory.

Individual control over learning leads to better memory outcomes, yet it is still unclear which aspects of control matter. One's sense of agency could be a key component, but it can be challenging to dissociate it from its consequences on the environment. Here we used a paradigm in which participants in one condition had the opportunity to choose between cues (choice condition) and in another were instructed which cue to select (fixed condition). Because the cues had no effect on the memoranda, we could isolate the effect of choice on memory. Participants also rated the cues for preference before and after encoding, allowing us to test how the number of times a cue was chosen affected its preference. By pooling multiple behavioral studies, we were able to use an individual differences approach to examine the relationship between choice effects on preference and memory. Replicating previous work, we found that immediate and delayed (24-h) recognition memory was higher for items encountered in the choice condition. We also found that cues that were selected more often increased their preference in the choice condition, but actually decreased their preference in the fixed condition, suggesting that choice engaged value-related processes. Critically, we found a positive across-subjects relationship between choice memory enhancements and choice-induced preference change for delayed but not for immediate memory. These data suggest that a shared value-based mechanism enhances preference for choice cues and memory consolidation of the choice outcomes. Thus, the value of choice may play an important role in learning enhancements.

Differential patterns of contextual organization of memory in first-episode psychosis.

Contextual information is used to support and organize episodic memory. Prior research has reliably shown memory deficits in psychosis; however, little research has characterized how this population uses contextual information during memory recall. We employed an approach founded in a computational framework of free recall to quantify how individuals with first episode of psychosis (FEP, N = 97) and controls (CON, N = 55) use temporal and semantic context to organize memory recall. Free recall was characterized using the Hopkins Verbal Learning Test-Revised (HVLT-R). We compared FEP and CON on three measures of free recall: proportion recalled, temporal clustering, and semantic clustering. Measures of temporal/semantic clustering quantified how individuals use contextual information to organize memory recall. We also assessed to what extent these measures relate to antipsychotic use and differentiated between different types of psychosis. We also explored the relationship between these measures and intelligence. In comparison to CON, FEP had reduced recall and less temporal clustering during free recall (p < 0.05, Bonferroni-corrected), and showed a trend towards greater semantic clustering (p = 0.10, Bonferroni-corrected). Within FEP, antipsychotic use and diagnoses did not differentiate between free recall accuracy or contextual organization of memory. IQ was related to free recall accuracy, but not the use of contextual information during recall in either group (p < 0.05, Bonferroni-corrected). These results show that in addition to deficits in memory recall, FEP differed in how they organize memories compared to CON.

Event Boundaries Trigger Rapid Memory Reinstatement of the Prior Events to Promote Their Representation in Long-Term Memory.

Although everyday experiences unfold continuously over time, shifts in context, or event boundaries, can influence how those events come to be represented in memory [1-4]. Specifically, mnemonic binding across sequential representations is more challenging at context shifts, such that successful temporal associations are more likely to be formed within than across contexts [1, 2, 5-9]. However, in order to preserve a subjective sense of continuity, it is important that the memory system bridge temporally adjacent events, even if they occur in seemingly distinct contexts. Here, we used pattern similarity analysis to scalp electroencephalographic (EEG) recordings during a sequential learning task [2, 3] in humans and showed that the detection of event boundaries triggered a rapid memory reinstatement of the just-encoded sequence episode. Memory reactivation was detected rapidly (∼200-800 ms from the onset of the event boundary) and was specific to context shifts that were preceded by an event sequence with episodic content. Memory reinstatement was not observed during the sequential encoding of events within an episode, indicating that memory reactivation was induced specifically upon context shifts. Finally, the degree of neural similarity between neural responses elicited during sequence encoding and at event boundaries correlated positively with participants' ability to later link across sequences of events, suggesting a critical role in binding temporally adjacent events in long-term memory. Current results shed light onto the neural mechanisms that promote episodic encoding not only for information within the event, but also, importantly, in the ability to link across events to create a memory representation of continuous experience.

Does mental context drift or shift?

Theories of episodic memory have generally proposed that individual memory traces are linked together by a representation of context that drifts slowly over time. Recent data challenge the notion that contextual drift is always slow and passive. In particular, changes in one's external environment or internal model induce discontinuities in memory that are reflected in sudden changes in neural activity, suggesting that context can shift abruptly. Furthermore, context change effects are sensitive to top-down goals, suggesting that contextual drift may be an active process. These findings call for revising models of the role of context in memory, in order to account for abrupt contextual shifts and the controllable nature of context change.

How the hippocampus preserves order: the role of prediction and context.

Remembering the sequence of events is critical for deriving meaning from our experiences and guiding behavior. Prior investigations into the function of the human hippocampus have focused on its more general role in associative binding, but recent work has focused on understanding its specific role in encoding and preserving the temporal order of experiences. In this review we summarize recent work in humans examining hippocampal contributions to sequence learning. We distinguish the learning of sequential relationships through repetition from the rapid, episodic acquisition of sequential associations. Taken together, this research begins to clarify the link between hippocampal representations and the preservation of the order of events.

The influence of context boundaries on memory for the sequential order of events.

Episodic memory allows people to reexperience the past by recovering the sequences of events that characterize those prior experiences. Although experience is continuous, people are able to selectively retrieve and reexperience more discrete episodes from their past, raising the possibility that some elements become tightly related to each other in memory, whereas others do not. The current series of experiments was designed to ask how shifts in context during an experience influence how people remember the past. Specifically, we asked how context shifts influence the ability to remember the relative order of past events, a hallmark of episodic memory. We found that memory for the order of events was enhanced within, rather than across, context shifts, or boundaries (Experiment 1). Next, we showed that this relative enhancement in order memory was eliminated when across-item associative processing was disrupted (Experiment 2), suggesting that context shifts have a selective effect on sequential binding. Finally, we provide evidence that the act of making order memory judgments involves the reactivation of representations that bridged the tested items (Experiment 3). Together, these data suggest that boundaries may serve to parse continuous experience into sequences of contextually related events and that this organization facilitates remembering the temporal order of events that share the same context.