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Antony, J. W.

Publications and source records attributed to Antony, J. W..

8 recordsLinked to original sources

Post-Learning Reactivation of Memories for Naturalistic Continuous Experiences

Memories are not static records of the past; rather, the act of remembering can change how an event is recalled. Intriguingly, several studies also suggest that memories may be reactivated during rest. However, reactivation has largely been studied for spatial tasks and discrete stimuli, and we know little about whether spontaneous reactivation occurs for long timescale naturalistic events and how reactivation affects retention. Using fMRI, we show that neural activity patterns in the hippocampus and the Default Mode Network during encoding of narrative events were spontaneously reactivated during rest. Contrary to predictions, reactivation did not strengthen recall of movie details, and instead exploratory analyses suggested that reactivation in the hippocampus was associated with more gist-like recall one week later. These findings support the idea that memories for complex events may be spontaneously reactivated, but they suggest that rather than simply strengthening episodic memories, reactivation might help transform them.

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Causal network structure predicts memory organization and neural reinstatement across events

Endel Tulving proposed that episodic memory is organized by spatiotemporal relationships, and current theories center the role of time and space in organizing memory. However, these theories are supported by paradigms that eliminate other forms of relationships, like causality. Here, we used fMRI to reveal the organization of neural representations that support episodic memory with a paradigm that decoupled time and causal relationships. Participants were scanned while watching and recalling a TV show featuring five temporally interleaved storylines. Behaviorally, the order of recalled events was best predicted by the strongest cause-effect relationship relative to temporal, spatial, or semantic associations. Neural similarity across different events in regions of the default mode network (DMN) reflected causal structure, and DMN patterns at event boundaries specifically reactivated prior, causally related events, suggesting causality allows us to stitch together related events across temporal gaps. Additionally, causal network distance between successive events predicted the strength of DMN pattern changes across event boundaries, suggesting causality also predicts stronger representational switching between unrelated events. Together, these findings suggest that the DMN supports the construction of the complex causal networks that play a central role in organizing how we understand and remember events.

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Memory reactivation during sleep does not act holistically on object memory

Memory reactivation during sleep is thought to facilitate memory consolidation. Most sleep reactivation research has examined how reactivation of specific facts, objects, and associations benefits their overall retention. However, our memories are not unitary, and not all features of a memory persist in tandem over time. Instead, our memories are transformed, with some features strengthened and others weakened. Does sleep reactivation drive memory transformation? We leveraged the Targeted Memory Reactivation technique in an object category learning paradigm to examine this question. Participants (20 female, 14 male) learned three categories of novel objects, where each object had unique, distinguishing features as well as features shared with other members of its category. We used a real-time EEG protocol to cue the reactivation of these objects during sleep at moments optimized to generate reactivation events. We found that reactivation improved memory for distinguishing features while worsening memory for shared features, suggesting a differentiation process. The results indicate that sleep reactivation does not act holistically on object memories, instead supporting a transformation process where some features are enhanced over others.

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Aversive memories can be weakened during human sleepvia the reactivation of positive interfering memories

Recollecting painful or traumatic experiences can be deeply troubling. Sleep may offer an opportunity to reduce such suffering. We developed a procedure to weaken older aversive memories by reactivating newer positive memories during sleep. Participants viewed 48 nonsense words each paired with a unique aversive image, followed by an overnight sleep. In the next evening, participants learned associations between half of the words and additional positive images, creating interference. During the following non-rapid-eye-movement sleep, auditory memory cues were unobtrusively delivered. Upon waking, presenting cues associated with both aversive and positive images during sleep, as opposed to not presenting cues, weakened aversive memory recall while increasing positive memory intrusions. Substantiating these memory benefits, computational modeling revealed that cueing facilitated evidence accumulation toward positive affect judgments. Moreover, cue-elicited theta brain rhythms during sleep predominantly predicted the recall of positive memories. A noninvasive sleep intervention can thus modify aversive recollection and affective responses. Significance StatementNot all memories are welcome: recollection and involuntary intrusions of aversive memories can be debilitating. Prior research shows that reactivating positive memories benefits psychological health, and memory reactivation can be externally triggered during human sleep. Here, we introduced a novel sleep-based memory updating procedure to weaken older aversive memories by reactivating newer positive memories. We found that such reactivation not only weakened the recall of aversive memories, but also increased involuntary intrusion of positive memories. Moreover, reactivation enhanced positive affect judgments. Our findings open new avenues for weakening aversive or traumatic memories during human sleep.

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Item-specific memory reactivation supports overnight memory consolidation

Memory consolidation stabilizes newly acquired information. Understanding how individual memories are reactivated during sleep is essential in theorizing memory consolidation. Via unobtrusively re-playing auditory memory cues to sleeping human participants, we identified the reactivation of individual memories during slow-wave sleep (SWS). Using representational similarity analysis (RSA) on cue-elicited electroencephalogram (EEG), we found functionally segregated item-specific representations: the early post-cue EEG activity (0-2 seconds) contained comparable representations for memory cues and for non-memory control cues, thus reflecting sensory processing. Critically, the later EEG activity (2.5-3 s) showed greater item-specific representations for post-sleep remembered items than for forgotten and control cues, demonstrating the reactivation and consolidation of individual memories. Moreover, spindles preferentially supported item-specific memory reactivation for items that were not tested before sleep. These findings delineated how cue-triggered item-specific memory reactivation, subserved by spindles during SWS, contributed to memory consolidation. These results will benefit future research aiming to perturb specific memory episodes during sleep.

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Memory out of context: Spacing effects and decontextualization in a computational model of the medial temporal lobe

Some neural representations change across multiple timescales. Here we argue that modeling this "drift" could help explain the spacing effect (the long-term benefit of distributed learning), whereby differences between stored and current temporal context activity patterns produce greater error-driven learning. We trained a neurobiologically realistic model of the entorhinal cortex and hippocampus to learn paired associates alongside temporal context vectors that drifted between learning episodes and/or before final retention intervals. In line with spacing effects, greater drift led to better model recall after longer retention intervals. Dissecting model mechanisms revealed that greater drift increased error-driven learning, strengthened weights in slower-drifting temporal context neurons (temporal abstraction), and improved direct cue-target associations (decontextualization). Intriguingly, these results suggest that decontextualization -- generally ascribed only to the neocortex -- can occur within the hippocampus itself. Altogether, our findings provide a mechanistic formalization for established learning concepts such as spacing effects and errors during learning.

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Long-term, multi-event surprise enhances autobiographical memory

Neurobiological and psychological models of learning emphasize the importance of prediction errors (surprises) for memory formation. These effects have focused on memory for information surrounding a momentary surprising event; however, it is less clear whether surprise that unfolds across multiple events and timescales impacts memory. We asked basketball fans about their most positive and negative autobiographical memories of individual plays, games, and seasons, allowing surprise measurements spanning seconds, hours, and months. We used advanced analytics on National Basketball Association play-by-play data and betting odds spanning 17 seasons, >22K games, >5.6M plays to compute and align the estimated surprise values of each memory. We found that surprising events biased positive memories on the scale of seconds and months and negative memories across all three timescales. Critically, game and season memories could not be explained by surprise at shorter timescales, suggesting that long-term, multi-event surprise influences memory. These results expand the role of surprise in models of learning and reinforce its relevance in real-world domains.

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Behavioral, physiological, and neural signatures of surprise during naturalistic sports viewing

Surprise signals a discrepancy between past and current beliefs. It is theorized to be linked to affective experiences, the creation of particularly resilient memories, and segmentation of the flow of experience into discrete perceived events. However, the ability to precisely measure naturalistic surprise has remained elusive. We used advanced basketball analytics to derive a quantitative measure of surprise and characterized its behavioral, physiological, and neural correlates in human subjects observing basketball games. We found that surprise was associated with segmentation of ongoing experiences, as reflected by subjectively perceived event boundaries and shifts in neocortical patterns underlying belief states. Interestingly, these effects differed by whether surprising moments contradicted or bolstered current predominant beliefs. Surprise also positively correlated with pupil dilation, activation in subcortical regions associated with dopamine, game enjoyment, and long-term memory. These investigations support key predictions from event segmentation theory and extend theoretical conceptualizations of surprise to real-world contexts.

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