Dataset Information

The human brain reactivates context-specific past information at event boundaries of naturalistic experiences.

ABSTRACT: Although we perceive the world in a continuous manner, our experience is partitioned into discrete events. However, to make sense of these events, they must be stitched together into an overarching narrative-a model of unfolding events. It has been proposed that such a stitching process happens in offline neural reactivations when rodents build models of spatial environments. Here we show that, while understanding a natural narrative, humans reactivate neural representations of past events. Similar to offline replay, these reactivations occur in the hippocampus and default mode network, where reactivations are selective to relevant past events. However, these reactivations occur, not during prolonged offline periods, but at the boundaries between ongoing narrative events. These results, replicated across two datasets, suggest reactivations as a candidate mechanism for binding temporally distant information into a coherent understanding of ongoing experience.

SUBMITTER: Hahamy A

PROVIDER: S-EPMC7614642 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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The human brain reactivates context-specific past information at event boundaries of naturalistic experiences.

Hahamy Avital A Dubossarsky Haim H Behrens Timothy E J TEJ

Nature neuroscience 20230529 6

Although we perceive the world in a continuous manner, our experience is partitioned into discrete events. However, to make sense of these events, they must be stitched together into an overarching narrative-a model of unfolding events. It has been proposed that such a stitching process happens in offline neural reactivations when rodents build models of spatial environments. Here we show that, while understanding a natural narrative, humans reactivate neural representations of past events. Simi ...[more]

PMID: 37248340

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Project description:We remember when things change. Particularly salient are experiences where there is a change in rewards, eliciting reward prediction errors (RPEs). How do RPEs influence our memory of those experiences? One idea is that this signal directly enhances the encoding of memory. Another, not mutually exclusive, idea is that the RPE signals a deeper change in the environment, leading to the mnemonic separation of subsequent experiences from what came before, thereby creating a new latent context and a more separate memory trace. We tested this in four experiments where participants learned to predict rewards associated with a series of trial-unique images. High-magnitude RPEs indicated a change in the underlying distribution of rewards. To test whether these large RPEs created a new latent context, we first assessed recognition priming for sequential pairs that included a high-RPE event or not (Exp. 1: n = 27 & Exp. 2: n = 83). We found evidence of recognition priming for the high-RPE event, indicating that the high-RPE event is bound to its predecessor in memory. Given that high-RPE events are themselves preferentially remembered (Rouhani, Norman, & Niv, 2018), we next tested whether there was an event boundary across a high-RPE event (i.e., excluding the high-RPE event itself; Exp. 3: n = 85). Here, sequential pairs across a high RPE no longer showed recognition priming whereas pairs within the same latent reward state did, providing initial evidence for an RPE-modulated event boundary. We then investigated whether RPE event boundaries disrupt temporal memory by asking participants to order and estimate the distance between two events that had either included a high-RPE event between them or not (Exp. 4). We found (n = 49) and replicated (n = 77) worse sequence memory for events across a high RPE. In line with our recognition priming results, we did not find sequence memory to be impaired between the high-RPE event and its predecessor, but instead found worse sequence memory for pairs across a high-RPE event. Moreover, greater distance between events at encoding led to better sequence memory for events across a low-RPE event, but not a high-RPE event, suggesting separate mechanisms for the temporal ordering of events within versus across a latent reward context. Altogether, these findings demonstrate that high-RPE events are both more strongly encoded, show intact links with their predecessor, and act as event boundaries that interrupt the sequential integration of events. We captured these effects in a variant of the Context Maintenance and Retrieval model (CMR; Polyn, Norman, & Kahana, 2009), modified to incorporate RPEs into the encoding process.

Dataset Information

The human brain reactivates context-specific past information at event boundaries of naturalistic experiences.

Publications

The human brain reactivates context-specific past information at event boundaries of naturalistic experiences.

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