Fast Sequences of Non-spatial State Representations in Humans

Kurth‐Nelson, Zeb; Economides, Marcos; Dolan, Raymond J.; Dayan, Peter

doi:10.1016/j.neuron.2016.05.028

Cited by 180 publications

(328 citation statements)

References 67 publications

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“…Vivid episodic memories in people have been characterized as the replay of multiple unique events in sequential order [1–3]. The hippocampus plays a critical role in episodic memories in both people and rodents [2, 4–6].…”

Section: Resultsmentioning

confidence: 99%

Replay of Episodic Memories in the Rat

et al. 2018

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Vivid episodic memories in people have been characterized as the replay of multiple unique events in sequential order [1-3]. The hippocampus plays a critical role in episodic memories in both people and rodents [2, 4-6]. Although rats remember multiple unique episodes [7, 8], it is currently unknown if animals "replay" episodic memories. Therefore, we developed an animal model of episodic memory replay. Here, we show that rats can remember a trial-unique stream of multiple episodes and the order in which these events occurred by engaging hippocampal-dependent episodic memory replay. We document that rats rely on episodic memory replay to remember the order of events rather than relying on non-episodic memories. Replay of episodic memories survives a long retention-interval challenge and interference from the memory of other events, which documents that replay is part of long-term episodic memory. The chemogenetic activating drug clozapine N-oxide (CNO), but not vehicle, reversibly impairs episodic memory replay in rats previously injected bilaterally in the hippocampus with a recombinant viral vector containing an inhibitory designer receptor exclusively activated by a designer drug (DREADD; AAV8-hSyn-hM4Di-mCherry). By contrast, two non-episodic memory assessments are unaffected by CNO, showing selectivity of this hippocampal-dependent impairment. Our approach provides an animal model of episodic memory replay, a process by which the rat searches its representations in episodic memory in sequential order to find information. Our findings using rats suggest that the ability to replay a stream of episodic memories is quite old in the evolutionary timescale.

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Section: Resultsmentioning

confidence: 99%

Replay of Episodic Memories in the Rat

et al. 2018

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“…Perhaps understanding how SWR sequences mesh episodes coherently (e.g., adjacent trajectories but not separated ones) may shed light on how human episodic constructive memory works (e.g., meshing memories of oneself at in the grandmother's house and of oneself at a past children's party to imagine how a children's party at the grandmother's house would be). Progress in the field may come from studies that directly probe sequential activity resembling SWR or theta sequences during human cognitive processing, possibly designed to test (and disentangle) alternative computational models.…”

Section: Resultsmentioning

confidence: 99%

Internally generated hippocampal sequences as a vantage point to probe future‐oriented cognition

Pezzulo

Kemere

Meer

2017

Annals of the New York Academy of Sciences

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Information processing in the rodent hippocampus is fundamentally shaped by internally generated sequences (IGSs), expressed during two different network states: theta sequences, which repeat and reset at the ∼8 Hz theta rhythm associated with active behavior, and punctate sharp wave-ripple (SWR) sequences associated with wakeful rest or slow-wave sleep. A potpourri of diverse functional roles has been proposed for these IGSs, resulting in a fragmented conceptual landscape. Here, we advance a unitary view of IGSs, proposing that they reflect an inferential process that samples a policy from the animal's generative model, supported by hippocampus-specific priors. The same inference affords different cognitive functions when the animal is in distinct dynamical modes, associated with specific functional networks. Theta sequences arise when inference is coupled to the animal's action-perception cycle, supporting online spatial decisions, predictive processing, and episode encoding. SWR sequences arise when the animal is decoupled from the action-perception cycle and may support offline cognitive processing, such as memory consolidation, the prospective simulation of spatial trajectories, and imagination. We discuss the empirical bases of this proposal in relation to rodent studies and highlight how the proposed computational principles can shed light on the mechanisms of future-oriented cognition in humans.

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“…Research in rodents suggests that replay can occur in either a forward or backward manner (Ambrose, Pfeiffer, & Foster, ), which may serve different functions for adaptive behavior. In humans, there are some initial indications from MEG that recently learned nonspatial sequences may be reinstated in a backward manner (Kurth‐Nelson, Economides, Dolan, & Dayan, ). One interesting future direction would be to explore whether these bidirectional replay processes not only exist in humans but also support the proactive and retroactive temporal memory integration processes described here.…”

Section: Retroactive Mechanisms Of Binding Sequential Memory Represenmentioning

confidence: 99%

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

2019

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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.

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Fast Sequences of Non-spatial State Representations in Humans

Cited by 180 publications

References 67 publications

Replay of Episodic Memories in the Rat

Replay of Episodic Memories in the Rat

Internally generated hippocampal sequences as a vantage point to probe future‐oriented cognition

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

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