Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval

Carr, Margaret F.; Jadhav, Shantanu P.; Frank, Loren M.

doi:10.1038/nn.2732

Cited by 823 publications

(899 citation statements)

References 80 publications

(139 reference statements)

Supporting

Mentioning

835

Contrasting

Unclassified

Order By: Relevance

“…One possibility may be that theta and highgamma activity coordinate separate processes relevant for memory, such as attention or semantic processing, and that these processes occur separately in time during encoding and simultaneously during retrieval. However, another possibility is that the observed temporal compression complements previous studies suggesting that retrieval reactivates internal representations of an experience on a faster timescale than the original experience (33,34).…”

Section: Discussionsupporting

confidence: 70%

Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval

Yaffe

Kerr

Damera³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

138

134

View full text Add to dashboard Cite

Reinstatement of neural activity is hypothesized to underlie our ability to mentally travel back in time to recover the context of a previous experience. We used intracranial recordings to directly examine the precise spatiotemporal extent of neural reinstatement as 32 participants with electrodes placed for seizure monitoring performed a paired-associates episodic verbal memory task. By cueing recall, we were able to compare reinstatement during correct and incorrect trials, and found that successful retrieval occurs with reinstatement of a gradually changing neural signal present during encoding. We examined reinstatement in individual frequency bands and individual electrodes and found that neural reinstatement was largely mediated by temporal lobe theta and high-gamma frequencies. Leveraging the high temporal precision afforded by intracranial recordings, our data demonstrate that high-gamma activity associated with reinstatement preceded theta activity during encoding, but during retrieval this difference in timing between frequency bands was absent. Our results build upon previous studies to provide direct evidence that successful retrieval involves the reinstatement of a temporal context, and that such reinstatement occurs with precise spatiotemporal dynamics.R einstatement of neural activity is hypothesized to underlie our ability to recover the internal representation of a previous experience, a process described as mental time travel (1-4). These internal representations, which may reflect the external environment or internal mental states, form the context in which an episodic memory is embedded. Central to the hypothesis of mental time travel is that context representations in the brain gradually change over time, and that successful retrieval of an episodic memory involves mentally jumping back in time to reexperience a particular context (5-8). Consistent with this paradigm, when an episode is successfully retrieved from memory, the memory for neighboring episodes that occurred close in time is enhanced, an effect known as contiguity (9). However, despite substantial behavioral data supporting this hypothesis, a number of important yet unanswered questions remain regarding its underlying neural mechanisms.Empiric support for neural reinstatement has largely emerged from functional MRI (fMRI) studies that have used multivoxel pattern analysis (MVPA) (10-12). MVPA relies on classifying neural activity during retrieval to dissociate broad manipulations such as category or task that are present during encoding (13-16). MVPA, however, is unable to directly examine whether successful retrieval reinstates the neural representations of individual items. Representational similarity analysis supports neural reinstatement of individual stimuli (17-19), but this alternative fMRI approach does not examine to what extent retrieval reinstates a changing neural representation of context. In addition, the limited temporal resolution of fMRI studies makes them unable to identify the precise spatiotemporal dynamics o...

show abstract

Section: Discussionsupporting

confidence: 70%

Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval

Yaffe

Kerr

Damera³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

138

134

View full text Add to dashboard Cite

show abstract

“…The relationship between the stimulus-induced and ongoing cortical activity revealed in our study has certain similarities with the "replay" of neuronal activity in neural circuits mediating episodic (9,24,43) and sensorimotor (44) learning. In those studies, the temporal firing patterns of multiple neurons during learning are repeated either during sleep (9,43,44) or in the awake state (25).…”

Section: Discussionsupporting

confidence: 54%

“…Indeed, sleep or anesthetized states are characterized by high synchronous activity due to widespread oscillations in the same frequency band and a global decrease in brain activity (23). Conversely, awake reactivation has been recently demonstrated during quiescent periods in hippocampal cells (24)(25)(26)(27)(28), and it has been shown to be influenced by the animal's current location (25)(26)(27)29), to occur with elevated precision in novel environments (25,29), and to represent pathways not previously experienced by the animal (28). Furthermore, a more recent study (22) found reactivation in awake rat visual cortical cells in response to a moving dot stimulus swept across a linear path of adjacent receptive fields following a conditioning period.…”

mentioning

confidence: 99%

Image sequence reactivation in awake V4 networks

Eagleman

Dragoi

2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

In the absence of sensory input, neuronal networks are far from being silent. Whether spontaneous changes in ongoing activity reflect previous sensory experience or stochastic fluctuations in brain activity is not well understood. Here we describe reactivation of stimulusevoked activity in awake visual cortical networks. We found that continuous exposure to randomly flashed image sequences induces reactivation in macaque V4 cortical networks in the absence of visual stimulation. This reactivation of previously evoked activity is stimulusspecific, occurs only in the same temporal order as the original response, and strengthens with increased stimulus exposures. Importantly, cells exhibiting significant reactivation carry more information about the stimulus than cells that do not reactivate. These results demonstrate a surprising degree of experience-dependent plasticity in visual cortical networks as a result of repeated exposure to unattended information. We suggest that awake reactivation in visual cortex may underlie perceptual learning by passive stimulus exposure.electrophysiology | monkey

show abstract

“…Regions associated with episodic memory that are engaged during memory task performance have been observed to be active even during rest, reflecting ongoing reinstatement of episodic memories (Wilson & McNaughton, 1994;Carr et al, 2011;Jadhav et al, 2012). These memory reinstatements can lead to the incidental reinstatement of the context in which the memories were experienced (Bornstein & Norman, 2017).…”

Section: Ddm Resultsmentioning

confidence: 99%

Refresh my memory: Episodic memory reinstatements intrude on working memory maintenance

Hoskin

Bornstein

Norman

et al. 2017

Preprint

View full text Add to dashboard Cite

A fundamental question in memory research is how different forms of memory interact. Previous research has shown that when working memory (WM) is overloaded or maintenance is interrupted in short-term memory tasks, humans and animals can rely on episodic memory (EM) to support performance. Furthermore, episodic memory reactivation appears also to occur on its own (i.e., irrespective of demand), even during the short delays typically used in WM experiments. Based on these observations, we hypothesized that EM reinstatements would affect WM, even in the absence of any interference. Using novel behavioral and neural signatures of the effect of EM on WM, we show that EM introduces additional information into WM by reinstating incidental associations (context) present during initial encoding. The first two experiments establish that the influence of encoding context is evident both in errors (Experiment 1) and in slowing of responses (Experiment 2). Experiment 3 shows that fMRI evidence of EM reinstatement during the delay predicts response times on each trial. Modeling WM search using a Drift-Diffusion Model (DDM), we show that fits improve when trial drift rate varies with fMRI evidence for reinstatement during that trial's delay period. These results expose a previously hidden interaction between WM maintenance and EM replay, and raise new questions about the adaptive nature of the interplay between these mechanisms.

show abstract

Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval

Cited by 823 publications

References 80 publications

Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval

Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval

Image sequence reactivation in awake V4 networks

Refresh my memory: Episodic memory reinstatements intrude on working memory maintenance

Contact Info

Product

Resources

About