Replay of cortical spiking sequences during human memory retrieval

Vaz, Alex P.; Wittig, John H.; Inati, Sara K.; Zaghloul, Kareem A.

doi:10.1126/science.aba0672

Cited by 159 publications

(212 citation statements)

References 36 publications

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“…Revisitation fixations countered the typical pattern of looking towards novel rather than previously viewed scene content (24), suggesting sporadic guidance by memory retrieval, and enhanced learning, as indicated by better subsequent spatiotemporal memory. This interpretation is consonant with shifts in hippocampal states from pronounced theta oscillations during novel exploration, to theta-free epochs marked with sharp-wave ripple events (35) thought to support replay of prior experience (36). Eye-movement tracking therefore provided a marker of memory processing with the requisite temporal precision to resolve the behavioral ramifications of dynamic changes in hippocampal activity reflecting encoding versus retrieval that occur rapidly over a brief interval (34, 37), even during a single episode during which learning occurs for a novel stimulus.…”

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confidence: 71%

Rapid coordination of effective learning by the human hippocampus

Kragel

Schuele

VanHaerents

et al. 2020

Preprint

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Although the human hippocampus is necessary for long-term memory, controversial findings suggest that hippocampal computations support short-term memory in the service of guiding effective behaviors during learning. We tested the counter-intuitive theory that the hippocampus contributes to long-term memory through remarkably short-term processing, as reflected in the sequence of eye movements during encoding of naturalistic scenes. While viewing scenes for the first time, participants generated patterns of eye movements that reflected a shift from stimulus-driven to memory-driven viewing and signaled effective spatiotemporal memory formation. Hippocampal theta oscillations recorded from depth electrodes predicted this viewing pattern. Moreover, effective viewing patterns were preceded by shifts towards top-down influence of hippocampal theta on activity within cortical networks that support visual perception and visuospatial attention. The hippocampus thus supports short-term memory processing that coordinates perception, attention, and behavior in the service of effective spatiotemporal learning. These findings motivate re-interpretation of long-term memory disorders as reflecting loss of the organizing influence of hippocampal short-term memory on learning.

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confidence: 71%

Rapid coordination of effective learning by the human hippocampus

Kragel

Schuele

VanHaerents

et al. 2020

Preprint

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“…During exploratory ('online') periods a 5-10 Hz (theta) oscillation observed in the local field potential (LFP) of rodents temporally organizes the spatial receptive fields of hippocampal place cells 7 , which themselves show a bias towards over-representation of rewarded locations 8 . Conversely, during quiet resting ('offline' periods) hippocampal activity is organized into short (50 to 100 ms) sharp-wave/ripple (SWR) events which are associated with transient 125-225Hz LFP oscillations and the time-compressed replay of previously encoded hippocampal representations [9][10][11] . SWRrelated reactivation is in turn thought to support the offline consolidation of hippocampaldependent memory traces 2,3,12 .…”

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confidence: 99%

Offline Memory Reactivation Promotes the Consolidation Of Spatially Unbiased Long-Term Cognitive Maps

Grosmark

Sparks

Davis

et al. 2020

Preprint

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Spatial memories which can last a lifetime are thought to be encoded during 'online' periods of exploration and subsequently consolidated into stable cognitive maps through their 'offline' reactivation. However, the mechanisms and computational principles by which offline reactivation stabilize long-lasting spatial representations remain poorly understood. Here we employed simultaneous fast calcium imaging and electrophysiology to track hippocampal place cells over weeks of online spatial reward learning behavior and offline resting. We describe that recruitment to persistent network-level offline reactivation of spatial experiences predicts cells' future multi-day representational stability. Moreover, while representations of reward-adjacent locations are generally more stable across days, reactivation-related stabilization is, conversely, most prominent for reward-distal locations. Thus, while occurring on millisecond time-scales, offline reactivation counter-balances the observed multi-day representational reward-adjacency bias, promoting the stabilization of cognitive maps which comprehensively reflect entire underlying spatial contexts. These findings suggest that post-learning offline-related memory consolidation plays complimentary and computationally distinct role in learning as compared to online encoding.

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“…These sequences are replayed in a time-compressed fashion during sleep [97][98][99] , in a complex dialog between the hippocampus and the cortex [100][101][102][103] , to consolidate the memory of the 24 experience 104,105 . Further, these place cell sequences can be reactivated by cueing in sleep 103,[106][107][108] . Although replay like phenomena have not been observed in flies, cued reactivation during sleep improved recall in bees 109 , and reactivation during sleep of dopaminergic neurons involved in memory acquisition was shown to facilitate consolidation of courtship memory in flies 110 , suggesting that such replay-like processes might be detected in Drosophila too.…”

Section: Discussionmentioning

confidence: 99%

A conserved role for sleep in supporting spatial learning inDrosophila

Melnattur

Kirszenblat

Morgan

et al. 2020

Preprint

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Sleep loss and aging impair hippocampus-dependent spatial learning in mammalian systems.Here we use the fly Drosophila melanogaster to investigate the relationship between sleep and spatial learning in healthy and impaired flies. The spatial learning assay is modeled after the Morris Water Maze. The assay uses a 'thermal maze' consisting of a 5X5 grid of Peltier plates maintained at 36-37C and a visual panorama. The first trial begins when a single tile that is associated with a specific visual cue is cooled to 25°C. For subsequent trials, the cold tile is heated, the visual panorama is rotated and the flies must find the new cold-tile by remembering its association with the visual cue. Significant learning was observed with two different wild-type strains -Cs and 2U, validating our design. Sleep deprivation prior to training impaired spatial learning. Learning was also impaired in the classic learning mutant rutabaga (rut); enhancing sleep restored learning to rut mutants. Further we found that flies exhibited dramatic age-dependent cognitive decline in spatial learning starting at 20-24 days of age.These impairments could be reversed by enhancing sleep. Finally, we find that spatial learning requires dopaminergic signaling and that enhancing dopaminergic signaling in aged flies restored learning. Our results are consistent with the impairments seen in rodents and humans.These results thus demonstrate a critical conserved role for sleep in supporting spatial learning, and suggest potential avenues for therapeutic intervention during aging. STATEMENT OF SIGNIFICANCEWe have studied the relationship between sleep and plasticity using a Drosophila learning assay modified after the Morris Water Maze. Using this assay, we find that sleep loss impairs spatial learning. As in mammals, flies exhibited age-dependent spatial learning impairments.Importantly, the age-dependent impairments were reversed by enhancing sleep. Interestingly, our results mirror studies on hippocampus dependent memories in rodents and humans. Thus, our data describe an evolutionarily conserved role for sleep in regulating spatial learning. They also support augmenting sleep as a therapeutic strategy to ameliorate learning impairments.

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Replay of cortical spiking sequences during human memory retrieval

Cited by 159 publications

References 36 publications

Rapid coordination of effective learning by the human hippocampus

Rapid coordination of effective learning by the human hippocampus

Offline Memory Reactivation Promotes the Consolidation Of Spatially Unbiased Long-Term Cognitive Maps

A conserved role for sleep in supporting spatial learning inDrosophila

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