Cortical ripples during NREM sleep and waking in humans

Dickey, Charles W.; Verzhbinsky, Ilya A.; Jiang, Xi; Bq, Rosen; Kajfez, Sophie; Eskandar, Emad; González-Martínez, Jorge; Ss, Cash; Halgren, Eric

doi:10.1101/2021.05.11.443637

Cited by 10 publications

(3 citation statements)

References 87 publications

(122 reference statements)

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“…( 19 ) was the first to describe cortical high-frequency events (cortical ripples). They observed these events in default-mode network regions (prefrontal and retrosplenial cortex), as well as the PPC, and they tended to occur together with HPC-R. Later, these oscillations were also reported in human subjects ( 27 – 31 ). It was also shown that these co-occurring events became more common after learning ( 19 ).…”

Section: Discussionmentioning

confidence: 89%

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Aleman‐Zapata

Morris

Genzel

2022

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

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Memory reactivation during non–rapid-eye-movement ripples is thought to communicate new information to a systems-wide network and thus can be a key player mediating the positive effect of sleep on memory consolidation. Causal experiments disrupting ripples have only been performed in multiday training paradigms, which decrease but do not eliminate memory performance, and no comparison with sleep deprivation has been made. To enable such investigations, we developed a one-session learning paradigm in a Plusmaze and show that disruption of either sleep with gentle handling or hippocampal ripples with electrical stimulation impaired long-term memory. Furthermore, we detected hippocampal ripples and parietal high-frequency oscillations after different behaviors, and a bimodal frequency distribution in the cortical events was observed. Faster cortical high-frequency oscillations increased after normal learning, a change not seen in the hippocampal ripple-disruption condition, consistent with these having a role in memory consolidation.

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Section: Discussionmentioning

confidence: 89%

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Aleman‐Zapata

Morris

Genzel

2022

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

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“…However, thalamocortical connections are also very rare compared to cortico-cortical ( 36 ). Given the strong relationship of cortical ripples to upstates, and less strongly to sleep spindles ( 11 ), and the role of thalamocortical interactions in the generation of upstates and spindles ( 37 ), it is possible that thalamocortical modulation via sleep waves may contribute to cortico-cortical ripple synchronization.…”

Section: Discussionmentioning

confidence: 99%

“…We recently reported, using human intracranial recordings, that ∼70-ms-long, ∼90-Hz ripples are ubiquitous in all regions of the cortex during NREM as well as waking ( 11 ). During waking, cortical ripples occur on local high-frequency activity peaks.…”

mentioning

confidence: 99%

Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall

Dickey

Verzhbinsky

Jiang

et al. 2022

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

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Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such “binding” of different components of mental events into unified representations occurs is unknown. The “binding-by-synchrony” theory proposes that distributed encoding areas are bound by synchronous oscillations enabling enhanced communication. However, evidence for such oscillations is sparse. Brief high-frequency oscillations (“ripples”) occur in the hippocampus and cortex and help organize memory recall and consolidation. Here, using intracranial recordings in humans, we report that these ∼70-ms-duration, 90-Hz ripples often couple (within ±500 ms), co-occur (≥ 25-ms overlap), and, crucially, phase-lock (have consistent phase lags) between widely distributed focal cortical locations during both sleep and waking, even between hemispheres. Cortical ripple co-occurrence is facilitated through activation across multiple sites, and phase locking increases with more cortical sites corippling. Ripples in all cortical areas co-occur with hippocampal ripples but do not phase-lock with them, further suggesting that cortico-cortical synchrony is mediated by cortico-cortical connections. Ripple phase lags vary across sleep nights, consistent with participation in different networks. During waking, we show that hippocampo-cortical and cortico-cortical coripples increase preceding successful delayed memory recall, when binding between the cue and response is essential. Ripples increase and phase-modulate unit firing, and coripples increase high-frequency correlations between areas, suggesting synchronized unit spiking facilitating information exchange. co-occurrence, phase synchrony, and high-frequency correlation are maintained with little decrement over very long distances (25 cm). Hippocampo-cortico-cortical coripples appear to possess the essential properties necessary to support binding by synchrony during memory retrieval and perhaps generally in cognition.

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Replay, the default mode network and the cascaded memory systems model

et al. 2022

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The replay of patterns of activity related to past experiences and memories is a striking manifestation of brain spontaneous activity. So is the coherent activation of sets of brain areas during rest, in particular, the default mode network (DMN). We propose that these two phenomena are strongly intertwined: their potential functions overlap, encompassing the reinstatement, reprocessing, and consolidation of memories, and the simulation of potential outcomes of actions. In our cascaded memory systems model, we hypothesize that the DMN forms the backbone for the propagation of replay, mediating interactions between the hippocampus and the whole neocortex for consolidation of new memories. The DMN may independently ignite replay cascades, which support reactivation of older memories, or high-level semantic representations. Transient cortical activations, inducing long-range correlation across the neocortex, are a key mechanism supporting a hierarchy of representations, from simple percepts, to semantic representations of causes, to whole episodes. Recent data show that similar, feedback-driven phenomena are widespread in the cortex [39][40][41] .

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Cortical ripples during NREM sleep and waking in humans

Cited by 10 publications

References 87 publications

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day

Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall

Replay, the default mode network and the cascaded memory systems model

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