Thalamic Spindles Promote Memory Formation during Sleep through Triple Phase-Locking of Cortical, Thalamic, and Hippocampal Rhythms

Latchoumane, Charles; Ngo, Hong‐Viet V.; Born, Jan; Shin, Hee‐Sup

doi:10.1016/j.neuron.2017.06.025

Cited by 456 publications

(543 citation statements)

References 61 publications

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“…Sleep promotes the consolidation of new memories and underlying synaptic refinements (Diekelmann & Born, ). More specifically, sleep‐specific brain oscillations during non‐rapid eye movement (NREM) sleep in the form of electroencephalographic (EEG) slow oscillations (SO; 0.16–1.25 Hz) and sleep spindles (sigma range, 12–16 Hz) and, potentially, their coordinated interplay have been linked to memory and synaptic plasticity (Latchoumane, Ngo, Born, & Shin, ; Rasch & Born, ; Staresina et al., ), but the impact needs to be specified.…”

Section: Introductionmentioning

confidence: 99%

Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Mikutta

Feige

Maier

et al. 2019

Journal of Sleep Research

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Initially independent lines of research suggest that sleep‐specific brain activity patterns, observed as electroencephalographic slow oscillatory and sleep spindle activity, promote memory consolidation and underlying synaptic refinements. Here, we further tested the emerging concept that specifically the coordinated interplay of slow oscillations and spindle activity (phase‐amplitude coupling) support memory consolidation. Particularly, we associated indices of the interplay between slow oscillatory (0.16–1.25 Hz) and spindle activity (12–16 Hz) during non‐rapid eye movement sleep (strength [modulation index] and phase degree of coupling) in 20 healthy adults with parameters of overnight declarative (word‐list task) and procedural (mirror‐tracing task) memory consolidation. The pattern of results supports the notion that the interplay between oscillations facilitates memory consolidation. The coincidence of the spindle amplitude maximum with the up‐state of the slow oscillation (phase degree) was significantly associated with declarative memory consolidation (r = .65, p = .013), whereas the overall strength of coupling (modulation index) correlated with procedural memory consolidation (r = .45, p = .04). Future studies are needed to test for potential causal effects of the observed association between neural oscillations during sleep and memory consolidation, and to elucidate ways of modulating these processes, for instance through non‐invasive brain‐stimulation techniques.

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Section: Introductionmentioning

confidence: 99%

Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Mikutta

Feige

Maier

et al. 2019

Journal of Sleep Research

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“…However, local PAC exists for other frequency pairs (26), with SOs exerting particularly powerful drives not only over spindle and ripple activity, but also over delta (49), theta (50), and gamma (36,38) components. Extending the notion of local PAC to cross-regional interactions, the phase of a slower rhythm in one brain structure may modulate expression of faster activity at the other site (24,47,51), thus constituting a second potential form of HPC-NC communication.…”

Section: Introductionmentioning

confidence: 99%

Phase-based coordination of hippocampal and neocortical oscillations during human sleep

Cox

Rüber

Staresina

et al. 2019

Preprint

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AbstractDuring sleep, new memories undergo a gradual transfer from the hippocampus (HPC) to the neocortex (NC). Precisely timed neural oscillations interacting within and between these brain structures are thought to mediate this sleep-dependent memory consolidation, but exactly which sleep oscillations instantiate the HPC-NC dialog, and via what mechanisms, remains elusive. Employing invasive electroencephalography in ten neurosurgical patients across a full night of sleep, we identified three broad classes of phase-based HPC-NC communication. First, we observed interregional phase synchrony for non-rapid eye movement (NREM) spindles, N2 and rapid eye movement (REM) theta, and N3 beta activity. Second, and most intriguingly, we found asymmetrical N3 cross-frequency phase-amplitude coupling between HPC SOs and NC activity spanning the delta to high-gamma/ripple bands, but not in the opposite direction. Lastly, N2 theta and NREM spindle synchrony were themselves modulated by HPC SOs. These novel forms of phase-based interregional communication emphasize the role of HPC SOs in the HPC-NC dialog, and may offer a physiological basis for the sleep-dependent reorganization of mnemonic content.

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“…They appear in NonREM sleep (NonREM for "non-rapid eye movement") and are most prominent in sleep stage 2. Beyond their supposed role in maintaining sleep, spindles are thought to be involved in the reactivation of recent memories during sleep and to be mainly responsible for the sleep-dependent plasticity in the neocortex (Bergmann, Mölle, Diedrichs, Born, & Siebner, 2012;Latchoumane, Ngo, Born, & Shin, 2017;Mölle, Marshall, Gais, & Born, 2002;Niethard, Burgalossi, & Born, 2017;Rasch & Born, 2013;Rosanova & Ulrich, 2005;Steriade, 1999).…”

mentioning

confidence: 99%

The reciprocal relation between sleep and memory in infancy: Memory‐dependent adjustment of sleep spindles and spindle‐dependent improvement of memories

Friedrich

Mölle

Friederici

et al. 2018

Developmental Science

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Sleep spindle activity in infants supports their formation of generalized memories during sleep, indicating that specific sleep processes affect the consolidation of memories early in life. Characteristics of sleep spindles depend on the infant's developmental state and are known to be associated with trait-like factors such as intelligence. It is, however, largely unknown which state-like factors affect sleep spindles in infancy. By varying infants' wake experience in a within-subject design, here we provide evidence for a learning- and memory-dependent modulation of infant spindle activity. In a lexical-semantic learning session before a nap, 14- to 16-month-old infants were exposed to unknown words as labels for exemplars of unknown object categories. In a memory test on the next day, generalization to novel category exemplars was tested. In a nonlearning control session preceding a nap on another day, the same infants heard known words as labels for exemplars of already known categories. Central-parietal fast sleep spindles increased after the encoding of unknown object-word pairings compared to known pairings, evidencing that an infant's spindle activity varies depending on its prior knowledge for newly encoded information. Correlations suggest that enhanced spindle activity was particularly triggered, when similar unknown pairings were not generalized immediately during encoding. The spindle increase triggered by previously not generalized object-word pairings, moreover, boosted the formation of generalized memories for these pairings. Overall, the results provide first evidence for a fine-tuned regulation of infant sleep quality according to current consolidation requirements, which improves the infant long-term memory for new experiences.

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Thalamic Spindles Promote Memory Formation during Sleep through Triple Phase-Locking of Cortical, Thalamic, and Hippocampal Rhythms

Cited by 456 publications

References 61 publications

Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Phase-based coordination of hippocampal and neocortical oscillations during human sleep

The reciprocal relation between sleep and memory in infancy: Memory‐dependent adjustment of sleep spindles and spindle‐dependent improvement of memories

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