Local Sleep Oscillations: Implications for Memory Consolidation

Geva-Sagiv, Maya; Nir, Yuval

doi:10.3389/fnins.2019.00813

Cited by 56 publications

(69 citation statements)

References 93 publications

(133 reference statements)

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“…Additionally, widespread slow wave oscillations are thought to play a crucial role in the temporal coordination of discrete sleep-related events, such as hippocampal ripples and thalamo-cortical spindles, across a large network of brain regions (e.g. Nicola et al, 2019) Recent studies have shown that during wakeful behaviour the cerebellum is crucial for hippocampal place cell stability and efficient navigation (Rochefort et al, 2011;Lefort et al, 2019;Burguière et al, 2005, Babayan et al, 2017. Furthermore, the neuroanatomical connectivity required to support this influence has been recently described and physiological correlates of cerebello-hippocampal interaction identified 'online' during goal-directed navigation (Watson et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Delta oscillations coordinate intra-cerebellar and cerebello-hippocampal network dynamics during sleep

Torres-Herraez

Watson

Rondi-Reig

2021

Preprint

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During sleep, the widespread coordination of neuronal oscillations across both cortical and subcortical brain regions is thought to support various physiological functions, including memory consolidation. However, how sleep-related activity within the brain’s largest sensorimotor structure, the cerebellum, is multiplexed with well described sleep-related mechanisms in regions such as the hippocampus remains unknown.To address this gap in knowledge, we simultaneously recorded from the dorsal hippocampus and three distinct regions of the cerebellum (Crus I, lobule VI and lobules II/III) during natural murine sleep. We found that LFP oscillations are coordinated between the two structures in a sleep-stage specific manner. Particularly during non-REM sleep, prominent delta frequency coherence was observed between lobule VI and hippocampus. We additionally observed that non-REM associated hippocampal sharp wave ripple activity can drive discrete LFP modulation in all the recorded cerebellar regions, with the shortest latency effects observed in lobule VI.We also describe discrete phasic sharp potentials, synchronized across cerebellar regions, which were strongly phase locked to the peak of ongoing cerebellar delta oscillations and found in greatest numbers during REM. These phasic sharp potentials recorded within the cerebellar cortex were found to be phase-locked to the trough of the hippocampal theta oscillation, further suggesting cross-structural coordination. During REM, cerebellar delta oscillation phase significantly modulated hippocampal theta frequency, and this effect was greatest when phasic sharp potentials were most abundant. Within all three cerebellar regions, prominent LFP oscillations were observed at both low (delta, <4 Hz) and very high frequencies (~ 250 Hz) during non-REM and REM sleep. Intra-cerebellar cross-frequency analysis revealed that delta frequency oscillations strongly modulate those in the very high frequency range.Together, these results reveal multiple candidate physiological mechanisms to support ‘offline’, bi-directional interaction within distributed cerebello-hippocampal networks. In particular, we describe a prominent cerebellar delta oscillation, which appears to act as a temporal coordinator of cerebellar activity at both local (intra-cerebellar) and distributed (cerebello-hippocampal) network levels.

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Section: Introductionmentioning

confidence: 99%

Delta oscillations coordinate intra-cerebellar and cerebello-hippocampal network dynamics during sleep

Torres-Herraez

Watson

Rondi-Reig

2021

Preprint

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“…The prominence of SO indicates the N3 stage, and the occurrence of SPs indicates the N2 stage [26]. Furthermore, the evidence suggests that SP nested in the up phase of the SO may play a role in memory consolidation [10]. A SWS model, including SOs and SPs, presents advantages to characterize the conditions promoting their co-occurrence.…”

Section: Resultsmentioning

confidence: 99%

Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

Torres

Orio

Escobar

2021

Preprint

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Slow-wave sleep cortical brain activity, conformed by slow-oscillations and sleep spindles, plays a key role in memory consolidation. The increase of the power of the slow-wave events, obtained by auditory sensory stimulation, positively correlates to memory consolidation performance. However, little is known about the experimental protocol maximizing this effect, which could be induced by the power of slow-oscillation, the number of sleep spindles, or the timing of both events' co-occurrence. Using a mean-field model of thalamocortical activity, we studied the effect of several stimulation protocols, varying the pulse shape, duration, amplitude, and frequency, as well as a target-phase using a closed-loop approach. We evaluated the effect of these parameters on slow-oscillations (SO) and sleep-spindles (SP), considering: (i) the power at the frequency bands of interest, (ii) the number of SO and SP, (iii) co-occurrences between SO and SP, and (iv) synchronization of SP with the up-peak of the SO. The first three targets are maximized using a decreasing ramp pulse with a pulse duration of 50 ms. Also, we observed a reduction in the number of SO when increasing the stimulus energy by rising its amplitude. To assess the target-phase parameter, we applied closed-loop stimulation at 0º, 45º, and 90º of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0º stimulation produces better results in the power and number of SO and SP than the rhythmic or aleatory stimulation. On the other hand, stimulating at 45º or 90º change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0º phase. Finally, we propose the application of closed-loop stimulation at the rising zero-cross point using pulses with a decreasing ramp shape and 50 ms of duration for future experimental work.

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“…It is also possible that the tDCS-induced slow waves and spindles are different from the naturally occurring, endogenous slow waves and spindles that are known to mediate memory consolidation during sleep. Slow waves and spindles vary substantially with respect to their distributions and trajectories on the scalp [ 87 ]. It may be that tDCS only induced a specific set of oscillations, e.g., over temporal regions, that do not contribute to memory consolidation.…”

Section: Discussionmentioning

confidence: 99%

Bi-Temporal Anodal Transcranial Direct Current Stimulation during Slow-Wave Sleep Boosts Slow-Wave Density but Not Memory Consolidation

et al. 2021

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Slow-wave sleep (SWS) has been shown to promote long-term consolidation of episodic memories in hippocampo–neocortical networks. Previous research has aimed to modulate cortical sleep slow-waves and spindles to facilitate episodic memory consolidation. Here, we instead aimed to modulate hippocampal activity during slow-wave sleep using transcranial direct current stimulation in 18 healthy humans. A pair-associate episodic memory task was used to evaluate sleep-dependent memory consolidation with face–occupation stimuli. Pre- and post-nap retrieval was assessed as a measure of memory performance. Anodal stimulation with 2 mA was applied bilaterally over the lateral temporal cortex, motivated by its particularly extensive connections to the hippocampus. The participants slept in a magnetic resonance (MR)-simulator during the recordings to test the feasibility for a future MR-study. We used a sham-controlled, double-blind, counterbalanced randomized, within-subject crossover design. We show that stimulation vs. sham significantly increased slow-wave density and the temporal coupling of fast spindles and slow-waves. While retention of episodic memories across sleep was not affected across the entire sample of participants, it was impaired in participants with below-average pre-sleep memory performance. Hence, bi-temporal anodal direct current stimulation applied during sleep enhanced sleep parameters that are typically involved in memory consolidation, but it failed to improve memory consolidation and even tended to impair consolidation in poor learners. These findings suggest that artificially enhancing memory-related sleep parameters to improve memory consolidation can actually backfire in those participants who are in most need of memory improvement.

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Local Sleep Oscillations: Implications for Memory Consolidation

Cited by 56 publications

References 93 publications

Delta oscillations coordinate intra-cerebellar and cerebello-hippocampal network dynamics during sleep

Delta oscillations coordinate intra-cerebellar and cerebello-hippocampal network dynamics during sleep

Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

Bi-Temporal Anodal Transcranial Direct Current Stimulation during Slow-Wave Sleep Boosts Slow-Wave Density but Not Memory Consolidation

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