Spontaneous slow oscillation—slow spindle features predict induced overnight memory retention

Abstract

Study Objectives Synchronization of neural activity within local networks and between brain regions is a major contributor to rhythmic field potentials such as the EEG. On the other hand, dynamic changes in microstructure and activity are reflected in the EEG, for instance slow oscillation (SO) slope can reflect synaptic strength. SO-spindle coupling is a measure for neural communication. It was previously associated with memory consolidation, but also shown to reveal strong inter-individual differences. In studies, weak electric current stimulation has modulated brain rhythms and memory retention. Here we investigate whether SO-spindle coupling and SO slope during baseline sleep are associated with (predictive of) stimulation efficacy on retention performance. Methods Twenty-five healthy subjects participated in three experimental sessions. Sleep-associated memory consolidation was measured in two sessions, in one anodal transcranial direct current stimulation oscillating at subjects individual SO frequency (so-tDCS) was applied during nocturnal sleep. The third session was without a learning task (baseline sleep). The dependence on SO-spindle coupling and SO-slope during baseline sleep of so-tDCS efficacy on retention performance were investigated. Results Stimulation efficacy on overnight retention of declarative memories was associated with nesting of slow spindles to SO trough in deep non-rapid eye movement baseline sleep. Steepness and direction of SO slope in baseline sleep were features indicative for stimulation efficacy. Conclusions Findings underscore a functional relevance of activity during the SO up-to-down state transition for memory consolidation and provide support for distinct consolidation mechanisms for types of declarative memories.

Application of Transcranial Direct Current Stimulation in Sleep Disturbances

“…Slow oscillatory tDCS (so-tDCS) studies have been conducted based on this hypothesis. However, some recent studies have indicated that so-tDCS does not improve memory consolidation despite increasing SWA and spindle activity [66][67][68][69]; however, any definite conclusions could be controversial and there is therefore a need for further refinement [70,71]. Saebipour et al [65] conducted a study of the application of so-tDCS (0.75 Hz) with an intensity ranging from 0 to 260 μA during stage 2 of NREM sleep in six patients with either sleep maintenance or non-restorative sleep insomnia with the goal of resonating their brain waves to the frequency of sleep slow-wave.…”

Enhancement of hippocampal-thalamocortical temporal coordination during slow-frequency long-duration anterior thalamic spindles

“…In addition the differential topographical distribution of slow and fast spindles in humans has not been observed in rodents (Kim et al, 2015). Unlike the human EEG/LFP spectrum in which both slow and fast spindle peaks are distinguishable (Dehnavi et al, 2021; Andrillon et al, 2011), the rodents spectrum shows no distinct peak at the spindle frequency range (7–15 Hz). (Mölle et al, 2009) so that distinguishing fast and slow spindles from the spectrum is not possible in rodents.…”

“…The method to calculate phase amplitude coupling was similar to the previous papers (Staresina et al, 2015; Dehnavi et al, 2021). First time–frequency representations (TFRs) were calculated for every spindle event by mtmconvol function of the FieldTrip toolbox (Oostenveld et al, 2011) with frequency steps of 0.25 Hz in the frequency range of 5-300 Hz.…”

“…A wide frequency range of 7-15 Hz are typically considered for spindles in rodents. Within this frequency band in human sleep slow and fast spindles with differential properties and functional relevance for memory consolidation are discriminated (Fernandez and Lüthi, 2020; Klinzing et al, 2016; Ayoub et al, 2013; Dehnavi et al, 2021; Hashemi et al, 2019). We hypothesize that the precise temporal modulation of CA1 units/ripples with spindles is frequency dependent so that spindles with lower frequencies provide longer windows of opportunity for cross-regional synchronization and information transfer.…”

Night Moves and Modes: Sleep Biomarkers for Neurocognitive Disorders

“…1–3 Impaired phase coupling of sleep spindles, slow oscillations, and hippocampal ripples during NREM sleep have been shown to correlate with impaired overnight memory consolidation. 4 Amyloid-beta burden can be predicted by reduced amplitude of 1 Hz slow wave activity in NREM 3. 2,3 Tau deposition and selective atrophy of the mesial temporal lobe in cognitively healthy older adults has been shown to correlate with impaired spindle-slow oscillation coupling and memory consolation.…”