Polarity-dependent modulation of sleep oscillations and cortical excitability in aging

TL;DR

This study shows that anodal tDCS improves sleep-related brain activity linked to memory in older adults, while cathodal tDCS does not, and that individual differences like chronotype matter.

Contribution

The study reveals that anodal tDCS enhances sleep oscillations more effectively than cathodal tDCS in older adults, challenging prior assumptions about polarity effects.

Findings

Anodal so-tDCS improved SO-spindle synchrony and spindle power in participants with intermediate or evening chronotypes.

Cathodal so-tDCS prolonged SO down-states but did not enhance oscillatory measures compared to sham.

Anodal so-tDCS increased cortical excitability, while cathodal so-tDCS did not shift the E/I balance as expected.

Abstract

During non-rapid eye movement (NREM) sleep, cortical slow oscillation (SO; <1 Hz) and thalamic sleep spindle activity (12–15 Hz) interact through precise phase coupling to support memory consolidation. Slow oscillatory transcranial direct current stimulation (so-tDCS) can modulate these oscillations. Traditionally, anodal so-tDCS is used to depolarize the cortex during SO up-states, thereby promoting SO activity and SO-spindle coupling. However, intracranial findings suggest that SO down-states, characterized by cortical hyperpolarization, can trigger thalamic spindle bursts. This raises the hypothesis that cathodal so-tDCS, by promoting hyperpolarization, could selectively enhance down-states and more effectively improve SO-spindle coupling.

We tested this hypothesis in 22 healthy older adults, a population known to exhibit diminished NREM oscillatory activity. Each participant received cathodal, anodal, and sham so-tDCS in separate nap sleep sessions. We quantified SO and spindle characteristics, their temporal coupling, and cortical excitation/inhibition (E/I) balance using EEG spectral slope. We also assessed individual circadian preference (chronotype) as a potential moderator.

We found that anodal so-tDCS improved SO-spindle synchrony and increased spindle power over sham in participants with intermediate or evening chronotypes, while cathodal so-tDCS did not enhance these oscillatory measures compared to sham, despite prolonging SO down-states. Anodal so-tDCS also shifted E/I balance toward increased excitability, indicating increased cortical excitability, whereas cathodal so-tDCS did not produce the anticipated opposite shift.

In summary, anodal, but not cathodal, so-tDCS effectively enhanced thalamocortical interactions underlying memory consolidation. Furthermore, these findings highlight the importance of individual factors such as chronotype in brain stimulation responsiveness.

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