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

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.