Beyond "more synchrony": Frequency- and phase-specific effects of fronto-parietal theta tACS in enhancing episodic...

Theta oscillations support episodic memory and long-range communication between prefrontal and parietal regions. Transcranial alternating current stimulation (tACS) offers a way to test how theta dynamics influence memory. In our previous work, stimulation 1 Hz below the individual theta frequency (ITF-1) improved episodic memory, and this improvement was correlated with changes in fronto-parietal connectivity. Here, we tested whether dual-site fronto-parietal theta tACS produces frequency- and phase-specific aftereffects on episodic memory and theta-network dynamics. Neurotypical adults (N = 42) were assigned to ITF-1 or ITF+1 groups, with ITF estimated from pre-tACS resting-state EEG. Participants completed three counterbalanced sessions of dual-site tACS over left prefrontal and posterior-parietal locations: in-phase, anti-phase, and sham. Pre- and post-stimulation assessments included episodic memory measures, namely free recall and temporal order judgment (TOJ) with confidence ratings, as well as EEG recordings. TOJ accuracy showed a significant Session × Group interaction, driven by greater improvement in ITF-1 than ITF+1 following anti-phase stimulation. In ITF-1, confidence-accuracy discrimination (metacognitive separation) decreased after in-phase relative to anti-phase and sham. Resting-state, but not event-related, theta connectivity showed an anti-phase-specific divergence in fronto-parietal coupling, increasing in ITF-1 and decreasing in ITF+1. Within ITF-1 anti-phase, larger increases in resting-state fronto-parietal connectivity were associated with greater TOJ gains. These findings indicate phase-, frequency, and state-specific modulation of episodic memory and fronto-parietal theta networks by tACS. While the behavioral advantage of lower-frequency stimulation aligned with our hypothesis, the selective benefit of anti-phase stimulation suggests a more flexible, task-dependent reconfiguration of long-range connectivity rather than a uniform increase in synchrony.