Working memory enhancement using real-time phase-tuned transcranial alternating current stimulation
David Haslacher, Alessia Cavallo, Philipp Reber, Anna Kattein, Moritz Thiele, Khaled Nasr, Kimia Hashemi, Rodika Sokoliuk, Gregor Thut, Surjo R. Soekadar
Abstract
BACKGROUND: Prior work has shown that transcranial alternating current stimulation (tACS) of parietooccipital alpha oscillations (8-14 Hz) can modulate working memory (WM) performance as a function of the phase lag to endogenous oscillations. However, leveraging this effect using real-time phase-tuned tACS has not been feasible so far due to stimulation artifacts preventing continuous phase tracking. OBJECTIVES AND HYPOTHESIS: We aimed to develop a system that tracks and adapts the phase lag between tACS and ongoing parietooccipital alpha oscillations in real-time. We hypothesized that such real-time phase-tuned tACS enhances working memory performance, depending on the phase lag. METHODS: We developed real-time phase-tuned closed-loop amplitude-modulated tACS (CLAM-tACS) targeting parietooccipital alpha oscillations. CLAM-tACS was applied at six different phase lags relative to ongoing alpha oscillations while participants (N = 21) performed a working memory task. To exclude that behavioral effects of CLAM-tACS were mediated by other factors such as sensory co-stimulation, a second group of participants (N = 25) received equivalent stimulation of the forehead. RESULTS: WM accuracy improved in a phase lag dependent manner (p = 0.0350) in the group receiving parietooccipital stimulation, with the strongest enhancement observed at 330° phase lag between tACS and ongoing alpha oscillations (p = 0.00273, d = 0.976). Moreover, across participants, modulation of frontoparietal alpha oscillations correlated both in amplitude (p = 0.0248) and phase (p = 0.0270) with the modulation of WM accuracy. No such effects were observed in the control group receiving frontal stimulation. CONCLUSIONS: Our results demonstrate the feasibility and efficacy of real-time phase-tuned CLAM-tACS in modulating both brain activity and behavior, thereby paving the way for further investigation into brain-behavior relationships and the exploration of innovative therapeutic applications.