Effects of Frontoparietal Theta tACS on Verbal Working Memory: Behavioral and Neurophysiological Analysis

Abstract

Left-lateralized frontoparietal theta oscillations are thought to play an important role in verbal working memory. We causally tested this idea by stimulating the frontoparietal theta network at individual theta frequencies (4 to 8 Hz) during verbal working memory and observing the subsequent behavioral and neurophysiological effects. Weak electric currents were delivered via two 4×1 HD electrode arrays centered at F3 and P3. Three stimulation configurations, including in-phase, anti-phase, or sham, were tested on three different days in a cross-over design. On each test day, the subject underwent three experimental sessions: pre-, during- and post-stimulation sessions. In all sessions, the subject performed a Sternberg verbal working memory task with three levels of memory load (load 2, 4 and 6), imposing three levels of cognitive demand. Analyzing behavioral, EEG, and pupillometry data from the post-stimulation sessions, we report three results. First, in-phase stimulation improved task performance only in subjects with higher working memory capacity (WMC) and under higher memory load (load 6). Second, in-phase stimulation enhanced frontoparietal theta synchrony during working memory retention only in subjects with higher WMC under higher memory loads (load 4 and load 6), and the enhanced frontoparietal theta synchronization is mainly driven by enhanced frontal→parietal theta Granger causality. Third, the pupil diameter was not different irrespective of whether the preceding stimulation was in-phase, anti-phase, or sham. These findings suggest that theta tACS effects on verbal working memory were load- and subject-dependent, rooted in tACS-induced changes in frontoparietal network interactions, and not driven by changes in arousal levels.