Verbal working memory is supported by a left-lateralized frontoparietal theta oscillation (4 to 8 Hz) network. We tested whether stimulating the left frontoparietal network at theta frequency during verbal working memory can produce observable after-stimulation effects in behavior and neurophysiology. Weak theta-band alternating 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 (within-subject) 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 and EEG data from the post-stimulation session, we report two main observations. First, in-phase stimulation improved task performance in subjects with higher working memory capacity (WMC) under higher memory load (load 6). Second, in-phase stimulation enhanced frontoparietal theta synchrony during working memory retention 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 frontalparietal theta Granger causality. These observations suggest that (1) in-phase theta transcranial alternating current stimulation (tACS) during verbal working memory can result in observable behavioral and neurophysiological consequences post stimulation, (2) the short-term plasticity effects are state- and individual-dependent, and (3) enhanced executive control underlies improved behavioral performance.
(A) The randomized, single-blind, cross-over, and sham-controlled design. (B) Timeline of the verbal working memory task with three levels of memory load (load 2, load 4, and load 6).
(A) Position of the two 4×1 HD-tACS arrays and the three stimulation protocols: in-phase (0-degree phase difference), anti-phase (180-degree phase difference), and sham. Within each array, the center electrode and the four surrounding electrodes have opposite polarity, forming a closed circuit. The center-surround, source-sink arrangement of the five electrodes enables better focality of electrical stimulation (high definition or HD). (B) Current flow under in-phase stimulation shown on 3D reconstruction of the cortical surface demonstrates maximal electrical field intensity over the left frontal and parietal cortex.
(A) Mean accuracy and (C) RT under different WM load conditions following the three stimulation protocols in all subjects (n = 20). (B) Mean accuracy and (C) RT under different WM load conditions following the three stimulation protocols in high (n = 10) and low (n = 10) WMC subjects. *p < 0.05. Green: post sham, red: post in-phase, blue: post anti-phase. *p<0.05.
(A) Left frontoparietal theta phase locking value (PLV) for high (top) and low (bottom) WMC subjects. (B) Right frontoparietal theta PLV for high and low WMC subjects. (C) Left frontal parietal theta band GC in high (top) and low (bottom) WMC subjects. (D) Left parietal frontal theta band GC in high and low WMC subjects. Green: post sham, red: post in-phase, blue: post anti-phase. *p<0.05.
There were no significant differences in pre-cue pupil diameter from the three post-stimulation sessions (all p > 0.1), indicating that the arousal level was not different whether the session was preceded by sham, in-phase, and anti-phase stimulations.