Brain-state determines learning improvements after transcranial alternating-current stimulation to frontal cortex

Abstract

Background: Theories of executive control propose that communication between medial frontal cortex (MFC) and lateral prefrontal cortex (lPFC) is critical for learning. 6-Hz phase synchronization may be the mechanism by which neural activity between MFC and lPFC is coordinated into a functional network. Recent evidence suggests that switching from eyes closed to open may induce a change in brain-state reflected by enhanced executive control and related functional connectivity.

Objective/hypothesis: To examine whether causal manipulation of MFC and lPFC can improve learning according to the brain-state induced by switching from eyes closed to open.

Methods: Within-subjects, sham-controlled, double-blind study of 30 healthy subjects, each receiving 6-Hz in-phase high definition transcranial alternating-current stimulation (HD-tACS) applied to MFC and right lPFC prior to performing a time estimation task.

Results: HD-tACS with eyes open improved learning ability relative to sham, whereas HD-tACS with eyes closed had no significant effect on behavior.

Conclusion: Results suggest a phase-sensitive mechanism in frontal cortex mediates components of learning performance in a state-dependent manner.

Keywords: Lateral prefrontal cortex; Learning; Medial frontal cortex; Transcranial alternating-current stimulation.

Fig. 1. Methods, Design, and Results

A, The right lateralized 8-channel in-phase high definition transcranial alternating-current stimulation (HD-tACS) montage and current-flow model shown on 3D reconstructions of the cortical surface. The yellow (positive) and blue (negative) circles in the montage reflect the polarity of electrical current applied over medial frontal cortex (MFC) and right lateral prefrontal cortex (lPFC) target regions. B, The sequence of events on feedback and nonfeedback trials in the time estimation task. C, Performance measures of absolute error magnitude, response variability, and adjustment efficiency across blocks of feedback (gray) and nonfeedback (white) trials after the 6-Hz eyes closed (red), 6-Hz eyes open (blue), and 10-Hz eyes open (green) active conditions, and the sham (black) condition in the same subjects. Error bars show ± 1 standard error of the mean.