TACS Phase Locking of Frontal Midline Theta Oscillations Disrupts Working Memory Performance.

Bankim S Chander,Jan Born,Matthias Witkowski,Niels Birbaumer,Stephen E Robinson,Surjo R Soekadar,Christoph Braun,Leonardo G Cohen

doi:10.3389/fncel.2016.00120

Abstract

Background: Frontal midline theta (FMT) oscillations (4–8 Hz) are strongly related to cognitive and executive control during mental tasks such as memory processing, arithmetic problem solving or sustained attention. While maintenance of temporal order information during a working memory (WM) task was recently linked to FMT phase, a positive correlation between FMT power, WM demand and WM performance was shown. However, the relationship between these measures is not well understood, and it is unknown whether purposeful FMT phase manipulation during a WM task impacts FMT power and WM performance. Here we present evidence that FMT phase manipulation mediated by transcranial alternating current stimulation (tACS) can block WM demand-related FMT power increase (FMTΔpower) and disrupt normal WM performance.Methods: Twenty healthy volunteers were assigned to one of two groups (group A, group B) and performed a 2-back task across a baseline block (block 1) and an intervention block (block 2) while 275-sensor magnetoencephalography (MEG) was recorded. After no stimulation was applied during block 1, participants in group A received tACS oscillating at their individual FMT frequency over the prefrontal cortex (PFC) while group B received sham stimulation during block 2. After assessing and mapping phase locking values (PLV) between the tACS signal and brain oscillatory activity across the whole brain, FMT power and WM performance were assessed and compared between blocks and groups.Results: During block 2 of group A but not B, FMT oscillations showed increased PLV across task-related cortical areas underneath the frontal tACS electrode. While WM task-related FMTΔpower and WM performance were comparable across groups in block 1, tACS resulted in lower FMTΔpower and WM performance compared to sham stimulation in block 2.Conclusion: tACS-related manipulation of FMT phase can disrupt WM performance and influence WM task-related FMTΔpower. This finding may have important implications for the treatment of brain disorders such as depression and attention deficit disorder associated with abnormal regulation of FMT activity or disorders characterized by dysfunctional coupling of brain activity, e.g., epilepsy, Alzheimer’s or Parkinson’s disease (AD/PD).

Highlights

Brain oscillations reflect rhythmic fluctuations in neuronal excitability modulating long-range communication between cortical and subcortical areas important for cognition and adaptive behavior in humans (Buzsáki and Draguhn, 2004)
The voxel with the highest ∆phase locking values (PLV) was located in the left prefrontal cortex (PFC) (Talairach coordinate [60, −6, 12]). ∆PLV at this voxel was significantly different between groups evidencing that transcranial alternating current stimulation (tACS), but not sham stimulation, resulted phase locking of Frontal midline theta (FMT) oscillations (Figure 3)
A topographic map based on the difference in FMT∆Power between group A and B showed that tACS-associated lack of power increase was widespread matching cortical areas previously identified to be active during execution of a 2-back task (Figure 5)

Summary

Background

Frontal midline theta (FMT) oscillations (4–8 Hz) are strongly related to cognitive and executive control during mental tasks such as memory processing, arithmetic problem solving or sustained attention. We present evidence that FMT phase manipulation mediated by transcranial alternating current stimulation (tACS) can block WM demand-related FMT power increase (FMT∆power) and disrupt normal WM performance. Results: During block 2 of group A but not B, FMT oscillations showed increased PLV across task-related cortical areas underneath the frontal tACS electrode. Conclusion: tACS-related manipulation of FMT phase can disrupt WM performance and influence WM task-related FMT∆power. This finding may have important implications for the treatment of brain disorders such as depression and attention deficit disorder associated with abnormal regulation of FMT activity or disorders characterized by dysfunctional coupling of brain activity, e.g., epilepsy, Alzheimer’s or Parkinson’s disease (AD/PD)

INTRODUCTION

Study Participants

RESULTS

DISCUSSION