Evaluation of Theta EEG Neurofeedback Procedure for Cognitive Training Using Simultaneous fMRI in Counterbalanced Active-Sham Study Design

Evaluation of mechanisms of action of EEG neurofeedback (EEG-nf) using simultaneous fMRI is highly desirable to ensure its effective application for clinical rehabilitation and therapy. Counterbalancing training runs with active neurofeedback and sham (neuro)feedback for each participant is a promising approach to demonstrate specificity of training effects to the active neurofeedback. We report the first study in which EEG-nf procedure is both evaluated using simultaneous fMRI and controlled via the counterbalanced active-sham study design. Healthy volunteers (n = 18) used EEG-nf to upregulate frontal theta EEG asymmetry (FTA) during fMRI while performing tasks that involved mental generation of a random numerical sequence and serial summation of numbers in the sequence. The FTA was defined as power asymmetry for channels F3 and F4 in [4–7] Hz band. Sham feedback was provided based on asymmetry of motion-related artifacts. The experimental procedure included two training runs with the active EEG-nf and two training runs with the sham feedback, in a randomized order. The participants showed significantly more positive FTA changes during the active EEG-nf conditions compared to the sham conditions, associated with significantly higher theta EEG power changes for channel F3. Temporal correlations between the FTA and fMRI activities of prefrontal, parietal, and occipital brain regions were significantly enhanced during the active EEG-nf conditions compared to the sham conditions. Temporal correlation between theta EEG power for channel F3 and fMRI activity of the left dorsolateral prefrontal cortex (DLPFC) was also significantly enhanced. Significant active-vs-sham difference in fMRI activations was observed for the left DLPFC. Our results demonstrate that mechanisms of EEG-nf training can be reliably evaluated using the counterbalanced active-sham study design and simultaneous fMRI.