Prefrontal oscillations during recall of conditioned and extinguished fear in humans.
Human neuroimaging studies indicate that the anterior midcingulate cortex (AMC) and the ventromedial prefrontal cortex (vmPFC) play important roles in the expression and extinction of fear, respectively. Electrophysiological rodent studies further indicate that oscillatory neuronal activity in homolog regions (i.e., prelimbic and infralimbic cortices) changes during fear expression and fear extinction recall. Whether similar processes occur in humans remains largely unexplored. By assessing scalp surface EEG in conjunction with LORETA source estimation of CS-related theta and gamma activity, we tested whether a priori defined ROIs in the human AMC and vmPFC similarly modulate their oscillatory activity during fear expression and extinction recall, respectively. To this end, 42 healthy individuals underwent a differential conditioning/differential extinction protocol with a Recall Test on the next day. In the Recall Test, nonextinguished versus extinguished stimuli evoked an increased differential (CS(+) vs CS(-)) response with regard to skin conductance and AMC-localized theta power. Conversely, extinguished versus nonextinguished stimuli evoked an increased differential response with regard to vmPFC-localized gamma power. Finally, individuals who failed to show a suppressed skin conductance response to the extinguished versus nonextinguished CS(+) also failed to show the otherwise observed alterations in vmPFC gamma power to extinguished CS(+). These results indicate that fear expression is associated with AMC theta activity, whereas successful fear extinction recall relates to changes in vmPFC gamma activity. The present work thereby bridges findings from prior rodent electrophysiological research and human neuroimaging studies and indicates that EEG is a valuable tool for future fear extinction research.
Department of Clinical Psychology, Justus-Liebig University Giessen, 35394 Giessen, Germany, and Center for Depression, Anxiety and Stress Research & McLean Imaging Center, McLean Hospital, Harvard Medical School, Belmont, Massachusetts 02478 erik.mueller@psychol.uni-giessen.de.
Erik M
EM
Mueller
Department of Clinical Psychology, Justus-Liebig University Giessen, 35394 Giessen, Germany, and.
Christian
C
Panitz
Department of Clinical Psychology, Justus-Liebig University Giessen, 35394 Giessen, Germany, and.
Christiane
C
Hermann
Center for Depression, Anxiety and Stress Research & McLean Imaging Center, McLean Hospital, Harvard Medical School, Belmont, Massachusetts 02478.
Diego A
DA
Pizzagalli
D000328:Adult; D000704:Analysis of Variance; D001931:Brain Mapping; D058256:Brain Waves / Q000502:physiology*; D015331:Cohort Studies; D003213:Conditioning, Psychological / Q000502:physiology*; D004569:Electroencephalography; D005108:Extinction, Psychological / Q000502:physiology*; D005239:Fear; D005260:Female; D005712:Galvanic Skin Response / Q000502:physiology; D006801:Humans; D008297:Male; D011939:Mental Recall / Q000502:physiology*; D017397:Prefrontal Cortex / Q000502:physiology*; D055815:Young Adult
conditioning; extinction; fear; theta