Oscillatory and non‐oscillatory brain activity reflects fear expression in an immediate and delayed fear extinction task

• Published in: Psychophysiology Vol. 60; no. 8; pp. e14283 - n/a
• Main Authors: Bierwirth, Philipp, Antov, Martin I., Stockhorst, Ursula
• Format: Journal Article
• Language: English
• Published: United States Blackwell Publishing Ltd 01.08.2023
• Subjects: Arousal; EEG; EKG; Electrocardiography; Extinction (Learning); Extinction behavior; Fear conditioning; fear extinction; immediate extinction deficit; Observational learning; oscillation detection; theta oscillations; Theta rhythms; fear conditioning; immediate extinction deficit; oscillation detection; EEG; fear extinction; theta oscillations
• ISSN: 0048-5772; 1469-8986; 1540-5958
• DOI: 10.1111/psyp.14283

Fear extinction is pivotal for inhibiting fear responding to former threat‐predictive stimuli. In rodents, short intervals between fear acquisition and extinction impair extinction recall compared to long intervals. This is called Immediate Extinction Deficit (IED). Importantly, human studies of the IED are sparse and its neurophysiological correlates have not been examined in humans. We, therefore, investigated the IED by recording electroencephalography (EEG), skin conductance responses (SCRs), an electrocardiogram (ECG), and subjective ratings of valence and arousal. Forty male participants were randomly assigned to extinction learning either 10 min after fear acquisition (immediate extinction) or 24 h afterward (delayed extinction). Fear and extinction recall were assessed 24 h after extinction learning. We observed evidence for an IED in SCR responses, but not in the ECG, subjective ratings, or in any assessed neurophysiological marker of fear expression. Irrespective of extinction timing (immediate vs. delayed), fear conditioning caused a tilt of the non‐oscillatory background spectrum with decreased low‐frequency power (<30 Hz) for threat‐predictive stimuli. When controlling for this tilt, we observed a suppression of theta and alpha oscillations to threat‐predictive stimuli, especially pronounced during fear acquisition. In sum, our data show that delayed extinction might be partially advantageous over immediate extinction in reducing sympathetic arousal (as assessed via SCR) to former threat‐predictive stimuli. However, this effect was limited to SCR responses since all other fear measures were not affected by extinction timing. Additionally, we demonstrate that oscillatory and non‐oscillatory activity is sensitive to fear conditioning, which has important implications for fear conditioning studies examining neural oscillations. Our findings provide further knowledge about the neurophysiological foundations of fear and extinction learning and the critical role of timing between both learning phases. By disentangling oscillatory and non‐oscillatory brain activity we show that standard power estimates can be highly distorted due to fear‐induced non‐oscillatory brain dynamics. Moreover, while animal studies demonstrate that timing of extinction learning impacts long‐term fear suppression, we observed that a similar effect of extinction timing seems to be limited to only some domains of fear responding in humans.