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

Abstract

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.

Pseudo‐mutual gazing enhances interbrain synchrony during remote joint attention tasking

“…Leveraging these computed probabilities, we discarded non‐brain components with a likelihood exceeding 90% of being categorized as muscle, eye, heart, line noise, channel noise, or other sources. This 90% threshold aligns with that utilized in Delorme's “Optimized Pipelines” (Delorme, 2023) and other studies (Bierwirth et al, 2023). The remaining independent components were then back‐projected to complete the signal reconstruction.…”

“…Being distanced from the primary sources of eye movement artifacts, these sites offered a more appropriate choice for the current study. Furthermore, to manage artifact rejection, we utilized independent component analysis (ICA, infomax algorithm) (Makeig et al, 1995) (Delorme, 2023) and other studies (Bierwirth et al, 2023). The remaining independent components were then backprojected to complete the signal reconstruction.…”

Alpha‐band oscillations and emotion: A review of studies on picture perception

“…The emotional modulation of alpha ERD seems to reflect the engagement of the motivational systems when a significant/arousing stimulus is detected. Consistently, a modulation of alpha ERD was also observed in studies that manipulated stimulus significance (arousal) by conditioning neutral stimuli (Bacigalupo & Luck, 2022;Bierwirth et al, 2023), and in anticipation paradigms, in which participants had to anticipate negative events, painful/aversive stimulation or possible threats (Del Percio et al, 2006;Onoda et al, 2007). Several conditioning studies reported greater alpha-band suppression following a conditioned stimulus (CS) that was paired with an aversive (CS+) vs. neutral (CS−) outcome (Bacigalupo & Luck, 2022;Chien et al, 2017;Friedl & Keil, 2020Panitz et al, 2019;Yin et al, 2020).…”

Temporal Alpha Power in Resting-State EEG as Neuromarker of Complex Childhood Trauma in Institutionalized Adolescents

“…Evidence suggests a relationship between excessive alpha power in the temporal region and fear-related processes, including fear conditioning and fear learning circuits [20,27].…”

“…Few studies have reported changes in EEG patterns [32], including increased alpha power, in individuals with PTSD [33] or during fear conditioning tasks [27,33]. These changes may indicate dysregulation of fear-learning circuits.…”