Oscillatory EEG activity induced by conditioning stimuli during fear conditioning reflects Salience and Valence of these stimuli more than Expectancy

Abstract

Imaging studies have described hemodynamic activity during fear conditioning protocols with stimulus trains in which a visual conditioned stimulus (CS+) is paired with an aversive unconditioned stimulus (US, painful laser pulse) while another visual stimulus is unpaired (CS-). We now test the hypothesis that CS Event Related Spectral Perturbations (ERSPs) are related to ratings of CS Expectancy (likelihood of pairing with the US), Valence (unpleasantness) and Salience (ability to capture attention). ERSP windows in EEG were defined by both time after the CS and frequency, and showed increased oscillatory power (Event Related Synchronization, ERS) in the Delta/Theta Windows (0-8Hz) and the Gamma Window (30-55Hz). Decreased oscillatory power (Event Related Desynchronization - ERD) was found in Alpha (8-14Hz) and Beta Windows (14-30Hz). The Delta/Theta ERS showed a differential effect of CS+ versus CS- at Prefrontal, Frontal and Midline Channels, while Alpha and Beta ERD were greater at Parietal and Occipital Channels early in the stimulus train. The Gamma ERS Window increased from habituation to acquisition over a broad area from frontal and occipital electrodes. The CS Valence and Salience were greater for CS+ than CS-, and were correlated with each other and with the ERD at overlapping channels, particularly in the Alpha Window. Expectancy and CS Skin Conductance Response were greater for CS+ than CS- and were correlated with ERSP at fewer channels than Valence or Salience. These results suggest that Alpha ERSP activity during fear conditioning reflects Valence and Salience of the CSs more than conditioning per se.

Keywords: EEG; event-related synchronization; fear conditioning; human; painful laser stimulus; salience.

Fig. 1

Fear conditioning protocol. Timelines for the Habituation (A) and Acquisition Phases (B) including approximate intervals of the Contexts (CXs), Unconditioned Stimuli (US), and Conditioning Stimuli (CS+ and CS−) which are randomized within the parameters specified in the text. Contexts and colors of the light which became the CS+ were randomized across patients (see text). The Contexts are shown as red and blue underlines to indicate that the Contexts are the background against which the CSs are presented. C shows the number of CS+, CS− and CXs within the blocks which comprise the Habituation and Acquisition Phases and which are shown in order of presentation. See text. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Time Frequency plots of ERSP averaged across subjects and Channels. CS+ is in the upper row and CS− is in the lower row. The three columns from left to right denote Hab, Acq 1 and Acq 2. The axes of the time frequency plot are labeled in the (A) with the Y axis from 0 to 150 Hz. Windows used in this analysis are labeled in (C). Color scale is in Db, as labeled. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

Time frequency plots across subjects for Acq 1 C– at Channels labeled above each plot and indicated by the arrangement of the time frequency plots relative to the forehead as labeled. Note that the vertical axis of each plot is from 0 to 100 Hz while the Color scale is as labeled and other conventions are as labeled in Fig. 2. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Time Frequency plots across subjects for Acq 1 CS+. Conventions as in Fig. 3.

Fig. 5

Time Frequency plots across subjects for Acq 2 CS−. Conventions as in Fig. 3.

Fig. 6

Time Frequency plots across subjects for Acq 2 CS+. Conventions as in Fig. 3.

Fig. 7

SCR and CS ratings during the behavioral protocol. (A) SCR at intervals after the CS+ (red line) and CS− (blue). (B) Plot of WIII ERD versus CS Salience across Subjects, Phases and Cues. (C) Plot of WIII ERD versus CS+ unpleasantness across CS, Phases and Cues. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)