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 (0–8 Hz) and the gamma Window (30–55 Hz). Decreased oscillatory power (Event Related Desynchronization – ERD) was found in alpha (8–14 Hz) and beta Windows (14–30 Hz). 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. The CS Valence and Salience were correlated with each other and with ERSP in the alpha Window more commonly than in other windows. Delta/theta ERSP differentiates between CS+ and CS− over a Midline Channel at which ERSP is correlated with Expectancy ratings. Although, both Expectancy and CS Skin Conductance Response (SCR) were correlated with ERSP this correlation occurred at fewer and different Channels than those for Valence or Salience. These results suggest that ERSP activity is related to Valence and Salience of the CSs more than to conditioning per se.

Imagery‐induced negative affect, social touch and frontal EEG power band activity

“…This was interpreted to reflect evolutionary shaped learning (Hornstein & Eisenberger, 2018;Seligman, 1970). Because oscillatory activity in the theta band affects fear conditioning (Chien, Colloca, Korzeniewska, Cheng, Campbell, Hillis & Lenz, 2017) and because in the present study, touching an attachment figure reduced theta activity, we suggest that reduced fear conditioning as a function of attachment activation is mediated or modulated by reduced theta brain activity. In conclusion, the nature of pair bonding modulates brain activity during partner presence.…”

Neural Oscillatory Correlates for Conditioning and Extinction of Fear

“…A power increase in gamma power was observed from habituation to the acquisition phase over a broad area in the frontal and occipital electrodes. The authors reported that alpha activity during fear conditioning reflects the salience and valence of conditioned/unconditioned stimuli rather than conditioning [ 33 ].…”

High‐precision magnetoencephalography for reconstructing amygdalar and hippocampal oscillations during prediction of safety and threat

“…Neuroimaging studies generally rely on a larger number of participants (N = 20), but include relatively few stimulus repetitions for each of them (e.g., 116 CS± acquisition and extinction trials in (Lithari et al, ), or 40 CS± acquisition trials in (Chien et al, )). Here, we opted for a different approach, including few participants ( N = 5), but increasing the precision of single measurements for each one of them (Meyer, Bonaiuto, et al, ; Troebinger, López, Lutti, Bradbury, et al, ), akin to what used in the field of precision functional mapping (Gordon et al, ) and the nonhuman primate literature (Klavir et al, ).…”

“…Our findings largely accord with what previous MEG/EEG studies have reported for the sensor level or for cortical areas. In these, CS+ presentations have been shown to result in a decrease in the power of slow oscillations, compared to presentations of CS− (Chien et al, ; Lithari et al, ; Moses et al, ). This pattern of results was replicated in our study, where theta power in the hippocampus and amygdala was significantly lower following presentations of CS+ compared to CS−.…”

“…On the other hand, noninvasive electrophysiological methods such as magnetoencephalography or electroencephalography (MEG/EEG), have found it difficult to isolate signals from amygdala, due to its small size and deep location. Indeed, most previous threat conditioning studies using MEG did not analyse or report the temporal dynamics of signals specifically emanating from the amygdala (Chien et al, ; Kluge et al, ; Moses, Bardouille, Brown, Ross, & McIntosh, ; Moses, Martin, Houck, Ilmoniemi, & Tesche, ; Rehbein et al, ; Tesche et al, ), while a few reported evoked responses in amygdala (Balderston, Schultz, Baillet, & Helmstetter, ; Moses et al, ), or indirect evidence of amygdalar contributions to a wider network underlying threat conditioning (Lithari et al, ; Lithari, Moratti, & Weisz, ). Thus, to date, there is no direct characterisation of amygdala oscillations during human threat conditioning.…”