Brain activity associated with illusory correlations in animal phobia

Abstract

Anxiety disorder patients were repeatedly found to overestimate the association between disorder-relevant stimuli and aversive outcomes despite random contingencies. Such an illusory correlation (IC) might play an important role in the return of fear after extinction learning; yet, little is known about how this cognitive bias emerges in the brain. In a functional magnetic resonance imaging study, 18 female patients with spider phobia and 18 healthy controls were exposed to pictures of spiders, mushrooms and puppies followed randomly by either a painful electrical shock or nothing. In advance, both patients and healthy controls expected more shocks after spider pictures. Importantly, only patients with spider phobia continued to overestimate this association after the experiment. The strength of this IC was predicted by increased outcome aversiveness ratings and primary sensory motor cortex activity in response to the shock after spider pictures. Moreover, increased activation of the left dorsolateral prefrontal cortex (dlPFC) to spider pictures predicted the IC. These results support the theory that phobia-relevant stimuli amplify unpleasantness and sensory motor representations of aversive stimuli, which in turn may promote their overestimation. Hyper-activity in dlPFC possibly reflects a pre-occupation of executive resources with phobia-relevant stimuli, thus complicating the accurate monitoring of objective contingencies and the unlearning of fear.

Keywords: covariation bias; fMRI; illusory correlation; pain; spider phobia.

Fig. 1

IC paradigm and covariation bias. (A) Three categories of pictures were presented (spiders, mushrooms and puppies). Exactly 50% of the pictures of each category were followed by a painful electrical shock. In order to keep attention focused on contingencies, participants were asked to press one of the two buttons depending on whether they expected a shock in a trial or not. The histograms show the expected proportion of shocks before (a priori, B) and the estimated proportion of shocks after the IC experiment (trial-by-trial a posteriori ICs, C). For trial-by-trial a posteriori ICs (C), each picture was presented again and the participants were asked to indicate whether a shock had followed that particular picture. Black and white bars display whether there had actually been presented a shock or nothing as an outcome. Both spider phobic and control participants expected more shocks following spiders before the experiment (B). Importantly, only spider-phobic participants (C, orange background) but not healthy controls (C, gray background) overestimated this association after the experiment. **P < 0.01; ***P < 0.001.

Fig. 2

Spider-phobic patients’ responses to picture onsets. The five ROIs (A–E) with significant differences in the contrast (spider > mushroom) are depicted (ROI analysis: P < 0.05, few corrected, k ≥ 5 voxels; display threshold: P < 0.005, uncorrected, k ≥ 10 voxels). Line diagrams show the time course of percent signal change for spider (green) and mushroom (black) pictures during picture presentation (grey background from 0 to 7.5 s) in spider phobia. The dlPFC (A), the right dlPFC (B), the left ACC (C), the left insula (D) and the left amygdala (E) showed enhanced activity in response to spiders vs mushrooms within spider phobics. However, only the left dlPFC correlated with the IC. The scatter plot (A) visualizes this correlation between the difference in brain activity in the left dlPFC during picture presentation and the trial-by-trial IC after the experiment (see Supplementary material and supplementary Table S2 for time course analysis). In the upper right corner (F), clusters that correlated with the trial-by-trial IC can be seen mainly in the left fronto-parietal regions including the dlPFC, BA 8 and the superior parietal cortex (spider phobia = yellow; healthy controls = blue; whole-brain analysis: P < 0.001, uncorrected; k ≥ 10 voxels).

Fig. 3

Activity in the PCL of spider-phobic patients and correlations with IC and ratings of shock aversiveness. The brain slices correspond with the peak voxel in right PCL (ROI-analysis: P < 0.05, k = 5 voxels) and show significant activation for the contrast [(shock-after-spider > nothing-after-spider) > (shock-after-mushroom > nothing-after-mushroom)] (P < 0.001, k = 10 voxels for display purpose, color scale represents t values). Scatterplots depict the association between right PCL activity (mean beta values of all voxels in the ROI) and trial-by-trial IC (left), respectively, the rated aversiveness of the electrical shock (right) depending on the picture type.