Abstract
Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor. Theories suggest altered emotional information processing as the key mechanism of rumination. However, studies on the anticipation processes in relation to rumination are scarce, even though expectation in this process is demonstrated to influence the processing of emotional stimuli. In addition, no published study has investigated violated expectation in relation to rumination yet. In the present study we examined the neural correlates of pain anticipation and perception using a fear conditioning paradigm with pain as the unconditioned stimulus in healthy subjects (N = 30). Rumination was assessed with the 10-item Ruminative Response Scale (RRS). Widespread brain activation – extending to temporal, parietal, and occipital lobes along with activation in the cingulate cortex, insula, and putamen – showed a positive correlation with rumination, supporting our hypothesis that trait rumination influences anticipatory processes. Interestingly, with violated expectation (when an unexpected, non-painful stimulus follows a pain cue compared to when an expected, painful stimulus follows the same pain cue) a negative association between rumination and activation was found in the posterior cingulate cortex, which is responsible for change detection in the environment and subsequent behavioral modification. Our results suggest that rumination is associated with increased neural response to pain perception and pain anticipation, and may deteriorate the identification of an unexpected omission of aversive stimuli. Therefore, targeting rumination in cognitive behavioral therapy of chronic pain could have a beneficial effect.
Highlights
Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor
Activation changes to painful stimuli Contrasting painful versus non-painful and contrasting painful with validly cued nonpainful stimuli led to widespread activation in brain areas involved in pain perception including the insula, thalamus, inferior frontal gyrus, middle cingulate gyrus, and in the midbrain at the level of periaqueductal gray
We found that rumination correlated with posterior cingulate cortex (PCC) activity – extending to the posterior midcingulate cortex – during the pain anticipation phase
Summary
Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor. Theories suggest altered emotional information processing as the key mechanism of rumination. Studies on the anticipation processes in relation to rumination are scarce, even though expectation in this process is demonstrated to influence the processing of emotional stimuli. Our results suggest that rumination is associated with increased neural response to pain perception and pain anticipation, and may deteriorate the identification of an unexpected omission of aversive stimuli. Several studies – using among others eyetracking (e.g., Duque, Sanchez, & Vazquez, 2014; Owens & Gibb, 2017), and reaction-time paradigms (e.g., Grafton, Southworth, Watkins, & MacLeod, 2016), and neuroimaging methodology (e.g., Vanderhasselt, Kuehn, & De Raedt, 2011; Vanderhasselt et al, 2013) showed that biased emotional and attentional processing of negative (aversive) information is associated with rumination. Expectations associated with negative and positive stimuli (events) may influence processing of emotional information and outcomes. Applying a mediation analysis, a study using painful heat stimuli demonstrated that brain activity associated with pain predictive cues had an effect on perceived pain both on a subjective and on a neural level (Atlas, Bolger, Lindquist, & Wager, 2010)
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