The Effect of High-Frequency Repetitive Transcranial Magnetic Stimulation on Emotion Processing, Reappraisal, and Craving in Alcohol Use Disorder Patients and Healthy Controls: A Functional Magnetic Resonance Imaging Study

Jochem M Jansen, Odile A van den Heuvel, Ysbrand D van der Werf, Stella J de Wit, Dick J Veltman, Wim van den Brink, Anna E Goudriaan, Jochem M Jansen, Odile A van den Heuvel, Ysbrand D van der Werf, Stella J de Wit, Dick J Veltman, Wim van den Brink, Anna E Goudriaan

Abstract

Impaired cognitive-motivational functioning is present in many psychiatric disorders, including alcohol use disorder (AUD). Emotion regulation is a key intermediate factor, relating to the (cognitive) regulation of emotional and motivational states, such as in regulation of craving or negative emotions that may lead to relapse in alcohol use. These cognitive-motivational functions, including emotion regulation, are a target in cognitive behavioral therapy and may possibly be improved by neurostimulation techniques. The present between-subjects, single-blind study assesses the effects of sham-controlled high-frequency neuronavigated repetitive transcranial magnetic stimulation (10 Hz) of the right dorsolateral prefrontal cortex (dlPFC) on several aspects relevant for emotion regulation (emotion processing and reappraisal abilities) and related brain activity, as well as self-reported craving in a sample of alcohol use disorder patients (AUD; n = 39) and healthy controls (HC; n = 36). During the emotion reappraisal task, participants were instructed to either attend or reappraise their emotions related to the negative, positive, neutral, and alcohol-related images, after which they rated their experienced emotions. We found that repetitive transcranial magnetic stimulation (rTMS) reduces self-reported experienced emotions in response to positive and negative images in AUD patients, whereas experienced emotions were increased in response to neutral and positive images in HCs. In the functional magnetic resonance imaging (fMRI) analyses, we found that rTMS reduces right dlPFC activity during appraisal of affective images relative to sham stimulation only in AUD patients. We could not confirm our hypotheses regarding the effect of rTMS craving levels, or on reappraisal related brain function, since no significant effects of rTMS on craving or reappraisal related brain function were found. These findings imply that rTMS can reduce the emotional impact of images as reflected in blood oxygenation level-dependent (BOLD) response, especially in AUD patients. Future studies should replicate and expand the current study, for instance, by assessing the effect of multiple stimulation sessions on both explicit and implicit emotion regulation paradigms and craving, and assess the effect of rTMS within subgroups with specific addiction-relevant image preferences. Clinical Trial Registration: www.ClinicalTrials.gov, identifier NCT02557815.

Keywords: alcohol use disorder; craving; emotion processing; emotion reappraisal; functional magnetic resonance imaging; repetetitive transcranial magnetic stimulation.

Figures

Figure 1
Figure 1
Effect of repetitive transcranial magnetic stimulation (rTMS) on experienced emotion. This figure shows the differential effects of rTMS and sham stimulation on experienced emotion in reaction to alcohol (A), neutral (B), positive (C), and negative (D) images. Note that a value of 50 represents “neutral” experienced emotion. Bars represent estimated marginal means, which are corrected for experienced emotion before rTMS. Error bars are standard deviations from the mean. ¥ = significant two-way interaction (group by stimulation), * = significant main effect of stimulation within participant group, pos. = positive, neg. = negative.
Figure 2
Figure 2
This figure shows the trend-significant interaction between emotion (alcohol, neutral, positive, negative) and stimulation (rTMS, sham) within the superior frontal gyrus. (A) This panel shows the location for the interaction in the bilateral superior frontal gyrus. For illustrative purposes, these results are depicted at a p < 0.001 uncorrected threshold (B). This panel shows the interaction within the peak voxel in the right superior frontal gyrus, based on the extracted beta weights.
Figure 3
Figure 3
The effect of rTMS on brain activity during emotion processing. (A) Cool coloring represents brain activity in the dorsolateral prefrontal cortex (dlPFC), which has decreased due to rTMS relative to sham stimulation in AUD patients. Hot coloring indicates brain activity in the supramarginal gyrus, which has increased due to rTMS stimulation relative to sham stimulation in AUD patients. For illustrative purposes, these results are depicted at a p < 0.001 uncorrected threshold. (B) This bar chart shows the effect of rTMS and sham stimulation on right dlPFC activity in AUD patients and HCs.
Figure 4
Figure 4
The effect of rTMS and sham stimulation on craving per group. This figure depicts the significant interaction between stimulation (rTMS, sham) and group [alcohol use disorder (AUD), healthy controls (HC)]. * Note that the values are log(x + 1) transformed. ¥ = significant two-way interaction.

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