Extending the concept of emotion regulation with model-based fMRI

Effective emotion regulation is essential for our social and emotional well-being. Yet, the concept of emotion regulation, as it is conventionally regarded in the field, does not take important aspects of emotions and emotion regulation into account. The overarching aim of the current thesis was to include such missing aspects and thereby expand the concept of emotion regulation. The expansion occurred in two directions: firstly, the definition of emotion within the field of emotion regulation was widened to include the motivational aspect of emotions in terms of value-based prediction errors and their neural implementation; and secondly, an underestimated type of emotion regulation – the social emotion regulation – and its neural underpinnings were investigated. Projects 1 and 2 of the current thesis expand the emotion part of emotion regulation. Project 1 investigated whether emotion regulation affects not only emotional response-related brain activity but also influences aversive prediction error-related activity, i.e., the motivation-related brain signal. We found that self- initiated reappraisal, a type of cognitive emotion regulation, indeed affected prediction error-related activity, such that this activity was enhanced in the ventral tegmental area, ventral striatum, insula and hippocampus, possibly via a prefrontal-tegmental pathway. Project 2 further examined the way emotion regulation affects emotions and prediction errors, by testing whether self- initiated reappraisal directly targets the brain network for motivated behaviour previously outlined by animal studies. We found that superior (in contrast to inferior) regulators affected the balance of competing influences of ventral striatal afferents on striatal aversive prediction error signals; they reduced the impact of subcortical striatal afferents (i.e., hippocampus, amygdala and ventral tegmental area), while keeping the influence of the prefrontal cortex on ventral striatal prediction errors constant. Inferior regulators, on the other hand, failed to supress subcortical inputs into the ventral striatum and instead counterproductively reduced the prefrontal influence on ventral striatal prediction error signals. Projects 3 and 4 of the thesis extend the regulation part of emotion regulation. Project 3 explored the neural correlates of social cognitive emotion regulation, specifically reappraisal, and directly compared them with those of self-initiated reappraisal. We found that regions of the anterior, the medial parietal, and the lateral temporo-parietal default mode network were specifically involved in social emotion regulation, and that social regulation success and the default mode network involvement during regulation were related to participants’ attachment security scores. Project 4 investigated social emotion modulation and its impact on two distinct types of emotional brain activity – emotional response- and aversive prediction error-related activity. We found – for the simple contrast of being with somebody versus being alone – a three-fold dissociation between signal types and insula subregions, including left and right anterior and posterior insula parts. Social emotion modulation reduced aversive stimulus-related activity in the posterior insula, while simultaneously increasing aversive prediction error-related activity in the anterior insula. Furthermore, the social effect on prediction error-related activity was positively associated with aversive learning in the right, but negatively in the left anterior insula. Altogether, by expanding the concept of emotion regulation, projects of the current thesis provide new insights into both the effects and the neural underpinnings of three distinct emotion regulation types. Considering that problems in both intrapersonal emotion regulation and social interaction are linked to affective disorders, our findings might contribute to a better understanding of these disorders and the disorder-specific emotional and social impairments

Extending the concept of emotion regulation with model-based fMRI

Effective emotion regulation is essential for our social and emotional well-being. Yet, the concept of emotion regulation, as it is conventionally regarded in the field, does not take important aspects of emotions and emotion regulation into account. The overarching aim of the current thesis was to include such missing aspects and thereby expand the concept of emotion regulation. The expansion occurred in two directions: firstly, the definition of emotion within the field of emotion regulation was widened to include the motivational aspect of emotions in terms of value-based prediction errors and their neural implementation; and secondly, an underestimated type of emotion regulation – the social emotion regulation – and its neural underpinnings were investigated. Projects 1 and 2 of the current thesis expand the emotion part of emotion regulation. Project 1 investigated whether emotion regulation affects not only emotional response-related brain activity but also influences aversive prediction error-related activity, i.e., the motivation-related brain signal. We found that self- initiated reappraisal, a type of cognitive emotion regulation, indeed affected prediction error-related activity, such that this activity was enhanced in the ventral tegmental area, ventral striatum, insula and hippocampus, possibly via a prefrontal-tegmental pathway. Project 2 further examined the way emotion regulation affects emotions and prediction errors, by testing whether self- initiated reappraisal directly targets the brain network for motivated behaviour previously outlined by animal studies. We found that superior (in contrast to inferior) regulators affected the balance of competing influences of ventral striatal afferents on striatal aversive prediction error signals; they reduced the impact of subcortical striatal afferents (i.e., hippocampus, amygdala and ventral tegmental area), while keeping the influence of the prefrontal cortex on ventral striatal prediction errors constant. Inferior regulators, on the other hand, failed to supress subcortical inputs into the ventral striatum and instead counterproductively reduced the prefrontal influence on ventral striatal prediction error signals. Projects 3 and 4 of the thesis extend the regulation part of emotion regulation. Project 3 explored the neural correlates of social cognitive emotion regulation, specifically reappraisal, and directly compared them with those of self-initiated reappraisal. We found that regions of the anterior, the medial parietal, and the lateral temporo-parietal default mode network were specifically involved in social emotion regulation, and that social regulation success and the default mode network involvement during regulation were related to participants’ attachment security scores. Project 4 investigated social emotion modulation and its impact on two distinct types of emotional brain activity – emotional response- and aversive prediction error-related activity. We found – for the simple contrast of being with somebody versus being alone – a three-fold dissociation between signal types and insula subregions, including left and right anterior and posterior insula parts. Social emotion modulation reduced aversive stimulus-related activity in the posterior insula, while simultaneously increasing aversive prediction error-related activity in the anterior insula. Furthermore, the social effect on prediction error-related activity was positively associated with aversive learning in the right, but negatively in the left anterior insula. Altogether, by expanding the concept of emotion regulation, projects of the current thesis provide new insights into both the effects and the neural underpinnings of three distinct emotion regulation types. Considering that problems in both intrapersonal emotion regulation and social interaction are linked to affective disorders, our findings might contribute to a better understanding of these disorders and the disorder-specific emotional and social impairments

Cognitive emotion regulation enhances aversive prediction error activity while reducing emotional responses

Cognitive emotion regulation is a powerful way of modulating emotional responses. However, despite the vital role of emotions in learning, it is unknown whether the effect of cognitive emotion regulation also extends to the modulation of learning. Computational models indicate prediction error activity, typically observed in the striatum and ventral tegmental area, as a critical neural mechanism involved in associative learning. We used model-based fMRI during aversive conditioning with and without cognitive emotion regulation to test the hypothesis that emotion regulation would affect prediction error-related neural activity in the striatum and ventral tegmental area, reflecting an emotion regulation-related modulation of learning. Our results show that cognitive emotion regulation reduced emotion-related brain activity, but increased prediction error-related activity in a network involving ventral tegmental area, hippocampus, insula and ventral striatum. While the reduction of response activity was related to behavioral measures of emotion regulation success, the enhancement of prediction error-related neural activity was related to learning performance. Furthermore, functional connectivity between the ventral tegmental area and ventrolateral prefrontal cortex, an area involved in regulation, was specifically increased during emotion regulation and likewise related to learning performance. Our data, therefore, provide first-time evidence that beyond reducing emotional responses, cognitive emotion regulation affects learning by enhancing prediction error-related activity, potentially via tegmental dopaminergic pathways. (C) 2015 Elsevier Inc. All rights reserved