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

Implicit and Explicit Emotion Regulation: Modulation by Aggressive Subtypes

Emotion regulation consists of multiple processes that serve to modify emotional reactions. This thesis examines both implicit (automatic) and explicit (deliberate) processes and explores how their function and efficacy are modulated by individual differences in subtypes of aggressive behaviour. These questions are examined in both healthy adults and adolescents. Methods include cognitive testing, self-report, heart rate perception, skin conductance response and functional magnetic resonance imaging. Using a paradigm where emotion is task-irrelevant, Chapter 2 explores how attention is implicitly captured by emotional faces and shows that core psychopathic traits are associated with reduced attention capture by fearful faces in a community sample. Chapter 3 investigates the conditions under which emotion can, and cannot, implicitly capture attention by varying cognitive load in a series of experiments. From Chapter 4 onwards, explicit emotion regulation is investigated. In Chapter 4 the efficacy of three subtypes of psychological distancing, a form of cognitive reappraisal, is examined. It is shown that interoceptive awareness of bodily states influences the ability to use distancing to regulate emotion effectively. Chapter 5 focuses on the efficacy of one of these strategies, namely temporal distancing (e.g. ‘this too shall pass’), across the transition from adolescence to adulthood. Using a novel experimental task, temporal distancing was shown to be effective across the age range studied, but was reduced with increasing reactive aggression. Neural correlates of temporal distancing are discussed in Chapter 6, which employs an fMRI-adapted version of the task used in Chapter 5. This thesis concludes that subtypes of aggression influence emotion regulation in different ways. It is therefore crucial to take aggression into account in order to understand individual differences in implicit and explicit emotion regulation

The Simon Effect in Rats: A Comparative Study on Conflict and Error Processing Using Electrophysiology and Functional µPET Imaging

Both humans and animals have the ability to learn from past experience and to adapt their behavior to resolve future conflicts faster or avoid them entirely. Conflicts in spatial stimulus–response tasks occur when the origin of the stimulus and the response area differ in location. Those conflicts lead to increased error rates, reaction times (RT) and movement time (MT) which has been termed Simon effect. A model of dual route processing (automatic and intentional) of stimulus features has been proposed, predicting response conflicts if the two routes are incongruent. Although there are various theories related to underlying neuronal mechanisms, it is commonly assumed that the anterior cingulate cortex (ACC) plays a crucial role in conflict and error processing. The Simon task is a neuropsychological interference task commonly used to study performance monitoring. Interestingly, the resulting conflict is far from uniquely human, as it has also been observed in pigeons, rats, and monkeys. On a neural level, the on-going monitoring of correct and incorrect behavior appears in the form of eventrelated potentials (ERPs). More precisely, the error-related negativity (ERN/Ne) component of the resulting ERP, assumed to be generated in the ACC, is suggested to reflect conflict and error monitoring. Unfortunately, there is often little correspondence between human and animal studies. On this account the present study uses a modified auditory Simon task to investigate a) the anatomical basis, b) the conflict- and errorrelated electrophysiological correlates and c) the performance monitoring from a crossspecies point of view. By using positron emission tomography (PET) in combination with the metabolic tracer [18F]fluorodeoxyglucose, which accumulates in metabolically active brain cells during the behavioral task, we first aim at identifying relevant brain areas in a rat model of the Simon task. According to the dual route model, brain areas involved in conflict processing are supposed to be activated when automatic and intentional route lead to different responses (dual route model). Results show specific activation patterns for different task settings coherent with the dual route model. Our data suggest that the rat motor cortex (M1) may be part of the automatic route or involved in its facilitation, while premotor (M2) and prelimbic areas, as well as the ACC appear to be essential for inhibiting the incorrect, automatic response, indicating conflict monitoring functions. Interestingly, our findings remarkably fit the pattern of activated regions reported during conflict processing in humans. To further support our findings, we measured local field potentials (LFP) from electrodes centered in the rat ACC. LFPs showed a negative slow wave less pronounced for errors at about 250-400 ms after reaction. Stimulus-locked data revealed a compatibility effect in rats, with a negative slow wave with onset in the latency range of the reaction. To finally compare these results with a human setup, we also developed a translational task for humans. In both species, similar behavioral effects were found, including an increase in error rate, RT and MT. In humans, although no difference in EEG amplitude between errors and hits in the ERN latency range was found, a pronounced error positivity between 250 and 350 ms after reaction was seen. Humans surprisingly demonstrated a stronger negativity for compatible compared to incompatible trials. Similarly to rats, this effect started at about the time of reaction time. Thus, both species (i) showed electrophysiological responses differentiating between errors and correct in a similar latency range, (ii) demonstrated a valid occurrence of the Simon effect and seem to pursue similar response strategies, both in terms of RT and MT and (iii) displayed sustained differences in the modulation of the ERP depending on correct or incorrect responses starting at the time of response and prior to reward/no reward. It is thus tempting to speculate that the underlying cognitive error processing mechanisms are highly similar across species. In conclusion, we found remarkable behavioral, electrophysiological and functional similarities between rat and human conflict and error processing. Our paradigm offers a new approach in integrative, cross-species research and provides a useful rodent model for investigating performance monitoring

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

Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval.

Abstract Functional MRI was used to investigate the role of medial temporal lobe and inferior frontal lobe regions in autobiographical recall. Prior to scanning, participants generated cue words for 50 autobiographical memories and rated their phenomenological properties using our autobiographical memory questionnaire (AMQ). During scanning, the cue words were presented and participants pressed a button when they retrieved the associated memory. The autobiographical retrieval task was interleaved in an event-related design with a semantic retrieval task (category generation). Region-of-interest analyses showed greater activation of the amygdala, hippocampus, and right inferior frontal gyrus during autobiographical retrieval relative to semantic retrieval. In addition, the left inferior frontal gyrus showed a more prolonged duration of activation in the semantic retrieval condition. A targeted correlational analysis revealed pronounced functional connectivity among the amygdala, hippocampus, and right inferior frontal gyrus during autobiographical retrieval but not during semantic retrieval. These results support theories of autobiographical memory that hypothesize co-activation of frontotemporal areas during recollection of episodes from the personal past

Brain Computations and Connectivity [2nd edition]

This is an open access title available under the terms of a CC BY-NC-ND 4.0 International licence. It is free to read on the Oxford Academic platform and offered as a free PDF download from OUP and selected open access locations. Brain Computations and Connectivity is about how the brain works. In order to understand this, it is essential to know what is computed by different brain systems; and how the computations are performed. The aim of this book is to elucidate what is computed in different brain systems; and to describe current biologically plausible computational approaches and models of how each of these brain systems computes. Understanding the brain in this way has enormous potential for understanding ourselves better in health and in disease. Potential applications of this understanding are to the treatment of the brain in disease; and to artificial intelligence which will benefit from knowledge of how the brain performs many of its extraordinarily impressive functions. This book is pioneering in taking this approach to brain function: to consider what is computed by many of our brain systems; and how it is computed, and updates by much new evidence including the connectivity of the human brain the earlier book: Rolls (2021) Brain Computations: What and How, Oxford University Press. Brain Computations and Connectivity will be of interest to all scientists interested in brain function and how the brain works, whether they are from neuroscience, or from medical sciences including neurology and psychiatry, or from the area of computational science including machine learning and artificial intelligence, or from areas such as theoretical physics

Psychological and Neural Processing of Social Risk and Discrepancy in Major Depressive Disorder

Major Depressive Disorder (MDD) is one of the most prevalent health conditions in the world, characterised by persistent low mood and disruption to education, relationships, and employment. Disruption to social functioning is a core feature of MDD, and this dimension of the disorder may offer valuable insight into its aetiology. This thesis aims to extend our understanding of social processing in MDD by testing hypotheses generated from a socio-evolutionary theoretical framework of MDD, with particular emphasis on the Social Risk Hypothesis of Depressed Mood, which conceptualises depressed mood as an adaptive response to elevated risk of social exclusion. The thesis pursues these aims utilising novel protocols and neuroeconomic games to examine social risk-taking and self-discrepancies, and by examining the role of regions of the physical pain network in social function and processing of unexpected social information. The thesis consists of nine chapters; one general methodology chapter (Chapter 3), five chapters detailing novel experimental studies (Chapters 4,5,6,7 and 8), one describing a reanalysis of existing data (Chapter 2), one introductory chapter and one discussion chapter (Chapters 1 and 9 respectively). Across these chapters, the thesis presents neural and behavioural evidence that MDD is associated with reduced social risk-taking, increased sensitivity to an exclusion-relevant context (in-group interactions) and stronger enforcement of social norms. The thesis presents neural evidence of a negative processing bias for self-discrepancies in MDD, linked to activation in the dorsal anterior cingulate cortex and anterior insula, and suggesting a role for perfectionism as a transdiagnostic sensitivity to such discrepancies. Suggestions for future research are discussed, including increased utilisation of neuroeconomic games, particularly in relation to assessing social function as a transdiagnostic marker. Overall, the thesis provides support for socio-evolutionary frameworks of affect, and highlights their unique perspective for understanding affective disorders, with some ‘deficits’ usefully reconceptualised as adaptive mechanisms

Public policy, social marketing and neuromarketing: from addressing the consumer behaviour to addressing the social behaviour - a study on the assessment of Public Service Announcements’ efficacy by neuro-metric indexes and techniques

The overall aim of this thesis is to investigate to what extent marketing can be a useful science for the public policy in developing effective Public Service Announcements (PSAs). In particular, hereby a specific discipline will be taken in consideration: the one that merges marketing with neuroscience, that is the so-called ‘neuromarketing’, which - in order to assess the advertising efficacy - adopts biometric and neurometric indexes. The objective of this work is to gain insights into the above-mentioned fields (marketing, neuroscience and public policy) by: - reviewing previous studies, as well as topical literature; - exploring the latest case studies and best practises; - examining the traditional methods’ results for the assessment of the PSAs (i.e. polls, surveys, focus groups) in their evolutionary path (till arriving to birth of the the neurometric methods) Such kind of research has the purpose to identify the factors that are considered relevant to answer the ultimate research question: is it possible today, by using state-of-the-art neurometric indexes and techniques, to provide policymakers with precise guidelines for developing effective PSAs, so that marketing will be able to address no more just the consumer behaviour, but also the social behaviour? In fact, the goal of any advertising campaign is to convey a specific message and reach a specific audience: the consumers. But, when talking about PSAs, many things changes: the KPIs for the assessment of their efficacy are no longer the commercial ones (GRP, reach etc.), but rather the gain obtained in public health after the airing of the campaign. Consequently, the specific message will be a different ‘call-to-action’: no more an invite to purchase, but rather to change a (wrong) social behaviour or adopt a (right) civil conscience. Given these premises, it is possible that marketing could be invested with a precise responsibility in terms of lives saved and public health. The practical and managerial implications of the research are the following: EU policymakers and local governments will have the opportunity to dispose of scientific data and information about the society that might be transformed in guidelines for producing effective PSAs based on the inner audience’s insights. The originality of this research resides in having framed the new neuromarketing protocols in the traditional Consumer Behaviour theory, combining thus future and past of the marketing research