Jennifer A. Silvers

Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion

This paper reviews and synthesizes functional imaging research that over the past decade has begun to offer new insights into the brain mechanisms underlying emotion regulation. Toward that end, the first section of the paper outlines a model of the processes and neural systems involved in emotion generation and regulation. The second section surveys recent research supporting and elaborating the model, focusing primarily on studies of the most commonly investigated strategy, which is known as reappraisal. At its core, the model specifies how prefrontal and cingulate control systems modulate activity in perceptual, semantic, and affect systems as a function of ones regulatory goals, tactics, and the nature of the stimuli and emotions being regulated. This section also shows how the model can be generalized to understand the brain mechanisms underlying other emotion regulation strategies as well as a range of other allied phenomena. The third and last section considers directions for future research, including how basic models of emotion regulation can be translated to understand changes in emotion across the life span and in clinical disorders.

Cognitive Reappraisal of Emotion: A Meta-Analysis of Human Neuroimaging Studies

In recent years, an explosion of neuroimaging studies has examined cognitive reappraisal, an emotion regulation strategy that involves changing the way one thinks about a stimulus in order to change its affective impact. Existing models broadly agree that reappraisal recruits frontal and parietal control regions to modulate emotional responding in the amygdala, but they offer competing visions of how this is accomplished. One view holds that control regions engage ventromedial prefrontal cortex (vmPFC), an area associated with fear extinction, that in turn modulates amygdala responses. An alternative view is that control regions modulate semantic representations in lateral temporal cortex that indirectly influence emotion-related responses in the amygdala. Furthermore, while previous work has emphasized the amygdala, whether reappraisal influences other regions implicated in emotional responding remains unknown. To resolve these questions, we performed a meta-analysis of 48 neuroimaging studies of reappraisal, most involving downregulation of negative affect. Reappraisal consistently 1) activated cognitive control regions and lateral temporal cortex, but not vmPFC, and 2) modulated the bilateral amygdala, but no other brain regions. This suggests that reappraisal involves the use of cognitive control to modulate semantic representations of an emotional stimulus, and these altered representations in turn attenuate activity in the amygdala.

Concurrent and lasting effects of emotion regulation on amygdala response in adolescence and young adulthood

This study used functional MRI (fMRI) to examine a novel aspect of emotion regulation in adolescent development: whether age predicts differences in both the concurrent and lasting effects of emotion regulation on amygdala response. In the first, active regulation, phase of the testing session, fMRI data were collected while 56 healthy individuals (age range: 10.50-22.92 years) reappraised aversive stimuli so as to diminish negative responses to them. After a short delay, the second, re-presentation, phase involved passively viewing the aversive images from the reappraisal task. During active regulation, older individuals showed greater drops in negative affect and inverse rostrolateral prefrontal-amygdala connectivity. During re-presentation, older individuals continued to show lasting reductions in the amygdala response to aversive stimuli they had previously reappraised, an effect mediated by rostrolateral PFC. These data suggest that one source of heightened emotionality in adolescence is a diminished ability to cognitively down-regulate aversive reactions.

Curbing Craving Behavioral and Brain Evidence That Children Regulate Craving When Instructed to Do So but Have Higher Baseline Craving Than Adults

Although one third of children and adolescents are overweight or obese, developmental changes in food craving and the ability to regulate craving remain poorly understood. We addressed this knowledge gap by examining behavioral and neural responses to images of appetizing unhealthy foods in individuals ages 6 through 23 years. On close trials (assessing unregulated craving), participants focused on a pictured food’s appetitive features. On far trials (assessing effortful regulation), participants focused on a food’s visual features and imagined that it was farther away. Across conditions, older age predicted less craving, less striatal recruitment, greater prefrontal activity, and stronger frontostriatal coupling. When effortfully regulating their responses to the images, all participants reported less craving and exhibited greater recruitment of lateral prefrontal cortex and less recruitment of ventromedial prefrontal cortex. Greater body mass predicted less regulation-related prefrontal activity, particularly among children. These results suggest that children experience stronger craving than adults but can also effectively regulate craving. Moreover, the mechanisms underlying regulation may differ for heavy and lean children.

Bad and worse: neural systems underlying reappraisal of high- and low-intensity negative emotions

One of the most effective strategies for regulating emotional responses is cognitive reappraisal. While prior work has made great strides in characterizing reappraisals neural mechanisms and behavioral outcomes, the key issue of how regulation varies as a function of emotional intensity remains unaddressed. We compared the behavioral and neural correlates of reappraisal of high- and low-intensity emotional responses using functional magnetic resonance imaging (fMRI). We found that successful reappraisal of both high- and low-intensity emotions depends upon recruitment of dorsomedial (dmPFC) as well as left dorsolateral (dlPFC) and ventrolateral (vlPFC) prefrontal cortex. However, reappraisal of high-intensity emotions more strongly activated left dlPFC, and in addition, activated right lateral and dorsomedial PFC regions not recruited by low-intensity reappraisal. No brain regions were more strongly recruited during reappraisal of low when compared with high-intensity emotions. Taken together, these results suggest that reappraisal of high-intensity emotion requires greater cognitive resources as evidenced by quantitative and qualitative differences in prefrontal recruitment. These data have implications for understanding how and when specific PFC systems are needed to regulate different types of emotional responses.

Previous Institutionalization Is Followed by Broader Amygdala-Hippocampal-PFC Network Connectivity during Aversive Learning in Human Development

Early institutional care can be profoundly stressful for the human infant, and, as such, can lead to significant alterations in brain development. In animal models, similar variants of early adversity have been shown to modify amygdala–hippocampal–prefrontal cortex development and associated aversive learning. The current study examined this rearing aberration in human development. Eighty-nine children and adolescents who were either previously institutionalized (PI youth; N = 46; 33 females and 13 males; age range, 7–16 years) or were raised by their biological parents from birth (N = 43; 22 females and 21 males; age range, 7–16 years) completed an aversive-learning paradigm while undergoing functional neuroimaging, wherein visual cues were paired with either an aversive sound (CS+) or no sound (CS−). For the PI youth, better aversive learning was associated with higher concurrent trait anxiety. Both groups showed robust learning and amygdala activation for CS+ versus CS− trials. However, PI youth also exhibited broader recruitment of several regions and increased hippocampal connectivity with prefrontal cortex. Stronger connectivity between the hippocampus and ventromedial PFC predicted significant improvements in future anxiety (measured 2 years later), and this was particularly true within the PI group. These results suggest that for humans as well as for other species, early adversity alters the neurobiology of aversive learning by engaging a broader prefrontal–subcortical circuit than same-aged peers. These differences are interpreted as ontogenetic adaptations and potential sources of resilience. SIGNIFICANCE STATEMENT Prior institutionalization is a significant form of early adversity. While nonhuman animal research suggests that early adversity alters aversive learning and associated neurocircuitry, no prior work has examined this in humans. Here, we show that youth who experienced prior institutionalization, but not comparison youth, recruit the hippocampus during aversive learning. Among youth who experienced prior institutionalization, individual differences in aversive learning were associated with worse current anxiety. However, connectivity between the hippocampus and prefrontal cortex prospectively predicted significant improvements in anxiety 2 years following scanning for previously institutionalized youth. Among youth who experienced prior institutionalization, age-atypical engagement of a distributed set of brain regions during aversive learning may serve a protective function.

The transition from childhood to adolescence is marked by a general decrease in amygdala reactivity and an affect-specific ventral-to-dorsal shift in medial prefrontal recruitment

Understanding how and why affective responses change with age is central to characterizing typical and atypical emotional development. Prior work has emphasized the role of the amygdala and prefrontal cortex (PFC), which show age-related changes in function and connectivity. However, developmental neuroimaging research has only recently begun to unpack whether age effects in the amygdala and PFC are specific to affective stimuli or may be found for neutral stimuli as well, a possibility that would support a general, rather than affect-specific, account of amygdala-PFC development. To examine this, 112 individuals ranging from 6 to 23 years of age viewed aversive and neutral images while undergoing fMRI scanning. Across age, participants reported more negative affect and showed greater amygdala responses for aversive than neutral stimuli. However, children were generally more sensitive to both neutral and aversive stimuli, as indexed by affective reports and amygdala responses. At the same time, the transition from childhood to adolescence was marked by a ventral-to-dorsal shift in medial prefrontal responses to aversive, but not neutral, stimuli. Given the role that dmPFC plays in executive control and higher-level representations of emotion, these results suggest that adolescence is characterized by a shift towards representing emotional events in increasingly cognitive terms.

Toward a Personalized Science of Emotion Regulation: Personalized Emotion Regulation

The ability to successfully regulate emotion plays a key role in healthy development and the maintenance of psychological well-being. Although great strides have been made in understanding the nature of regulatory processes and the consequences of deploying them, a comprehensive understanding of emotion regulation that can specify what strategies are most beneficial for a given person in a given situation is still a far-off goal. In this review, we argue that moving toward this goal represents a central challenge for the future of the field. As an initial step, we propose a concrete framework that (i) explicitly considers emotion regulation as an interaction of person, situation, and strategy, (ii) assumes that regulatory effects vary according to these factors, and (iii) sets as a primary scientific goal the identification of person-, situation-, and strategy-based contingencies for successful emotion regulation. Guided by this framework, we review current questions facing the field, discuss examples of contextual variation in emotion regulation success, and offer practical suggestions for continued progress in this area.

Vigilance, the Amygdala, and Anxiety in Youths With a History of Institutional Care

BACKGROUND Early adversity is commonly associated with alterations of amygdala circuitry and increased anxiety. While many theoretical and clinical accounts of early adversity suggest that it increases vigilance to threatening stimuli, the present study tested whether heightened anxiety and amygdala reactivity associated with early adversity enhanced goal-directed attention for threatening stimuli. Showing this association would provide support that these adversity-induced alterations are developmental adaptations of the individual. METHODS 34 children and adolescents who experienced early adversity in the form of previous institutionalization (PI) (26 female, mean age=13.49 years) and a comparison group of 33 children and adolescents who were reared by their biological parents since birth (16 female, mean age=13.40 years) underwent fMRI scanning while completing a visual search task that involved quickly locating a negative (fearful face) or positive target (happy face) in an array of neutral distractor stimuli (neutral faces). RESULTS Across both groups, individual differences in vigilant behavior were positively associated with amygdala responses for negative versus positive stimuli. However, a moderation analysis revealed that the degree to which amygdala responses were greater for negative versus positive stimuli was associated with greater anxiety symptomology for PI youth, but not comparison youth. CONCLUSIONS Together, these findings suggest that institutional care strengthens linkages between amygdala reactivity and anxiety, perhaps serving to enhance goal-directed attention. The findings are discussed as both adaptations as well as risk to the individual.

Spatial and Temporal Cortical Variability Track with Age and Affective Experience During Emotion Regulation in Youth

Variability is a fundamental feature of human brain activity that is particularly pronounced during development. However, developmental neuroimaging research has only recently begun to move beyond characterizing brain function exclusively in terms of magnitude of neural activation to incorporate estimates of variability. No prior neuroimaging study has done so in the domain of emotion regulation. We investigated how age and affective experiences relate to spatial and temporal variability in neural activity during emotion regulation. In the current study, 70 typically developing youth aged 8-17 years completed a cognitive reappraisal task of emotion regulation while undergoing functional magnetic resonance imaging. Estimates of spatial and temporal variability during regulation were calculated across a network of brain regions, defined a priori, and were then related to age and affective experiences. Results showed that increasing age was associated with reduced spatial and temporal variability in a set of frontoparietal regions (e.g., dorsomedial prefrontal cortex, superior parietal lobule) known to be involved in effortful emotion regulation. In addition, youth who reported less negative affect during regulation had less spatial variability in the ventrolateral prefrontal cortex, which has previously been linked to cognitive reappraisal. We interpret age-related reductions in spatial and temporal variability as implying neural specialization. These results suggest that the development of emotion regulation is undergirded by a process of neural specialization and open up a host of possibilities for incorporating neural variability into the study of emotion regulation development.