Neural correlates of incidental and directed facial emotion processing in adolescents and adults

Our knowledge on the development of the affective and cognitive circuitries that underlie affect regulation is still limited. This functional magnetic resonance imaging (fMRI) study examined whether there is more efficient prefrontal modulation of affective circuits with development. Ten adolescents (mean age 14 ± 2 years) and 10 adults (mean age 30 ± 6 years) underwent two scanning conditions that required different levels of cognitive control over face emotion processing. A ‘directed’ emotion processing condition required judgment of facial expressions. An ‘incidental’ emotion processing condition required an age judgment. For the incidental emotion processing condition, adolescents, compared with adults, showed less activation in right ventrolateral prefrontal cortex (VLPFC) and greater activation in paralimbic regions, suggesting greater emotional reactivity and immature prefrontal circuitries for affect regulation. For the directed emotion processing condition, adolescents, compared with adults, showed decreased recruitment of both the dorsal and pregenual right anterior cingulate cortex (ACC), suggesting immature modulatory functions of the ACC during directed face emotion processing. These results indicate that the neural circuitries for affect regulation are still developing in adolescence and have not yet reached the adult level.     

Neural bases of reappraisal regulatory effect on negative emotion in high reappraisers

Previous studies have reported that individual differences in reappraisal use are associated with particular patterns of neural activity. We hypothesized that if ’high reappraisers’ (individuals who use reappraisal well in a behavioral experiment) completed two training sessions, they would exhibit more reliable patterns of neural activity related to cognitive reappraisal. In the present study, 13 high reappraisers were selected from 27 healthy volunteers through an initial behavioral experiment (first training) followed by a functional MRI experiment (second training). Emotional images selected from the International Affective Picture System were used for both the behavioral and functional MRI sessions of the experiment. The behavioral results revealed that reappraisal reduced subjective unpleasantness. The functional MRI results revealed that the cognitive reappraisal used by high reappraisers decreased the activation of emotion-responsive regions, including the amygdala, insula, and cingulate gyrus, and increased the activation of regulation-related regions, including the inferior prefrontal cortex, orbital prefrontal cortex, and dorsal medial prefrontal cortex. These findings suggest the involvement of inferior orbital and dorsal medial prefrontal cortex in constructing reappraisal strategies that modulate activity in emotion-processing systems.     

Brain functional correlates of emotion regulation across adolescence and young adulthood

Few studies have examined the neural correlates of emotion regulation across adolescence and young adulthood. Existing studies of cognitive reappraisal indicate that improvements in regulatory efficiency may develop linearly across this period, in accordance with maturation of prefrontal cortical systems. However, there is also evidence for adolescent differences in reappraisal specific to the activation of “social‐information processing network” regions, including the amygdala and temporal‐occipital cortices. Here, we use fMRI to examine the neural correlates of emotional reactivity and reappraisal in response to aversive social imagery in a group of 78 adolescents and young adults aged 15–25 years. Within the group, younger participants exhibited greater activation of temporal‐occipital brain regions during reappraisal in combination with weaker suppression of amygdala reactivity—the latter being a general correlate of successful reappraisal. Further analyses demonstrated that these age‐related influences on amygdala reactivity were specifically mediated by activation of the fusiform face area. Overall, these findings suggest that enhanced processing of salient social cues (i.e., faces) increases reactivity of the amygdala during reappraisal and that this relationship is stronger in younger adolescents. How these relationships contribute to well‐known vulnerabilities of emotion regulation during this developmental period will be an important topic for ongoing research. Hum Brain Mapp 37:7–19, 2016. © 2015 Wiley Periodicals, Inc.     

Anticipatory brain activity predicts the success or failure of subsequent emotion regulation

Expectations about an upcoming emotional event have the power to shape one’s subsequent affective response for better or worse. Here, we used mediation analyses to examine the relationship between brain activity when anticipating the need to cognitively reappraise aversive images, amygdala responses to those images and subsequent success in diminishing negative affect. We found that anticipatory activity in right rostrolateral prefrontal cortex was associated with greater subsequent left amygdala responses to aversive images and decreased regulation success. In contrast, anticipatory ventral anterior insula activity was associated with reduced amygdala responses and greater reappraisal success. In both cases, left amygdala responses mediated the relationship between anticipatory activity and reappraisal success. These results suggest that anticipation facilitates successful reappraisal via reduced anticipatory prefrontal ‘cognitive’ elaboration and better integration of affective information in paralimbic and subcortical systems.     

Brain activation during cognitive reappraisal depending on regulation goals and stimulus valence

Neural bases of cognitive reappraisal may depend on the direction of regulation (up- or downregulation) and stimulus valence (positive or negative). This study aimed to examine this using a cognitive reappraisal task and conjunction analysis on a relatively large sample of 83 individuals. We identified regions in which activations were common for all these types of emotion regulation. We also investigated differences in brain activation between the ‘decrease’ and ‘increase’ emotional response conditions, and between the regulation of negative and positive emotions. The common activation across conditions involved mainly the prefrontal and temporal regions. Decreasing emotions was associated with stronger involvement of the dorsolateral prefrontal cortex, while increasing with activation of the amygdala and hippocampus. Regulation of negative emotions involved stronger activation of the lateral occipital cortex, while regulation of positive emotions involved stronger activation of the anterior cingulate cortex extending to the medial prefrontal cortex. This study adds to previous findings, not only by doing a conjunction analysis on both emotional valences and regulation goals, but also doing this in a bigger sample size. Results suggest that reappraisal is not a uniform process and may have different neural bases depending on regulation goals and stimulus valence.     

Electrocortical evidence of increased post-reappraisal neural reactivity and its link to depressive symptoms

Few studies have examined whether effortful emotion regulation has a protracted impact on subsequent affective appraisal, and even fewer have investigated this effect on a trial-by-trial basis. In this study, we hypothesized that engaging cognitive resources via reappraisal during a trial would result in a subsequent period of increased reactivity on the next trial, as quantified using event-related potentials and oscillations. Forty-eight healthy individuals passively viewed unpleasant and neutral pictures followed by an auditory instruction to either continue viewing normally or reappraise emotional response to pictures. Viewing unpleasant pictures yielded increased late positive potential (LPP) and decreased posterior alpha (8–13 Hz) compared with neutral pictures. A similar pattern was observed on trials that immediately ‘followed’ emotion regulation instructions. Moreover, individuals with increased self-reported depressive symptoms showed greater LPP and alpha modulation following emotion regulation, suggesting that these responses may relate to compromised emotion regulation ability. This study demonstrates that cognitive reappraisal induces subsequent heightened reactivity that may reflect transient resource depletion, and these effects are more pronounced among those with increased depressive symptoms. Interventions that focus on emotion regulation might use these electrocortical markers to track changes in regulatory efficacy.     

Brain structural basis of cognitive reappraisal and expressive suppression

Cognitive reappraisal and expressive suppression, two major emotion regulation strategies, are differentially related to emotional well-being. The aim of this study was to test the association of individual differences in these two emotion regulation strategies with gray matter volume of brain regions that have been shown to be involved in the regulation of emotions. Based on high-resolution magnetic resonance images of 96 young adults voxel-based morphometry was used to analyze the gray matter volumes of the a priori regions of interest, including amygdala, insula, dorsal anterior cingulate and paracingulate cortex, medial and lateral prefrontal cortex (PFC) and their association with cognitive reappraisal and expressive suppression usage as well as neuroticism. A positive association of cognitive reappraisal with right and tendentially left amygdala volume and of neuroticism with left amygdala volume (marginally significant) was found. Expressive suppression was related to dorsal anterior cingulate/paracingulate cortex and medial PFC gray matter volume. The results of this study emphasize the important role of the amygdala in individual differences in cognitive reappraisal usage as well as neuroticism. Additionally, the association of expressive suppression usage with larger volumes of the medial PFC and dorsal anterior/paracingulate cortex underpins the role of these regions in regulating emotion-expressive behavior.     

An fMRI Study of the Neural Correlates of Incidental Versus Directed Emotion Processing in Pediatric Bipolar Disorder

ObjectiveTo use functional neuroimaging to probe the affective circuitry dysfunctions underlying disturbances in emotion processing and emotional reactivity in pediatric bipolar disorder (PBD).MethodEqual numbers of controls (HC) and unmedicated patients with euthymia and PBD were matched for age, sex, race, socioeconomic status, and IQ (n = 10 per group; mean age 14.2 years [SD 2.0 years]). The task consisted of a “directed” emotion processing condition where subjects judged whether emotion in facial expression was positive or negative and an “incidental” condition where subjects judged whether faces expressing similar affect were older or younger than 35 years.ResultsRelative to the directed condition, the incidental condition elicited greater activation in the right amygdala and the right insula, the left middle frontal gyrus, and the left posterior cingulate cortex in patients with PBD, in contrast to the HC that showed greater activation in the right superior frontal gyrus. In both incidental and directed conditions, relative to visual fixation, patients with PBD showed less activation in the right prefrontal cortex (superior, middle, and inferior frontal gyri) and the pregenual anterior cingulate cortex and greater activation in the posterior visual and face-processing regions (i.e., right precuneus/cuneus, fusiform gyrus).ConclusionsIncreased amygdala activation observed in patients with PBD elicited by incidental emotional processing relative to directed emotional processing may indicate more intense automatic emotional reactivity. Furthermore, the right prefrontal systems that are believed to modulate affect seem to be less engaged in patients with PBD regardless of whether the emotion processing is incidental or directed, which may signify reduced top-down control of emotional reactivity in PBD.     

Hemodynamic correlates of emotion regulation in frontal lobe epilepsy patients and healthy participants

The ability to regulate emotions is indispensable for maintaining psychological health. It heavily relies on frontal lobe functions which are disrupted in frontal lobe epilepsy. Accordingly, emotional dysregulation and use of maladaptive emotion regulation strategies have been reported in frontal lobe epilepsy patients. Therefore, it is of clinical and scientific interest to investigate emotion regulation in frontal lobe epilepsy. We studied neural correlates of upregulating and downregulating emotions toward aversive pictures through reappraisal in 18 frontal lobe epilepsy patients and 17 healthy controls using functional magnetic resonance imaging. Patients tended to report more difficulties with impulse control than controls. On the neural level, patients had diminished activity during upregulation in distributed left‐sided regions, including ventrolateral and dorsomedial prefrontal cortex, angular gyrus and anterior temporal gyrus. Patients also showed less activity than controls in the left precuneus for upregulation compared to downregulation. Unlike controls, they displayed no task‐related activity changes in the left amygdala, whereas the right amygdala showed task‐related modulations in both groups. Upregulation‐related activity changes in the left inferior frontal gyrus, insula, orbitofrontal cortex, anterior and posterior cingulate cortex, and precuneus were correlated with questionnaire data on habitual emotion regulation. Our results show that structural or functional impairments in the frontal lobes disrupt neural mechanisms underlying emotion regulation through reappraisal throughout the brain, including posterior regions involved in semantic control. Findings on the amygdala as a major target of emotion regulation are in line with the view that specifically the left amygdala is connected with semantic processing networks.     

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 reappraisal’s 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.     

Inhibition in the face of emotion: Characterization of the spatial‐temporal dynamics that facilitate automatic emotion regulation

Emotion regulation mediates socio‐cognitive functions and is essential for interactions with others. The capacity to automatically inhibit responses to emotional stimuli is an important aspect of emotion regulation; the underlying neural mechanisms of this ability have been rarely investigated. Forty adults completed a Go/No‐go task during magnetoencephalographic (MEG) recordings, where they responded rapidly to either a blue or purple frame which contained angry or happy faces. Subjects responded to the target color in an inhibition (75% Go trials) and a vigilance condition (25% Go trials). As expected, inhibition processes showed early, sustained activation (200–450 ms) in the right inferior frontal gyrus (IFG). Emotion‐related inhibition processes showed greater activity with angry faces bilaterally in the orbital‐frontal gyri (OFG) starting at 225 ms and temporal poles from 250 ms, with right hemisphere dominance. The presence of happy faces elicited earlier activity in the right OFG. This study demonstrates that the timing of inhibition processes varies with the emotional context and that there is much greater activation in the presence of angry faces. It underscores the importance of the right IFG for inhibition processes, but the OFG in automatic emotion regulation.     

Neural indicators of emotion regulation via acceptance vs reappraisal in remitted major depressive disorder

Mood disorders are characterized by impaired emotion regulation abilities, reflected in alterations in frontolimbic brain functioning during regulation. However, little is known about differences in brain function when comparing regulatory strategies. Reappraisal and emotional acceptance are effective in downregulating negative affect, and are components of effective depression psychotherapies. Investigating neural mechanisms of reappraisal vs emotional acceptance in remitted major depressive disorder (rMDD) may yield novel mechanistic insights into depression risk and prevention. Thirty-seven individuals (18 rMDD, 19 controls) were assessed during a functional magnetic resonance imaging task requiring reappraisal, emotional acceptance or no explicit regulation while viewing sad images. Lower negative affect was reported following reappraisal than acceptance, and was lower following acceptance than no explicit regulation. In controls, the acceptance > reappraisal contrast revealed greater activation in left insular cortex and right prefrontal gyrus, and less activation in several other prefrontal regions. Compared with controls, the rMDD group had greater paracingulate and right midfrontal gyrus (BA 8) activation during reappraisal relative to acceptance. Compared with reappraisal, acceptance is associated with activation in regions linked to somatic and emotion awareness, although this activation is associated with less reduction in negative affect. Additionally, a history of MDD moderated these effects.     

Dedifferentiation of emotion regulation strategies in the aging brain

Different emotion regulation strategies are distinctly represented in the brains of younger adults. Decreasing a reaction to a negative situation by reinterpreting it (reappraisal) relies on cognitive control regions in the prefrontal cortex, while distracting away from a stressor involves more posterior medial structures. In this study, we used Multi-Voxel pattern analyses (MVPA) to examine whether reappraisal and distraction strategies have distinct representations in the older adult brain, or whether emotion regulation strategies become more dedifferentiated in later life. MVPA better differentiated the two emotion regulation strategies for younger adults than for older adults, and revealed the greatest age-related differences in differentiation in the posterior medial cortex (PMC). Univariate analyses revealed equal PMC recruitment across strategies for older adults, but greater activity during distraction than reappraisal for younger adults. The PMC is central to self-focused processing, and thus our findings are consistent with the possibility that focusing on the self may be a default mechanism across emotion regulation strategies for older people.     

Variation in orbitofrontal cortex volume: relation to sex, emotion regulation and affect

Sex differences in brain structure have been examined extensively but are not completely understood, especially in relation to possible functional correlates. Our two aims in this study were to investigate sex differences in brain structure, and to investigate a possible relation between orbitofrontal cortex subregions and affective individual differences. We used tensor-based morphometry to estimate local brain volume from MPRAGE images in 117 healthy right-handed adults (58 female), age 18–40 years. We entered estimates of local brain volume as the dependent variable in a GLM, controlling for age, intelligence and whole-brain volume. Men had larger left planum temporale. Women had larger ventromedial prefrontal cortex (vmPFC), right lateral orbitofrontal (rlOFC), cerebellum, and bilateral basal ganglia and nearby white matter. vmPFC but not rlOFC volume covaried with self-reported emotion regulation strategies (reappraisal, suppression), expressivity of positive emotions (but not of negative), strength of emotional impulses, and cognitive but not somatic anxiety. vmPFC volume statistically mediated sex differences in emotion suppression. The results confirm prior reports of sex differences in orbitofrontal cortex structure, and are the first to show that normal variation in vmPFC volume is systematically related to emotion regulation and affective individual differences.     

Neural representation of emotion regulation goals

The use of top–down cognitive control mechanisms to regulate emotional responses as circumstances change is critical for mental and physical health. Several theoretical models of emotion regulation have been postulated; it remains unclear, however, in which brain regions emotion regulation goals (e.g., the downregulation of fear) are represented. Here, we examined the neural mechanisms of regulating emotion using fMRI and identified brain regions representing reappraisal goals. Using a multimethodological analysis approach, combining standard activation‐based and pattern‐information analyses, we identified a distributed network of lateral frontal, temporal, and parietal regions implicated in reappraisal and within it, a core system that represents reappraisal goals in an abstract, stimulus‐independent fashion. Within this core system, the neural pattern‐separability in a subset of regions including the left inferior frontal gyrus, middle temporal gyrus, and inferior parietal lobe was related to the success in emotion regulation. Those brain regions might link the prefrontal control regions with the subcortical affective regions. Given the strong association of this subsystem with inner speech functions and semantic memory, we conclude that those cognitive mechanisms may be used for orchestrating emotion regulation. Hum Brain Mapp 37:600–620, 2016. © 2015 Wiley Periodicals, Inc.     

The role of the medial frontal cortex in the maintenance of emotional states

Evidence is accruing that people can maintain their emotional states, but how they do it and which brain regions are responsible still remains unclear. We examined whether people maintain emotional states ‘actively’, with explicit elaboration of the emotion, or ‘passively’, without elaboration. Twenty-four participants completed an emotion maintenance task in which they either maintained the emotional intensity from the first picture of a pair to compare to that of the second picture (‘maintain’ condition), or only rated their emotional response to the second picture (‘non-maintain’ condition). Supporting the ‘active’ maintenance hypothesis, when maintaining vs not maintaining emotion, participants exhibited increased height and width of activation in the dorsal medial frontal cortex (MFC) and lateral prefrontal cortex, regions associated with explicit emotion generation and manipulation of contents in working memory, respectively. Supporting the ‘passive’ maintenance hypothesis, however, when viewing negative emotional pictures (vs neutral pictures) that were not explicitly maintained, participants exhibited greater duration of activity in the rostral MFC, a region associated with implicit emotion generation. Supported by behavioral findings, this evidence that people maintain emotional states both naturally in the rMFC and strategically in the dMFC may be critical for understanding normal as well as disordered emotion regulation.     

The neural correlates of sex differences in emotional reactivity and emotion regulation

Sex differences in emotional responding have been repeatedly postulated but less consistently shown in empirical studies. Because emotional reactions are modulated by cognitive appraisal, sex differences in emotional responding might depend on differences in emotion regulation. In this study, we investigated sex differences in emotional reactivity and emotion regulation using a delayed cognitive reappraisal paradigm and measured whole‐brain BOLD signal in 17 men and 16 women. During fMRI, participants were instructed to increase, decrease, or maintain their emotional reactions evoked by negative pictures in terms of cognitive reappraisal. We analyzed BOLD responses to aversive compared to neutral pictures in the initial viewing phase and the effect of cognitive reappraisal in the subsequent regulation phase. Women showed enhanced amygdala responding to aversive stimuli in the initial viewing phase, together with increased activity in small clusters within the prefrontal cortex and the temporal cortex. During cognitively decreasing emotional reactions, women recruited parts of the orbitofrontal cortex, the anterior cingulate, and the dorsolateral prefrontal cortex to a lesser extent than men, while there was no sex effect on amygdala activity. In contrast, compared to women, men showed an increased recruitment of regulatory cortical areas during cognitively increasing initial emotional reactions, which was associated with an increase in amygdala activity. Clinical implications of these findings are discussed. Hum Brain Mapp, 2010. © 2009 Wiley‐Liss, Inc.     

In search of the depressive self: extended medial prefrontal network during self-referential processing in major depression

Major depression is associated with an excessive self-focus, a tendency to engage oneself in self-referential processing. The medial frontal gyrus (MFG) is central to self-referential processing. This study aimed to explore the neural bases of this excessive self-focus and to disambiguate the role of the MFG in the pathophysiology of major depression. We presented 15 depressed patients and 15 healthy subjects with personality traits during functional magnetic resonance imaging and asked them to judge whether each trait described them (‘self’ condition) or a generally desirable trait (‘general’ condition). Both patients and healthy subjects activated the MFG in ‘self’ vs ‘general’ condition. However, the activation of the dorsal part of the MFG and of the dorsolateral prefrontal cortex (DLPFC) in ‘self’ vs ‘general’ condition was unique to patients. Additionally, patients displayed an increased functional connectivity between the MFG, the dorsal anterior cingulate cortex and the DLPFC. These results provide evidence for an extended medial prefrontal network during self-referential processing in major depression, suggesting the involvement of a greater cognitive control.     

Evidence for dissociable cognitive and neural pathways from poverty versus maltreatment to deficits in emotion regulation

Poverty and threat exposure (TE) predict deficits in emotion regulation (ER). Effective cognitive ER (i.e., reappraisal) may be supported by: (1) cognitive processes implicated in generating and implementing cognitive reappraisal, supported by activation in brain regions involved in cognitive control (e.g., frontal, insular, and parietal cortices) and (2) emotion processing and reactivity, involving identification, encoding, and maintenance of emotional states and related variation in brain activity of regions involved in emotional reactivity (i.e., amygdala). Poverty is associated with deficits in cognitive control, and TE with alterations in emotion processing and reactivity. Our goal was to identify dissociable emotional and cognitive pathways to ER deficits from poverty and TE. Measures of cognitive ability, emotional processing and reactivity, ER, and neural activity during a sadness ER task, were examined from a prospective longitudinal study of youth at risk for depression (n = 139). Both cognitive ability and left anterior insula extending into the frontal operculum activity during a sadness reappraisal task mediated the relationship between poverty and ER. Emotion processing/reactivity didn’t mediate the relationship of TE to ER. Findings support a cognitive pathway from poverty to ER deficits. They also underscore the importance of dissociating mechanisms contributing to ER impairments from adverse early childhood experiences.     

Dispositional use of emotion regulation strategies and resting-state cortico-limbic functional connectivity

Neuroimaging functional connectivity (FC) analyses have shown that the negative coupling between the amygdala and cortical regions is linked to better emotion regulation in experimental settings. Nevertheless, no studies have examined the association between resting-state cortico-amygdalar FC and the dispositional use of emotion regulation strategies. We aim at assessing the relationship between the resting-state FC patterns of two different amygdala territories, with different functions in the emotion response process, and trait-like measures of cognitive reappraisal and expressive suppression. Forty-eight healthy controls completed the Emotion Regulation Questionnaire (ERQ) and underwent a resting-state functional magnetic resonance imaging acquisition. FC maps of basolateral and centromedial amygdala (BLA/CMA) with different cortical areas were estimated with a seed-based approach, and were then correlated with reappraisal and suppression scores from the ERQ. FC between left BLA and left insula and right BLA and the supplementary motor area (SMA) correlated inversely with reappraisal scores. Conversely, FC between left BLA and the dorsal anterior cingulate cortex correlated directly with suppression scores. Finally, FC between left CMA and the SMA was inversely correlated with suppression. Top-down regulation from the SMA seems to account for the dispositional use of both reappraisal and suppression depending on the specific amygdala nucleus being modulated. In addition, modulation of amygdala activity from cingulate and insular cortices seem to also account for the habitual use of the different emotion regulation strategies.