Variety in emotional life: within-category typicality of emotional experiences is associated with neural activity in large-scale brain networks

The tremendous variability within categories of human emotional experience receives little empirical attention. We hypothesized that atypical instances of emotion categories (e.g. pleasant fear of thrill-seeking) would be processed less efficiently than typical instances of emotion categories (e.g. unpleasant fear of violent threat) in large-scale brain networks. During a novel fMRI paradigm, participants immersed themselves in scenarios designed to induce atypical and typical experiences of fear, sadness or happiness (scenario immersion), and then focused on and rated the pleasant or unpleasant feeling that emerged (valence focus) in most trials. As predicted, reliably greater activity in the ‘default mode’ network (including medial prefrontal cortex and posterior cingulate) was observed for atypical (vs typical) emotional experiences during scenario immersion, suggesting atypical instances require greater conceptual processing to situate the socio-emotional experience. During valence focus, reliably greater activity was observed for atypical (vs typical) emotional experiences in the ‘salience’ network (including anterior insula and anterior cingulate), suggesting atypical instances place greater demands on integrating shifting body signals with the sensory and social context. Consistent with emerging psychological construction approaches to emotion, these findings demonstrate that is it important to study the variability within common categories of emotional experience.     

Common and distinct brain networks underlying explicit emotional evaluation: a meta-analytic study

Brain mechanisms underlying explicit evaluation of emotion have been explored using different tasks including ‘stimulus-focused evaluation’, ‘evaluation of one''s own emotion’ and ‘evaluation of others’ emotions’. Yet the extent to which similar brain mechanisms underlie different evaluation tasks is unclear. A meta-analysis of published neuroimaging studies of explicit emotional evaluation was conducted to examine common and distinct regions underlying these different evaluation tasks. This study revealed regions common to all three tasks: The amygdala and LPFC as common regions may be involved in emotion–cognition interactions, and the DMPFC may possibly play integrative roles in explicit emotional evaluation. Distinct regions were also identified: (i) the sensory cortex and VLPFC were specifically associated with ‘stimulus evaluation’, possibly involved in perceptual and conceptual processing; (ii) the insula and rACC were specifically associated with ‘evaluation of one''s own emotion’, potentially associated with interoceptive and experiential processing; and (iii) the STS and TPJ were specifically associated with ‘evaluation of others’ emotions’, potentially reflecting their roles in TOM and empathy. These findings suggest that different types of explicit emotional evaluation may involve common and distinct networks and provide new insights on multiple mechanisms underlying explicit emotional evaluation.     

The neural correlates of emotion alignment in social interaction

Talking about emotion and sharing emotional experiences is a key component of human interaction. Specifically, individuals often consider the reactions of other people when evaluating the meaning and impact of an emotional stimulus. It has not yet been investigated, however, how emotional arousal ratings and physiological responses elicited by affective stimuli are influenced by the rating of an interaction partner. In the present study, pairs of participants were asked to rate and communicate the degree of their emotional arousal while viewing affective pictures. Strikingly, participants adjusted their arousal ratings to match up with their interaction partner. In anticipation of the affective picture, the interaction partner’s arousal ratings correlated positively with activity in anterior insula and prefrontal cortex. During picture presentation, social influence was reflected in the ventral striatum, that is, activity in the ventral striatum correlated negatively with the interaction partner’s ratings. Results of the study show that emotional alignment through the influence of another person’s communicated experience has to be considered as a complex phenomenon integrating different components including emotion anticipation and conformity.     

‘Ecstasy’ as a social drug: MDMA preferentially affects responses to emotional stimuli with social content

3,4-Methylenedioxymethamphetamine (MDMA, ‘ecstasy’) is used recreationally to improve mood and sociability, and has generated clinical interest as a possible adjunct to psychotherapy. One way that MDMA may produce positive ‘prosocial’ effects is by changing responses to emotional stimuli, especially stimuli with social content. Here, we examined for the first time how MDMA affects subjective responses to positive, negative and neutral emotional pictures with and without social content. We hypothesized that MDMA would dose-dependently increase reactivity to positive emotional stimuli and dampen reactivity to negative stimuli, and that these effects would be most pronounced for pictures with people in them. The data were obtained from two studies using similar designs with healthy occasional MDMA users (total N = 101). During each session, participants received MDMA (0, 0.75 and 1.5 mg/kg oral), and then rated their positive and negative responses to standardized positive, negative and neutral pictures with and without social content. MDMA increased positive ratings of positive social pictures, but reduced positive ratings of non-social positive pictures. We speculate this ‘socially selective’ effect contributes to the prosocial effects of MDMA by increasing the comparative value of social contact and closeness with others. This effect may also contribute to its attractiveness to recreational users.     

The influence of self-awareness on emotional memory formation: an fMRI study

Evidence from functional neuroimaging studies of emotional perception shows that when attention is focused on external features of emotional stimuli (external perceptual orienting—EPO), the amygdala is primarily engaged, but when attention is turned inwards towards one’s own emotional state (interoceptive self-orienting—ISO), regions of the salience network, such as the anterior insula (AI) and the dorsal anterior cingulate cortex (dACC), also play a major role. Yet, it is unknown if ISO boosts the contributions of AI and dACC not only to emotional ‘perception’ but also to emotional ‘memory’. To investigate this issue, participants were scanned with functional magnetic resonance imaging (fMRI) while viewing emotional and neutral pictures under ISO or EPO, and memory was tested several days later. The study yielded three main findings: (i) emotion boosted perception-related activity in the amygdala during both ISO and EPO and in the right AI exclusively during ISO; (ii) emotion augmented activity predicting subsequent memory in AI and dACC during ISO but not during EPO and (iii) high confidence memory was associated with increased amygdala–dACC connectivity, selectively for ISO encoding. These findings show, for the first time, that ISO promotes emotional memory formation via regions associated with interoceptive awareness of emotional experience, such as AI and dACC.     

Evidence for an emotion maintenance deficit in schizophrenia

Research has indicated that people with schizophrenia have deficits in reward representation and goal-directed behavior, which may be related to the maintenance of emotional experiences. Using a laboratory-based study, we investigated whether people with schizophrenia were able to maintain an emotional experience when given explicit instructions to do so. Twenty-eight people with schizophrenia and 19 people without completed a behavioral task judging their emotional experience of pictures held over a three second delay. This emotion maintenance task was compared to a subsequent in-the-moment emotion experience rating of each picture. In addition, all participants completed an analogous brightness experience maintenance and rating task, and patients completed a standardized visual working memory task. Participants with schizophrenia showed normal in-the-moment emotion experience of the emotion pictures; however, they showed decreased performance on emotion maintenance (for both positive and negative emotion) compared to participants without schizophrenia, even after controlling for brightness maintenance. The emotion maintenance deficit was not associated with visual brightness performance nor with performance on the visual working memory task; however, negative emotion maintenance was associated with an interview-based rating of motivation. These findings suggest that some aspects of impaired emotion maintenance in schizophrenia may be related to deficits in motivated behavior.     

Culture shapes electrocortical responses during emotion suppression

Previous work has shown that emotional control is highly valued in Asian culture. However, little is known about how this cultural value might influence emotional processing. Here, we hypothesized that Asians are ‘culturally trained’ to down-regulate emotional processing when required to suppress emotional expressions. Such down-regulation, however, is unlikely for European Americans because their culture values emotional expression (vs control) more. To test these predictions, we adopted the parietal late positive potential (LPP) of the event-related potential as an objective indicator of emotional processing. Both Asian and European Americans were exposed to either unpleasant or neutral pictures while instructed to either attend or suppress expression of emotions. Both groups showed an equally pronounced parietal positivity ∼600 ms post-stimulus. As predicted, however, Asians subsequently showed a significant decrease of the parietal LPP in the suppression (vs attend) condition. The initial positivity completely disappeared 2000 ms post-stimulus. In contrast, for European Americans the parietal LPP suppression effect was completely absent although there was an early occurring, sustained increase in frontal positivity in the suppression (vs attend) condition. Implications for culture and emotion research are discussed.     

ERP dynamics underlying successful directed forgetting of neutral but not negative pictures

Subjective experience suggests that negatively arousing memories are harder to control than neutral ones. Here, we investigate this issue in an item-cued directed forgetting experiment. Electroencephalogram event-related potentials (ERPs) were recorded as participants viewed un-arousing neutral and highly arousing negative photographs, each followed by a cue to remember or forget it. Directed forgetting, that is reduced recognition of ‘to-be-forgotten’ items, occurred for neutral but not negative pictures. ERPs revealed three underlying effects: first, during picture viewing a late parietal positive potential (LPP) was more pronounced for negative than for neutral pictures. Second, ‘remember’ cues were associated with larger LPPs than ‘forget’ cues. Third, an enhanced frontal positivity appeared for ‘forget’ cues. This frontal positivity was generated in right dorso-lateral prefrontal regions following neutral pictures and in medial frontal cortex following negative pictures. LPP magnitude when viewing negative pictures was correlated with reduced directed forgetting, whereas both the enhanced frontal positivity for forget cues and the larger parietal positivity for remember cues predicted more directed forgetting. This study indicates that both processes of selective rehearsal (parietal positivities) and frontally controlled inhibition contribute to successful directed forgetting. However, due to their deeper incidental processing, highly arousing negative pictures are exempt from directed forgetting.     

The neural correlates of trait resilience when anticipating and recovering from threat

A facet of emotional resilience critical for adapting to adversity is flexible use of emotional resources. We hypothesized that in threatening situations, this emotional flexibility enables resilient people to use emotional resources during appropriately emotional events, and conserve emotional resources during innocuous events. We tested this hypothesis using functional magnetic resonance imaging in a repeated recovery from threat task with low- and high-trait resilient individuals (LowR and HighR, respectively, as measured by ER89). In an event-related design, 13 HighR and 13 LowR participants viewed ‘threat’ cues, which signaled either an aversive or neutral picture with equal probabilities, or ‘nonthreat’ cues, which signaled a neutral picture. Results show that when under threat, LowR individuals exhibited prolonged activation in the anterior insula to both the aversive and neutral pictures, whereas HighR individuals exhibited insula activation only to the aversive pictures. These data provide neural evidence that in threatening situations, resilient people flexibly and appropriately adjust the level of emotional resources needed to meet the demands of the situation.     

Neural correlates of affective stimulus evaluation: a case-by-case analysis

A recent study provided first evidence that neural correlates of affective stimulus evaluation, that is, the early posterior negativity (EPN) and late positive potential (LPP), can be assessed at the individual case level. Expanding the case-by-case approach, the main aim of the present study was to explore the process of affective stimulus evaluation within the individual participant with respect to multiple emotional stimulus classes. Toward this end, each participant viewed separate blocks of low- and high-arousing pictures from behavior systems of predator fear, disease avoidance and sexual reproduction. Thirteen out of 16 participants showed larger EPN and LPP amplitudes for higher- than lower-arousing stimuli for all three behavior systems. Furthermore, rather than indicating a general lack of emotional modulation, cases of non-significant EPN (N = 3) and LPP (N = 2) tests in individual participants appeared to be specific to a single emotion category. Overall, assessing the emotional modulation of the EPN and LPP across multiple behavior systems strengthens the case-by-case approach regarding an effect that is ‘common to all’ as well as by differentiating non-significant effects within individuals in terms of a content-specific or general phenomenon. Implications for revealing a general principle of emotion functioning and biomarker development are discussed.     

Extended self: spontaneous activation of medial prefrontal cortex by objects that are ‘mine’

The concept of extended self refers to the idea that people incorporate self-relevant others or objects into one’s sense of self. Initial neural support for the notion of extended self was provided by fMRI evidence that medial prefrontal cortex (MPFC) showed greater activation while people imagined objects belonging to them compared with someone else (Kim & Johnson, 2012). This study investigated whether self-associated objects (i.e. ‘mine’) subsequently engage MPFC spontaneously when a task does not require explicit self-referential judgments. During fMRI scanning, participants detected ‘oddballs’ (objects with a specific frame color) intermixed with objects participants had previously imagined belonging to them or to someone else and previously unseen non-oddball objects. There was greater activity in MPFC and posterior cingulate cortex for those ‘self-owned’ objects that participants were more successful at imagining owning compared with ‘other-owned’ objects. In addition, change in object preference following the ownership manipulation (a mere ownership effect) was predicted by activity in MPFC. Overall, these results provide neural evidence for the idea that personally relevant external stimuli may be incorporated into one’s sense of self.     

Self-reference modulates the processing of emotional stimuli in the absence of explicit self-referential appraisal instructions

Self-referential evaluation of emotional stimuli has been shown to modify the way emotional stimuli are processed. This study aimed at a new approach by investigating whether self-reference alters emotion processing in the absence of explicit self-referential appraisal instructions. Event-related potentials were measured while subjects spontaneously viewed a series of emotional and neutral nouns. Nouns were preceded either by personal pronouns (‘my’) indicating self-reference or a definite article (‘the’) without self-reference. The early posterior negativity, a brain potential reflecting rapid attention capture by emotional stimuli was enhanced for unpleasant and pleasant nouns relative to neutral nouns irrespective of whether nouns were preceded by personal pronouns or articles. Later brain potentials such as the late positive potential were enhanced for unpleasant nouns only when preceded by personal pronouns. Unpleasant nouns were better remembered than pleasant or neutral nouns when paired with a personal pronoun. Correlation analysis showed that this bias in favor of self-related unpleasant concepts can be explained by participants’ depression scores. Our results demonstrate that self-reference acts as a first processing filter for emotional material to receive higher order processing after an initial rapid attention capture by emotional content has been completed. Mood-congruent processing may contribute to this effect.     

Oxytocin enhances pupil dilation and sensitivity to ‘hidden’ emotional expressions

Sensing others’ emotions through subtle facial expressions is a highly important social skill. We investigated the effects of intranasal oxytocin treatment on the evaluation of explicit and ‘hidden’ emotional expressions and related the results to individual differences in sensitivity to others’ subtle expressions of anger and happiness. Forty healthy volunteers participated in this double-blind, placebo-controlled crossover study, which shows that a single dose of intranasal oxytocin (40 IU) enhanced or ‘sharpened’ evaluative processing of others’ positive and negative facial expression for both explicit and hidden emotional information. Our results point to mechanisms that could underpin oxytocin’s prosocial effects in humans. Importantly, individual differences in baseline emotional sensitivity predicted oxytocin’s effects on the ability to sense differences between faces with hidden emotional information. Participants with low emotional sensitivity showed greater oxytocin-induced improvement. These participants also showed larger task-related pupil dilation, suggesting that they also allocated the most attentional resources to the task. Overall, oxytocin treatment enhanced stimulus-induced pupil dilation, consistent with oxytocin enhancement of attention towards socially relevant stimuli. Since pupil dilation can be associated with increased attractiveness and approach behaviour, this effect could also represent a mechanism by which oxytocin increases human affiliation.     

A selective role for right insula—basal ganglia circuits in appetitive stimulus processing

Hemispheric lateralization of hedonic evaluation (‘liking’) and incentive motivation (‘wanting’) in neural networks connecting the basal ganglia and insula (BG-I) in humans was examined. Participants with brain damage restricted to the BG-I of the right (n = 5) or left (n = 5) hemisphere, and 26 healthy participants matched on age, sex and intelligence quotient were tested on positively and negatively valenced pictures drawn from varied stimulus categories (Vijayaraghavan et al., 2008). Liking was assessed with explicit ratings of pleasantness using a nine-point Likert scale. Wanting was quantified as the amount of work (via repeated keypresses) that participants expended to increase (approach) or decrease (withdraw) viewing time. Right-lesion patients showed abnormally low viewing times and liking ratings for positive images. For a subset of positive images depicting sexual content, right-lesion patients exhibited active withdrawal, while the other two groups approached such stimuli. These results suggest that the right basal ganglia–insula complex plays a greater role than the left in supporting hedonic evaluation and motivational approach to positively valenced stimuli. The finding that active avoidance of stimuli that were not ‘liked’ was spared in both right- and left-sided lesion subjects suggests that unilateral damage to insula/basal ganglia circuits may not be sufficient to affect general incentive motivation independent of preference.     

Emotional Complexity and the Neural Representation of Emotion in Motion

According to theories of emotional complexity, individuals low in emotional complexity encode and represent emotions in visceral or action-oriented terms, whereas individuals high in emotional complexity encode and represent emotions in a differentiated way, using multiple emotion concepts. During functional magnetic resonance imaging, participants viewed valenced animated scenarios of simple ball-like figures attending either to social or spatial aspects of the interactions. Participant’s emotional complexity was assessed using the Levels of Emotional Awareness Scale. We found a distributed set of brain regions previously implicated in processing emotion from facial, vocal and bodily cues, in processing social intentions, and in emotional response, were sensitive to emotion conveyed by motion alone. Attention to social meaning amplified the influence of emotion in a subset of these regions. Critically, increased emotional complexity correlated with enhanced processing in a left temporal polar region implicated in detailed semantic knowledge; with a diminished effect of social attention; and with increased differentiation of brain activity between films of differing valence. Decreased emotional complexity was associated with increased activity in regions of pre-motor cortex. Thus, neural coding of emotion in semantic vs action systems varies as a function of emotional complexity, helping reconcile puzzling inconsistencies in neuropsychological investigations of emotion recognition.     

No fear,no panic: probing negation as a means for emotion regulation

This electroencephalographic study investigated if negating one’s emotion results in paradoxical effects or leads to effective emotional downregulation. Healthy participants were asked to downregulate their emotions to happy and fearful faces by using negated emotional cue words (e.g. no fun, no fear). Cue words were congruent with the emotion depicted in the face and presented prior to each face. Stimuli were presented in blocks of happy and fearful faces. Blocks of passive stimulus viewing served as control condition. Active regulation reduced amplitudes of early event-related brain potentials (early posterior negativity, but not N170) and the late positive potential for fearful faces. A fronto-central negativity peaking at about 250 ms after target face onset showed larger amplitude modulations during downregulation of fearful and happy faces. Behaviorally, negating was more associated with reappraisal than with suppression. Our results suggest that in an emotional context, negation processing could be quite effective for emotional downregulation but that its effects depend on the type of the negated emotion (pleasant vs unpleasant). Results are discussed in the context of dual process models of cognition and emotion regulation.     

Brain dynamics of visual attention during anticipation and encoding of threat- and safe-cues in spider-phobic individuals

This study systematically investigated the sensitivity of the phobic attention system by measuring event-related potentials (ERPs) in spider-phobic and non-phobic volunteers in a context where spider and neutral pictures were presented (phobic threat condition) and in contexts where no phobic but unpleasant and neutral or only neutral pictures were displayed (phobia-irrelevant conditions). In a between-group study, participants were assigned to phobia-irrelevant conditions either before or after the exposure to spider pictures (pre-exposure vs post-exposure participants). Additionally, each picture was preceded by a fixation cross presented in one of three different colors that were informative about the category of an upcoming picture. In the phobic threat condition, spider-phobic participants showed a larger P1 than controls for all pictures and signal cues. Moreover, individuals with spider phobia who were sensitized by the exposure to phobic stimuli (i.e. post-exposure participants) responded with an increased P1 also in phobia-irrelevant conditions. In contrast, no group differences between spider-phobic and non-phobic individuals were observed in the P1-amplitudes during viewing of phobia-irrelevant stimuli in the pre-exposure group. In addition, cues signaling neutral pictures elicited decreased stimulus-preceding negativity (SPN) compared with cues signaling emotional pictures. Moreover, emotional pictures and cues signaling emotional pictures evoked larger early posterior negativity (EPN) and late positive potential (LPP) than neutral stimuli. Spider phobics showed greater selective attention effects than controls for phobia-relevant pictures (increased EPN and LPP) and cues (increased LPP and SPN). Increased sensitization of the attention system observed in spider-phobic individuals might facilitate fear conditioning and promote generalization of fear playing an important role in the maintenance of anxiety disorders.     

Neurocognitive processing of infant stimuli in mothers and non-mothers: psychophysiological,cognitive and neuroimaging evidence

Emerging evidence indicates that mothers and non-mothers show different neurocognitive responses to infant stimuli. This study investigated mothers’ psychophysiological, cognitive and neuronal responses to emotional infant stimuli. A total of 35 mothers with 4-month-old infants and 18 control women without young children underwent computerized tests assessing neurocognitive processing of infant stimuli. Their eye gazes and eye fixations, galvanic skin responses (GSRs) and facial expressions towards infant emotional stimuli were recorded during the tasks. Participants underwent functional magnetic resonance imaging during which they viewed pictures of an unknown infant and, for mothers, their own infants. Mothers gazed more and had increased GSR towards infant stimuli and displayed more positive facial expressions to infant laughter, and self-reported more positive ratings of infant vocalizations than control women. At a neural level, mothers showed greater neural response in insula, dorsolateral prefrontal cortex and occipital brain regions within a predefined ‘maternal neural network’ while watching images of their own vs unknown infants. This specific neural response to own infants correlated with less negative ratings of own vs unknown infants’ signals of distress. Differences between mothers and control women without young children could be interpreted as neurocognitive adaptation to motherhood in the mothers.     

Opioid receptor blockade and warmth-liking: effects on interpersonal trust and frontal asymmetry

The emotion ‘warmth-liking’ (WL) associated with feelings of affection and acceptance is regularly activated in social contexts. WL has been suggested to be more closely related to the consummatory phase of post-goal attainment positive affect than to pre-goal attainment positive affect/approach motivation and to be partly mediated by brain opioids. To validate these assumptions we employed film/imagery to induce either a neutral emotional state or WL in female participants after intake of either placebo or the opioid antagonist naltrexone. Dependent variables were emotion self-report, interpersonal trust (TRUST, i.e. a behavioral indicator of WL) and frontal asymmetry (i.e. an electroencephalogram (EEG) indicator of approach motivation/behavioral activation). We found that participants reported more WL in the placebo/WL group than in the placebo/neutral group and both naltrexone groups. In addition, TRUST increased in the WL group after placebo, but not after naltrexone, and this pattern was reversed in the neutral control groups. Consequently, opioid blockade suppressed or even reversed the effects of the WL induction on the levels of self-report and behavior, respectively. In addition, we observed reduced relative left-frontal asymmetry in the WL (vs neutral) group, consistent with reduced approach motivation. Overall, these results suggest opioidergic influences on WL and TRUST and reduced approach motivation/behavioral activation for the positive emotion WL.