Humans daily face social situations involving conflicts between competing moral decision. Despite a substantial amount of studies published over the past 10 years, the respective role of emotions and reason, their possible interaction, and their behavioural expression during moral evaluation remains an unresolved issue. A dualistic approach to moral evaluation proposes that the right dorsolateral prefrontal cortex (rDLPFc) controls emotional impulses. However, recent findings raise the possibility that the right DLPFc processes emotional information during moral decision making. We used repetitive transcranial magnetic stimulation (rTMS) to transiently disrupt rDLPFc activity before measuring decision making in the context of moral dilemmas. Results reveal an increase of the probability of utilitarian responses during objective evaluation of moral dilemmas in the rTMS group (compared to a SHAM one). This suggests that the right DLPFc function not only participates to a rational cognitive control process, but also integrates emotions generated by contextual information appraisal, which are decisive for response selection in moral judgements.
moral judgement; rTMS; right prefrontal cortex; emotion; utilitarism; decision
Emotion regulation plays a crucial role in adaptive functioning and mounting evidence suggests that some emotion regulation strategies are often more effective than others. However, little attention has been paid to the different ways emotions can be generated: from the ‘bottom-up’ (in response to inherently emotional perceptual properties of the stimulus) or ‘top-down’ (in response to cognitive evaluations). Based on a process priming principle, we hypothesized that mode of emotion generation would interact with subsequent emotion regulation. Specifically, we predicted that top-down emotions would be more successfully regulated by a top-down regulation strategy than bottom-up emotions. To test this hypothesis, we induced bottom-up and top-down emotions, and asked participants to decrease the negative impact of these emotions using cognitive reappraisal. We observed the predicted interaction between generation and regulation in two measures of emotional responding. As measured by self-reported affect, cognitive reappraisal was more successful on top-down generated emotions than bottom-up generated emotions. Neurally, reappraisal of bottom-up generated emotions resulted in a paradoxical increase of amygdala activity. This interaction between mode of emotion generation and subsequent regulation should be taken into account when comparing of the efficacy of different types of emotion regulation, as well as when reappraisal is used to treat different types of clinical disorders.
emotion elicitation; emotion regulation; amygdale; reappraisal; face
Emotional processing is influenced by cognitive processes and vice versa, indicating a profound interaction of these domains. The investigation of the neural mechanisms underlying this interaction is not only highly relevant for understanding the organization of human brain function. Rather, it may also help in understanding dysregulated emotions in affective disorders and in elucidating the neurobiology of cognitive behavioural therapy (e.g. in borderline personality disorder), which aims at modulating dysfunctional emotion processes by cognitive techniques, such as restructuring. In the majority of earlier studies investigating the interaction of emotions and cognition, the main focus has been on the investigation of the effects of emotional stimuli or, more general, emotional processing, e.g. instituted by emotional material that needed to be processed, on cognitive performance and neural activation patterns. Here we pursued the opposite approach and investigated the modulation of implicit processing of emotional stimuli by cognitive demands using an event-related functional magnetic resonance imaging––study on a motor short-term memory paradigm with emotional interferences. Subjects were visually presented a finger-sequence consisting either of four (easy condition) or six (difficult condition) items, which they had to memorize. After a short pause positive, negative or neutral International affective picture system pictures or a green dot (as control condition) were presented. Subjects were instructed to reproduce the memorized sequence manually as soon as the picture disappeared. Analysis showed that with increasing cognitive demand (long relative to short sequences), neural responses to emotional pictures were significantly reduced in amygdala and orbitofrontal cortex. In contrast, the more difficult task evoked stronger activation in a widespread frontoparietal network. As stimuli were task-relevant go-cues and hence had to be processed perceptually, we would interpret this as a specific attenuation of affective responses by concurrent cognitive processing––potentially reflecting a relocation of resources mediated by the frontoparietal network.
neuroimaging; distraction; cognition; attention; valence
Learning to make choices that yield rewarding outcomes requires the computation of three distinct signals: stimulus values that are used to guide choices at the time of decision making, experienced utility signals that are used to evaluate the outcomes of those decisions and prediction errors that are used to update the values assigned to stimuli during reward learning. Here we investigated whether monetary and social rewards involve overlapping neural substrates during these computations. Subjects engaged in two probabilistic reward learning tasks that were identical except that rewards were either social (pictures of smiling or angry people) or monetary (gaining or losing money). We found substantial overlap between the two types of rewards for all components of the learning process: a common area of ventromedial prefrontal cortex (vmPFC) correlated with stimulus value at the time of choice and another common area of vmPFC correlated with reward magnitude and common areas in the striatum correlated with prediction errors. Taken together, the findings support the hypothesis that shared anatomical substrates are involved in the computation of both monetary and social rewards.
social reward; monetary reward; ventromedial prefrontal cortex; ventral striatum
The error-related negativity (ERN) is an event-related potential (ERP) that indexes error monitoring. Research suggests that the ERN is increased in internalizing disorders, such as depression and anxiety. Although studies indicate that the ERN is insensitive to state-related fluctuations in anxiety, few studies have carefully examined the effect of state-related changes in sadness on the ERN. In the current study, we sought to determine whether the ERN would be altered by a sad mood induction using a between-subjects design. Additionally, we explored if this relationship would be moderated by individual differences in neuroticism—a personality trait related to both anxiety and depression. Forty-seven undergraduate participants were randomly assigned to either a sad or neutral mood induction prior to performing an arrow version of the flanker task. Participants reported greater sadness following the sad than neutral mood induction; there were no significant group differences on behavioral or ERP measures. Across the entire sample, however, participants with a larger increase in sad mood from baseline to post-induction had a larger (i.e. more negative) ERN. Furthermore, this effect was larger among individuals reporting higher neuroticism. These data indicate that neuroticism moderates the relationship between the ERN and changes in sad mood.
event-related potential; error-related negativity; emotion; affect; sad mood induction
The present study investigates patterns of event-related brain potentials following the presentation of attitudinal stimuli among political moderates (N = 12) and anarchists (N = 11). We used a modified oddball paradigm to investigate the evaluative inconsistency effect elicited by stimuli embedded in a sequence of contextual stimuli with an opposite valence. Increased late positive potentials (LPPs) of extreme political attitudes were observed. Moreover, this LPP enhancement was larger among anarchists than among moderates, indicating that an extreme political attitude of a moderate differs from an extreme political attitude of an anarchist. The discussion elaborates on the meaning of attitude extremity for moderates and extremists.
brain; anarchism; ERP; extremism; ideology; political attitudes
Since people with low status are more likely to experience social evaluative threat and are therefore more inclined to monitor for these threats and inhibit approach behaviour, we expected that low-status subjects would be more engaged in evaluating their own performance, compared with high-status subjects. We created a highly salient social hierarchy based on the performance of a simple time estimation task. Subjects could achieve high, middle or low status while performing this task simultaneously with other two players who were either higher or lower in status. Subjects received feedback on their own performance, as well as on the performance of the other two players simultaneously. Electroencephalography (EEG) was recorded from all three participants. The results showed that medial frontal negativity (an event-related potential reflecting performance evaluation) was significantly enhanced for low-status subjects. Implications for status-related differences in goal-directed behaviour are discussed.
status; power; ERP; MFN; FRN; PCA
We tested the ability of white participants to encode and retain over a brief period of time information about the identity of white and black people, using faces as stimuli in a standard change detection task and tracking neural activity using electroencephalography. Neural responses recorded over the posterior parietal cortex reflecting visual working memory activity increased in amplitude as a function of the number of faces that had to be maintained in memory. Critically, these memory-related neural responses varied as a function of participants’ implicit racial prejudice toward black people. High-prejudiced participants encoded black people faces with a lower degree of precision compared to low-prejudiced participants, suggesting that the class of mental operations affected by implicit racial prejudice includes basic cognitive mechanisms underpinning the encoding and maintenance of faces’ visual representations in visual working memory.
implicit racial prejudice; visual working memory; electroencephalography; event-related potentials
The relationship between anger and aggression is imperfect. Based on work on the neuroscience of anger, we predicted that anger associated with greater relative left frontal cortical activation would be more likely to result in aggression. To test this hypothesis, we combined transcranial direct current stimulation (tDCS) over the frontal cortex with interpersonal provocation. Participants received insulting feedback after 15 min of tDCS and were able to aggress by administering noise blasts to the insulting participant. Individuals who received tDCS to increase relative left frontal cortical activity behaved more aggressively when they were angry. No relation between anger and aggression was observed in the increase relative right frontal cortical activity or sham condition. These results concur with the motivational direction model of frontal asymmetry, in which left frontal activity is associated with anger. We propose that anger with approach motivational tendencies is more likely to result in aggression.
Aggression; anger; frontal cortex; approach motivation; transcranial direct current stimulation
Among a range of cognitive functions of the amygdala, recent studies suggest its involvement in identification of the pupil size. To further address its role, we investigated the response of the amygdala to human and cat faces with varied pupil size, taking into account the effect of the gender and subjective attractiveness ratings. Twenty-seven subjects underwent functional magnetic resonance imaging while viewing faces with large and small pupils. Large pupil faces induced increased activation in the amygdala, without interactions with either subject or stimuli gender, although no equivalent activation differences were seen for cat face stimuli. The activation differences were irrespective of the perceived attractiveness, and without explicit knowledge about the manipulation of the pupil size. These data support the idea that the amygdala is responsive not only to explicit or implicit fear, abhorrence or preference, but also to other elements that might suggest heightened vigilance of biologically relevant stimuli, which does not necessarily require subjective awareness.
Amygdala; fMRI; pupil; biological relevance
Individuals with low self-esteem have been found to react more negatively to signs of interpersonal rejection than those with high self-esteem. However, previous research has found that individual differences in attentional control can attenuate negative reactions to social rejection among vulnerable, low self-esteem individuals. The current fMRI study sought to elucidate the neurobiological substrate of this buffering effect. We hypothesized and found that while looking at scenes of social rejection (vs negative scenes) low self-esteem high attentional control individuals engaged the rostral anterior cingulate cortex (rACC), an area of the brain associated with emotional control, more than their low self-esteem low attentional control peers. Furthermore, we found that low self-esteem high attentional control individuals evaluated social rejection as less arousing and less rejecting in a separate behavioral task. Importantly, activation in the rACC fully mediated the relationship between the interaction of self-esteem and attentional control and emotional evaluations, suggesting that the rACC activation underlies the buffering effects of attentional control. Results are discussed in terms of individual differences in emotional vulnerability and protection and by highlighting the role of rACC in emotion regulation.
attentional control; self-esteem; social rejection; rostral anterior cingulate cortex; emotion regulation
The current study takes a new approach to understand the neural systems that support emotion-congruent judgment. The bulk of previous neural research has inferred emotional influences on judgment from disadvantageous judgments or non-random individual differences. The current study manipulated the influence of emotional information on judgments of stimuli that were equivocally composed of positive and negative attributes. Emotion-congruent processing was operationalized in two ways: neural activation significantly associated with primes that lead to emotionally congruent judgments and neural activation significantly associated with judgments that were preceded by emotionally congruent primes. Distinct regions of medial orbitofrontal cortex were associated with these patterns of emotion-congruent processing. Judgments that were incongruent with preceding primes were associated with dorsomedial prefrontal cortex, ventrolateral prefrontal cortex and lateral orbitofrontal cortex activity. The current study demonstrates a new approach to investigate the neural systems associated with emotion-congruent judgment. The findings suggest that medial OFC may support attentional processes that underlie emotion-congruent judgment.
mood; affect; attention; orbitofrontal; fMRI
There are increasing reports of people experiencing pain when observing pain in another. This describes the phenomenon of synaesthetic pain which, until recently, had been primarily reported in amputees with phantom pain. In the current study, we used electroencephalography (EEG) to investigate how amputees who experience synaesthetic pain process pain observed in another. Participants were grouped according to amputees who experience phantom and synaesthetic pain (n = 8), amputees who experience phantom pain but not synaesthetic pain (n = 10) and healthy controls (n = 10). Participants underwent EEG as they observed still images of hands and feet in potentially painful and non-painful situations. We found that pain synaesthetes showed some reduced event-related potential (ERP) components at certain electrode sites, and reduced theta- and alpha band power amplitude at a central electrode. The finding of reduced ERP amplitude and theta band power may reflect inhibition of the processing of observed pain (e.g. avoidance/guarding as a protective strategy), and reduced alpha band power may indicate a disinhibition in control processes that may result in synaesthetic pain. These results provide the first documentation of atypical neurophysiological activity in amputees who experience synaesthetic pain when processing pain in another.
synaesthesia for pain; empathy for pain; phantom pain; electroencephalography
This study investigated depression-related differences in primiparous mothers’ neural response to their own infant’s distress cues. Mothers diagnosed with major depressive disorder (n = 11) and comparison mothers with no diagnosable psychopathology (n = 11) were exposed to their own 18-months-old infant’s cry sound, as well as unfamiliar infant’s cry and control sound, during functional neuroimaging. Depressed mothers’ response to own infant cry greater than other sounds was compared to non-depressed mothers’ response in the whole brain [false discovery rate (FDR) corrected]. A continuous measure of self-reported depressive symptoms (CESD) was also tested as a predictor of maternal response. Non-depressed mothers activated to their own infant’s cry greater than control sound in a distributed network of para/limbic and prefrontal regions, whereas depressed mothers as a group failed to show activation. Non-depressed compared to depressed mothers showed significantly greater striatal (caudate, nucleus accumbens) and medial thalamic activation. Additionally, mothers with lower depressive symptoms activated more strongly in left orbitofrontal, dorsal anterior cingulate and medial superior frontal regions. Non-depressed compared to depressed mothers activated uniquely to own infant greater than other infant cry in occipital fusiform areas. Disturbance of these neural networks involved in emotional response and regulation may help to explain parenting deficits in depressed mothers.
depression; fMRI; mother; infant; cry
The present study examined the neural correlates of long-term intense romantic love using functional magnetic resonance imaging (fMRI). Ten women and 7 men married an average of 21.4 years underwent fMRI while viewing facial images of their partner. Control images included a highly familiar acquaintance; a close, long-term friend; and a low-familiar person. Effects specific to the intensely loved, long-term partner were found in: (i) areas of the dopamine-rich reward and basal ganglia system, such as the ventral tegmental area (VTA) and dorsal striatum, consistent with results from early-stage romantic love studies; and (ii) several regions implicated in maternal attachment, such as the globus pallidus (GP), substantia nigra, Raphe nucleus, thalamus, insular cortex, anterior cingulate and posterior cingulate. Correlations of neural activity in regions of interest with widely used questionnaires showed: (i) VTA and caudate responses correlated with romantic love scores and inclusion of other in the self; (ii) GP responses correlated with friendship-based love scores; (iii) hypothalamus and posterior hippocampus responses correlated with sexual frequency; and (iv) caudate, septum/fornix, posterior cingulate and posterior hippocampus responses correlated with obsession. Overall, results suggest that for some individuals the reward-value associated with a long-term partner may be sustained, similar to new love, but also involves brain systems implicated in attachment and pair-bonding.
Although empathic responses to stimuli with emotional contents may occur automatically, humans are capable to intentionally empathize with other individuals. Intentional empathy for others is even possible when they do not show emotional expressions. However, little is known about the neuronal mechanisms of this intentionally controlled empathic process. To investigate the neuronal substrates underlying intentional empathy, we scanned 20 healthy Chinese subjects, using fMRI, when they tried to feel inside the emotional states of neutral or angry faces of familiar (Asian) and unfamiliar (Caucasian) models. Skin color evaluation of the same stimuli served as a control task. Compared to a baseline condition, the empathy task revealed a network of established empathy regions, including the anterior cingulate cortex, bilateral inferior frontal cortex and bilateral anterior insula. The contrast of intentional empathy vs skin color evaluation, however, revealed three regions: the bilateral inferior frontal cortex, whose hemodynamic responses were independent of perceived emotion and familiarity and the right-middle temporal gyrus, whose activity was modulated by emotion but not by familiarity. These findings extend our understanding of the role of the inferior frontal cortex and the middle temporal gyrus in empathy by demonstrating their involvement in intentional empathy.
fMRI; brain imaging; empathy
Social interaction deficits and restricted repetitive behaviors and interests that characterize autism spectrum disorders (ASDs) may both reflect aberrant functioning of brain reward circuits. However, no neuroimaging study to date has investigated the integrity of reward circuits using an incentive delay paradigm in individuals with ASDs. In the present study, we used functional magnetic resonance imaging to assess blood-oxygen level-dependent activation during reward anticipation and outcomes in 15 participants with an ASD and 16 matched control participants. Brain activation was assessed during anticipation of and in response to monetary incentives and object image incentives previously shown to be visually salient for individuals with ASDs (e.g. trains, electronics). Participants with ASDs showed decreased nucleus accumbens activation during monetary anticipation and outcomes, but not during object anticipation or outcomes. Group × reward-type-interaction tests revealed robust interaction effects in bilateral nucleus accumbens during reward anticipation and in ventromedial prefrontal cortex during reward outcomes, indicating differential responses contingent on reward type in these regions. Results suggest that ASDs are characterized by reward-circuitry hypoactivation in response to monetary incentives but not in response to autism-relevant object images. The clinical implications of the double dissociation of reward type and temporal phase in reward circuitry function in ASD are discussed.
autism; reward; nucleus accumbens; anticipation; functional magnetic resonance imaging
The idea of ‘extended self’ refers to the incorporation of personally relevant external stimuli into one’s concept of self. The current study used a transient imagined ownership paradigm to explore brain regions that support the association between self and objects. We hypothesized that incidental associations between self and objects would be manifested by activation in a brain region, medial prefrontal cortex (MPFC), recruited in explicit self-referential processing. We further predicted that a memorial advantage for, and positivity-bias towards, self-relevant objects would be related to activity in MPFC. As anticipated, MPFC showed greater activation when objects were assigned to participants compared to when objects were assigned to another person. Activity in MPFC was also associated with superior subsequent source memory and increased preference for objects assigned to the self. These findings provide neural evidence for the incorporation of self-relevant objects into an extended self, which, in turn, increases their judged value (mere ownership effect).
extended self; ownership; self-referential processing; medial prefrontal cortex; fMRI
This study investigated whether human chemosensory-stress cues affect neural activity related to the evaluation of emotional stimuli. Chemosensory stimuli were obtained from the sweat of 64 male donors during both stress (first-time skydive) and control (exercise) conditions, indistinguishable by odor. We then recorded event-related potentials (ERPs) from an unrelated group of 14 participants while they viewed faces morphed with neutral-to-angry expressions and inhaled nebulized stress and exercise sweat in counter-balanced blocks, blind to condition. Results for the control condition ERPs were consistent with previous findings: the late positive potential (LPP; 400–600 ms post stimulus) in response to faces was larger for threatening than both neutral and ambiguous faces. In contrast, the stress condition was associated with a heightened LPP across all facial expressions; relative to control, the LPP was increased for both ambiguous and neutral faces in the stress condition. These results suggest that stress sweat may impact electrocortical activity associated with attention to salient environmental cues, potentially increasing attentiveness to otherwise inconspicuous stimuli.
emotion; attention; event-related potential; late positive potential; pheromones
Gender-based stereotypes undermine females’ performance on challenging math tests, but how do they influence their ability to learn from the errors they make? Females under stereotype threat or non-threat were presented with accuracy feedback after each problem on a GRE-like math test, followed by an optional interactive tutorial that provided step-wise problem-solving instruction. Event-related potentials tracked the initial detection of the negative feedback following errors [feedback related negativity (FRN), P3a], as well as any subsequent sustained attention/arousal to that information [late positive potential (LPP)]. Learning was defined as success in applying tutorial information to correction of initial test errors on a surprise retest 24-h later. Under non-threat conditions, emotional responses to negative feedback did not curtail exploration of the tutor, and the amount of tutor exploration predicted learning success. In the stereotype threat condition, however, greater initial salience of the failure (FRN) predicted less exploration of the tutor, and sustained attention to the negative feedback (LPP) predicted poor learning from what was explored. Thus, under stereotype threat, emotional responses to negative feedback predicted both disengagement from learning and interference with learning attempts. We discuss the importance of emotion regulation in successful rebound from failure for stigmatized groups in stereotype-salient environments.
LPP; FRN; ERP; math; emotion regulation; memory
The amygdala is critically involved in mediating physiological and behavioral responses to threat. In particular, neuroimaging research indicates that the amygdala is highly responsive to facial signals of threat such as fearful and angry expressions. However, individuals differ substantially in both their relative sensitivity to threat and the magnitude of amygdala reactivity to facial signals of threat. Here, we report the novel finding that individual differences in trait anger are positively correlated with bilateral dorsal amygdala reactivity to angry facial expressions, but only among men with elevated trait anxiety scores. These findings add to the growing body of evidence indicating that variability in personality traits contribute to individual differences in threat-related amygdala reactivity and further suggest that heightened amygdala reactivity to angry faces may be uniquely involved in the expression of reactive aggression in men.
amygdala; threat; trait anger; trait anxiety; reactive aggression; brain imaging
When you see someone reach into a cookie jar, their goal remains obvious even if you know that the last cookie has already been eaten. Thus, it is possible to infer the goal of an action even if you know that the goal cannot be achieved. Previous research has identified distinct brain networks for processing information about object locations, actions and mental-state inferences. However, the relationship between brain networks for action understanding in social contexts remains unclear. Using functional magnetic resonance imaging, this study assesses the role of these networks in understanding another person searching for hidden objects. Participants watched movie clips depicting a toy animal hiding and an actor, who was ignorant of the hiding place, searching in the filled or empty location. When the toy animal hid in the same location repeatedly, the blood oxygen level-dependent (BOLD) response was suppressed in occipital, posterior temporal and posterior parietal brain regions, consistent with processing object properties and spatial attention. When the actor searched in the same location repeatedly, the BOLD signal was suppressed in the inferior frontal gyrus, consistent with the observation of hand actions. In contrast, searches towards the filled location compared to the empty location were associated with a greater response in the medial prefrontal cortex and right temporal pole, which are both associated with mental state inference. These findings show that when observing another person search for a hidden object, brain networks for processing information about object properties, actions and mental state inferences work together in a complementary fashion. This supports the hypothesis that brain regions within and beyond the putative human mirror neuron system are involved in action comprehension within social contexts.
mentalizing; mirror neuron system; action observation; social cognition; fMRI
A considerable body of evidence derived from terror management theory indicates that the awareness of mortality represents a potent psychological threat engendering various forms of psychological defense. However, extant research has yet to examine the neurological correlates of cognitions about one’s inevitable death. The present study thus investigated in 17 male participants patterns of neural activation elicited by mortality threat. To induce mortality threat, participants answered questions arranged in trial blocks that referred to fear of death and dying. In the control condition participants answered questions about fear of dental pain. Neural responses to mortality threat were greater than to pain threat in right amygdala, left rostral anterior cingulate cortex, and right caudate nucleus. We discuss implications of these findings for stimulating further research into the neurological correlates of managing existential fear.
brain; defense mechanism; fear of death; fMRI; mortality salience; terror management theory
Social bonds fulfill the basic human need to belong. Being rejected thwarts this basic need, putting bonds with others at risk. Attachment theory suggests that people satisfy their need to belong through different means. Whereas anxious attachment is associated with craving acceptance and showing vigilance to cues that signal possible rejection, avoidant attachment is associated with discomfort with closeness and using avoidant strategies to regulate one’s relationships. Given these different styles by which people satisfy their need to belong (that can operate simultaneously within the same individual), responses to social rejection may differ according to these individual differences in attachment anxiety and avoidance. To test this hypothesis, we used neuroimaging techniques to examine how the degree to which people display each of the two attachment dimensions (anxiety and avoidance) uniquely correlated with their neural activity during a simulated experience of social exclusion. Anxious attachment related to heightened activity in the dorsal anterior cingulate cortex (dACC) and anterior insula, regions previously associated with rejection-related distress. In contrast, avoidant attachment related to less activity in these regions. Findings are discussed in terms of the strategies that individuals with varying attachment styles might use to promote maintenance of social bonds.
Social rejection; attachment style; fMRI; social neuroscience; social exclusion
Our recent work showed that close relationships result in shared cognitive and neural representations of the self and one’s mother in collectivistic individuals (Zhu et al., 2007, Neuroimage, 34, 1310–7). However, it remains unknown whether close others, such as mother, father and best friend, are differentially represented in collectivistic brains. Here, using functional magnetic resonance imaging and a trait judgment task, we showed evidence that, while trait judgments of the self and mother generated comparable activity in the medial prefrontal cortex (MPFC) and anterior cingulate (ACC) of Chinese adults, trait judgments of mother induced greater MPFC/ACC activity than trait judgments of father and best friend. Our results suggest that, while neural representations of the self and mother overlapped in the MPFC/ACC, close others such as mother, father and best friend are unequally represented in the MPFC/ACC of collectivistic brains.
close other; self; medial prefrontal cortex; anterior cingulate; fMRI