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1.  Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation 
Humans observe various peoples’ social suffering throughout their lives, but it is unknown whether the same brain mechanisms respond to people we are close to and strangers’ social suffering. To address this question, we had participant’s complete functional magnetic resonance imaging (fMRI) while observing a friend and stranger experience social exclusion. Observing a friend’s exclusion activated affective pain regions associated with the direct (i.e. firsthand) experience of exclusion [dorsal anterior cingulate cortex (dACC) and insula], and this activation correlated with self-reported self-other overlap with the friend. Alternatively, observing a stranger’s exclusion activated regions associated with thinking about the traits, mental states and intentions of others [‘mentalizing’; dorsal medial prefrontal cortex (DMPFC), precuneus, and temporal pole]. Comparing activation from observing friend’s vs stranger’s exclusion showed increased activation in brain regions associated with the firsthand experience of exclusion (dACC and anterior insula) and with thinking about the self [medial prefrontal cortex (MPFC)]. Finally, functional connectivity analyses demonstrated that MPFC and affective pain regions activated in concert during empathy for friends, but not strangers. These results suggest empathy for friends’ social suffering relies on emotion sharing and self-processing mechanisms, whereas empathy for strangers’ social suffering may rely more heavily on mentalizing systems.
doi:10.1093/scan/nss019
PMCID: PMC3624958  PMID: 22355182
empathy; social pain; anterior cingulate cortex; medial prefrontal cortex
2.  Who Is Most Vulnerable to Social Rejection? The Toxic Combination of Low Self-Esteem and Lack of Negative Emotion Differentiation on Neural Responses to Rejection 
PLoS ONE  2014;9(3):e90651.
People have a fundamental need to belong that, when satisfied, is associated with mental and physical well-being. The current investigation examined what happens when the need to belong is thwarted—and how individual differences in self-esteem and emotion differentiation modulate neural responses to social rejection. We hypothesized that low self-esteem would predict heightened activation in distress-related neural responses during a social rejection manipulation, but that this relationship would be moderated by negative emotion differentiation—defined as adeptness at using discrete negative emotion categories to capture one's felt experience. Combining daily diary and neuroimaging methodologies, the current study showed that low self-esteem and low negative emotion differentiation represented a toxic combination that was associated with stronger activation during social rejection (versus social inclusion) in the dorsal anterior cingulate cortex and anterior insula—two regions previously shown to index social distress. In contrast, individuals with greater negative emotion differentiation did not show stronger activation in these regions, regardless of their level of self-esteem; fitting with prior evidence that negative emotion differentiation confers equanimity in emotionally upsetting situations.
doi:10.1371/journal.pone.0090651
PMCID: PMC3942456  PMID: 24594689
3.  Entering Adolescence: Resistance to Peer Influence, Risky Behavior, and Neural Changes in Emotion Reactivity 
Neuron  2011;69(5):10.1016/j.neuron.2011.02.019.
SUMMARY
Adolescence is often described as a period of heightened reactivity to emotions paired with reduced regulatory capacities, a combination suggested to contribute to risk-taking and susceptibility to peer influence during puberty. However, no longitudinal research has definitively linked these behavioral changes to underlying neural development. Here, 38 neurotypical participants underwent two fMRI sessions across the transition from late childhood (10 years) to early adolescence (13 years). Responses to affective facial displays exhibited a combination of general and emotion-specific changes in ventral striatum (VS), ventromedial PFC, amygdala, and temporal pole. Furthermore, VS activity increases correlated with decreases in susceptibility to peer influence and risky behavior. VS and amygdala responses were also significantly more negatively coupled in early adolescence than in late childhood while processing sad and happy versus neutral faces. Together, these results suggest that VS responses to viewing emotions may play a regulatory role that is critical to adolescent interpersonal functioning.
doi:10.1016/j.neuron.2011.02.019
PMCID: PMC3840168  PMID: 21382560
4.  Longitudinal change in the neural bases of adolescent social self-evaluations: Effects of age and pubertal development 
Self-evaluations undergo significant transformation during early adolescence, developing in parallel with the heightened complexity of teenagers’ social worlds. Intuitive theories of adolescent development, based in part on animal work, suggest that puberty is associated with neural-level changes that facilitate a “social reorientation” (Nelson, Leibenluft, McClure, and Pine, 2005). However, direct tests of this hypothesis using neuroimaging are limited in humans. This longitudinal fMRI study examined neurodevelopmental trajectories associated with puberty, self-evaluations, and the presumed social reorientation during the transition from childhood to adolescence. Participants (N = 27, M age = 10.1 and 13.1 years at timepoints one and two, respectively) engaged in trait evaluations of two targets (the self and a familiar fictional other), across two domains of competence (social and academic). Responses in ventromedial PFC increased with both age and pubertal development during self-evaluations in the social domain, but not in the academic domain. These results suggest changes in social self-evaluations are intimately connected with biology, not just peer contexts, and provide important empirical support for the relationship between neurodevelopment, puberty, and social functioning.
doi:10.1523/JNEUROSCI.4074-12.2013
PMCID: PMC3809090  PMID: 23616547
5.  Time spent with friends in adolescence relates to less neural sensitivity to later peer rejection 
Involvement with friends carries many advantages for adolescents, including protection from the detrimental effects of being rejected by peers. However, little is known about the mechanisms through which friendships may serve their protective role at this age, or the potential benefit of these friendships as adolescents transition to adulthood. As such, this investigation tested whether friend involvement during adolescence related to less neural sensitivity to social threats during young adulthood. Twenty-one adolescents reported the amount of time they spent with friends outside of school using a daily diary. Two years later they underwent an fMRI scan, during which they were ostensibly excluded from an online ball-tossing game by two same-age peers. Findings from region of interest and whole brain analyses revealed that spending more time with friends during adolescence related to less activity in the dorsal anterior cingulate cortex and anterior insula—regions previously linked with negative affect and pain processing—during an experience of peer rejection 2 years later. These findings are consistent with the notion that positive relationships during adolescence may relate to individuals being less sensitive to negative social experiences later on.
doi:10.1093/scan/nsq098
PMCID: PMC3252626  PMID: 21183457
adolescence; friendship; peer rejection; functional magnetic resonance imaging
6.  Do neural responses to rejection depend on attachment style? An fMRI study 
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.
doi:10.1093/scan/nsq107
PMCID: PMC3277372  PMID: 21467049
Social rejection; attachment style; fMRI; social neuroscience; social exclusion
7.  Facing puberty: associations between pubertal development and neural responses to affective facial displays 
Adolescence is marked by profound psychosocial and physiological changes. Although investigations into the interactions between these forces have begun to shed light on the neural correlates of affective processing during the transition to adolescence, relatively little is known about the relationship between pubertal development and emotion perception at the neural level. In the current longitudinal study, 45 neurotypical participants were shown affective facial displays while undergoing fMRI, at ages 10 and 13. Neural responses to emotional expressions at both time points were then correlated with a self-report measure of pubertal development, revealing positive associations with activity in amygdala, thalamus and visual cortical areas at age 10 that increased in magnitude and extent by age 13. At the latter time point, pubertal development was additionally correlated with enhanced responses to faces in temporal pole, ventrolateral prefrontal cortex (PFC) and dorsomedial PFC. Longitudinal comparisons revealed that the relationships between pubertal development and activity in the amygdala, hippocampus and temporal pole were significantly stronger during early adolescence than late childhood. These results suggest that pubertal development per se is linked to neural processing of socioemotional stimuli, particularly with respect to the integration of complex perceptual input and higher order cortical processing of affective content.
doi:10.1093/scan/nsr066
PMCID: PMC3252633  PMID: 22228752
adolescence; puberty; emotion; fMRI; amygdala; longitudinal
8.  Witnessing peer rejection during early adolescence: Neural correlates of empathy for experiences of social exclusion 
Social neuroscience  2010;5(5-6):496-507.
Neuroimaging studies with adults have begun to reveal the neural bases of empathy; however, this research has focused on empathy for physical pain, rather than empathy for negative social experiences. Moreover, this work has not examined adolescents who may frequently witness and empathize with others who experience negative social experiences like peer rejection. Here, we examined neural activity among early adolescents observing social exclusion compared to observing inclusion, and how this activity related to both trait empathy and subsequent prosocial behavior. Participants were scanned while they observed an individual whom they believed was being socially excluded. At least one day prior to the scan they reported their trait empathy, and following the scan they wrote emails to the excluded victim that were rated for prosocial behavior (e.g., helping, comforting). Observing exclusion compared to inclusion activated regions involved in mentalizing (i.e., dorsomedial prefrontal cortex; DMPFC), particularly among highly empathic individuals. Additionally, individuals who displayed more activity in affective, pain-related regions during observed exclusion compared to inclusion subsequently wrote more prosocial emails to excluded victims. Overall findings suggest that when early adolescents witness social exclusion in their daily lives, some may actually ‘feel the pain’ of the victims and act more prosocially toward them as a result.
doi:10.1080/17470919.2010.490673
PMCID: PMC2957502  PMID: 20602283
adolescence; empathy; peer rejection; social exclusion; functional magnetic resonance imaging
9.  Neural regions associated with self control and mentalizing are recruited during prosocial behaviors towards the family☆ 
Neuroimage  2011;58(1):242-249.
Prosocial decisions can be difficult because they often involve personal sacrifices that do not generate any direct, immediate benefits to the self. The current study used functional magnetic resonance imaging (fMRI) to understand how individuals decide to provide support to others. Twenty-five participants were scanned as they completed a task in which they made costly decisions to contribute money to their family and noncostly decisions to accept personal monetary rewards. Decisions to contribute to the family recruited brain regions involved in self-control and mentalizing, especially for individuals with stronger family obligation preferences. Psychophysiological interaction (PPI) analyses revealed that individuals with stronger family obligation preferences showed greater functional coupling between regions involved in self-control and mentalizing with the ventral striatum, a region involved in reward processing. These findings suggest that prosocial behavior may require both social cognition and deliberate effort, and the application of these processes may result in greater positive reinforcement during prosocial behavior.
doi:10.1016/j.neuroimage.2011.06.013
PMCID: PMC3276247  PMID: 21703352
10.  An fMRI investigation of responses to peer rejection in adolescents with autism spectrum disorders 
Peer rejection is particularly pervasive among adolescents with autism spectrum disorders (ASD). However, how adolescents with ASD differ from typically developing adolescents in their responses to peer rejection is poorly understood. The goal of the current investigation was to examine neural responses to peer exclusion among adolescents with ASD compared to typically developing adolescents. Nineteen adolescents with ASD and 17 typically developing controls underwent fMRI as they were ostensibly excluded by peers during an online game called Cyberball. Afterwards, participants reported their distress about the exclusion. Compared to typically developing adolescents, those with ASD displayed less activity in regions previously linked with the distressing aspect of peer exclusion, including the subgenual anterior cingulate and anterior insula, as well as less activity in regions previously linked with the regulation of distress responses during peer exclusion, including the ventrolateral prefrontal cortex and ventral striatum. Interestingly, however, both groups self-reported equivalent levels of distress. This suggests that adolescents with ASD may engage in differential processing of social experiences at the neural level, but be equally aware of, and concerned about, peer rejection. Overall, these findings contribute new insights about how this population may differentially experience negative social events in their daily lives.
doi:10.1016/j.dcn.2011.01.004
PMCID: PMC3272329  PMID: 22318914
Autism spectrum disorders; Peer rejection; Social exclusion; Adolescence; Functional magnetic resonance imaging
11.  Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection 
Developmental research has demonstrated the harmful effects of peer rejection during adolescence; however, the neural mechanisms responsible for this salience remain unexplored. In this study, 23 adolescents were excluded during a ball-tossing game in which they believed they were playing with two other adolescents during an fMRI scan; in reality, participants played with a preset computer program. Afterwards, participants reported their exclusion-related distress and rejection sensitivity, and parents reported participants’ interpersonal competence. Similar to findings in adults, during social exclusion adolescents displayed insular activity that was positively related to self-reported distress, and right ventrolateral prefrontal activity that was negatively related to self-reported distress. Findings unique to adolescents indicated that activity in the subgenual anterior cingulate cortex (subACC) related to greater distress, and that activity in the ventral striatum related to less distress and appeared to play a role in regulating activity in the subACC and other regions involved in emotional distress. Finally, adolescents with higher rejection sensitivity and interpersonal competence scores displayed greater neural evidence of emotional distress, and adolescents with higher interpersonal competence scores also displayed greater neural evidence of regulation, perhaps suggesting that adolescents who are vigilant regarding peer acceptance may be most sensitive to rejection experiences.
doi:10.1093/scan/nsp007
PMCID: PMC2686232  PMID: 19470528
peer rejection; adolescence; functional magnetic resonance imaging
12.  Gaining while giving: An fMRI study of the rewards of family assistance among White and Latino youth 
Social neuroscience  2010;5(5-6):508-518.
Family assistance is an important aspect of family relationships for adolescents across many cultures and contexts. Motivations to help family members may be driven by both cultural factors and early family experiences. Here, we used functional magnetic resonance imaging to examine (1) cultural differences in neural reward activity among White and Latino youth during online experiences of family assistance and (2) how prior family experiences related to neural reward activity when helping the family. Participants were scanned as they made decisions to contribute money to their family and themselves. Latino and White participants showed similar behavioral levels of helping but distinct patterns of neural activity within the mesolimbic reward system. Whereas Latino participants showed more reward activity when contributing to their family, White participants showed more reward activity when gaining cash for themselves. In addition, participants who felt more identified with their family and who derived greater fulfillment from helping their family two years prior to the scan showed increased reward system activation when contributing to their family. These results suggest that family assistance may be guided, in part, by the personal rewards one attains from that assistance, and that this sense of reward may be modulated by cultural influences and prior family experiences.
doi:10.1080/17470911003687913
PMCID: PMC3079017  PMID: 20401808
Family assistance; Culture; fMRI; Reward; Social identity
13.  EFFECTS OF YOHIMBINE AND HYDROCORTISONE ON PANIC SYMPTOMS, AUTONOMIC RESPONSES AND ATTENTION TO THREAT IN HEALTHY ADULTS 
Psychopharmacology  2009;204(3):445-455.
Rationale
Research in rodents and non-human primates implicates the noradrenergic system and hypothalamic-pituitary-adrenal axis in stress, anxiety, and attention to threat. Few studies examine how these two neurochemical systems interact to influence anxiety and attention in humans.
Objective
To examine the effects of exogenous yohimbine and hydrocortisone, as well as their combination (Y+H) on panic symptoms and attention to social threat cues.
Methods
32 healthy adults underwent a pharmacological challenge in which they were blindly randomized to either: yohimbine, hydrocortisone, Y+H, or placebo. Thirty minutes after drug infusion, attention to threat was measured using the dot probe task, a visual attention task that presents angry, happy and neutral faces and measures the degree of attention allocated towards or away from the emotional faces. Panic and autonomic measures were assessed before and 30 minutes after drug infusion.
Results
There was a significant increase in panic symptoms in the yohimbine and Y+H groups but not in the hydrocortisone or placebo groups. Yohimbine resulted in a greater increase in panic symptoms than Y+H. On the dot probe task, the placebo group exhibited an attention bias to angry faces whereas this bias was absent after yohimbine. When collapsing across groups, increased panic symptoms was associated with less attention to angry faces.
Conclusions
Exogenous hydrocortisone may attenuate noradrenergic-induced panic symptoms. The inverse relationship between panic symptoms and attention to angry faces extends prior research demonstrating attention modulation by stressful conditions.
doi:10.1007/s00213-009-1475-x
PMCID: PMC2740930  PMID: 19266185
yohimbine; hydrocortisone; panic symptoms; attention; threat cues; adults
14.  Recognition of facial emotions among maltreated children with high rates of post-traumatic stress disorder 
Child abuse & neglect  2007;32(1):139-153.
Objective
The purpose of this study is to examine processing of facial emotions in a sample of maltreated children showing high rates of post-traumatic stress disorder (PTSD). Maltreatment during childhood has been associated independently with both atypical processing of emotion and the development of PTSD. However, research has provided little evidence indicating how high rates of PTSD might relate to maltreated children’s processing of emotions.
Method
Participants’ reaction time and labeling of emotions were measured using a morphed facial emotion identification task. Participants included a diverse sample of maltreated children with and without PTSD and controls ranging in age from 8 to 15 years. Maltreated children had been removed from their homes and placed in state custody following experiences of maltreatment. Diagnoses of PTSD and other disorders were determined through combination of parent, child, and teacher reports.
Results
Maltreated children displayed faster reaction times than controls when labeling emotional facial expressions, and this result was most pronounced for fearful faces. Relative to children who were not maltreated, maltreated children both with and without PTSD showed enhanced response times when identifying fearful faces. There was no group difference in labeling of emotions when identifying different facial emotions.
Conclusions
Maltreated children show heightened ability to identify fearful faces, evidenced by faster reaction times relative to controls. This association between maltreatment and atypical processing of emotion is independent of PTSD diagnosis.
doi:10.1016/j.chiabu.2007.09.006
PMCID: PMC2268025  PMID: 18155144
Maltreatment; Emotional processing; PTSD; Children

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