Revealed masks: Facial mimicry after oxytocin administration in forensic psychopathic patients.

Facial mimicry serves as an evolutionarily rooted important interpersonal communication process that touches on the concepts of socialization and empathy. Facial electromyography (EMG) of the corrugator muscle and the zygomaticus muscle was recorded while male forensic psychopathic patients and controls watched morphed angry or happy facial expressions. We tested the hypothesis that psychopathic patients would show weaker short latency facial mimicry (that is, within 600 ms after stimulus onset) than controls. Exclusively in the group of 20 psychopathic patients, we tested in a placebo-controlled crossover within-subject design the hypothesis that oxytocin would enhance short-latency facial mimicry. Compared with placebo, we found no oxytocin-related significant short-latency responses of the corrugator and the zygomaticus. However, compared with 19 normal controls, psychopathic patients in the placebo condition showed significantly weaker short-latency zygomaticus responses to happy faces, while there was a trend toward significantly weaker short-latency corrugator responses to angry faces. These results are consistent with a recent study of facial EMG responses in adolescents with psychopathic traits. We therefore posit a lifetime developmental deficit in psychopathy pertaining short-latency mimicry of emotional facial expressions. Ultimately, this deficit in mimicking angry and happy expressions may hinder the elicitation of empathy, which is known to be impaired in psychopathy.

Facing infant cuteness: How nurturing care motivation and oxytocin system gene methylation are associated with responses to baby schema features.

Baby schema features are a specific set of physical features-including chubby cheeks, large, low-set eyes, and a large, round head-that have evolutionary adaptive value in their ability to trigger nurturant care. In this study among nulliparous women (N = 81; M age = 23.60, SD = 0.44), we examined how sensitivity to these baby schema features differs based on individual variations in nurturant care motivation and oxytocin system gene methylation. We integrated subjective ratings with measures of facial expressions and electroencephalography (EEG) in response to infant faces that were manipulated to contain more or less pronounced baby schema features. Linear mixed effects analyses demonstrated that infants with more pronounced baby schema features were rated as cuter and participants indicated greater motivation to take care of them. Furthermore, infants with more pronounced baby schema features elicited stronger smiling responses and enhanced P2 and LPP amplitudes compared to infants with less pronounced baby schema features. Importantly, individual differences significantly predicted baby schema effects. Specifically, women with low OXTR methylation and high nurturance motivation showed enhanced differentiation in automatic neurophysiological responses to infants with high and low levels of baby schema features. These findings highlight the importance of considering individual differences in continued research to further understand the complexities of sensitivity to child cues, including facial features, which will improve our understanding of the intricate neurobiological system that forms the basis of caregiving behavior.

Reciprocal self-disclosure makes children feel more loved by their parents in the moment: A proof-of-concept experiment.

Feeling loved by one's parents is critical for children's health and well-being. How can such feelings be fostered? A vital feature of loving interactions is reciprocal self-disclosure, where individuals disclose intimate information about themselves. In a proof-of-concept experiment, we examined whether encouraging reciprocal self-disclosure in parent-child dyads would make children feel more loved during the conversation. Participants were 218 children (ages 8-13, 50% girls, 94% Dutch) and one of their parents (ages 28-56, 62% women, 90% Dutch). Parent-child dyads received a list of 14 questions and took turns asking them each other for 9 min. Dyads were assigned randomly to engage in self-disclosure (questions invoking escalated intimacy) or small talk (questions invoking minimal intimacy). Before and after, children reported how loved they felt by their parent during the conversation. Self-disclosure made children feel more loved during the conversation than did small talk. Compared to small talk, self-disclosure did not instigate conversations that were lengthier or more positive; rather, it instigated conversations that were more emotionally charged (reflecting anger, anxiety, and sadness), social (discussing family and friends), reflective (creating insight), and meaningful (addressing deeply personal topics, including the passing of loved ones). The dyad's gender composition did not significantly moderate these effects. Our research suggests that reciprocal self-disclosure can make children feel more loved in the moment, uncovers linguistic signatures of reciprocal self-disclosure, and offers developmental scientists a tool to examine causal effects of reciprocal self-disclosure in parent-child dyads. Future work should examine long-term effects in everyday parent-child interactions. RESEARCH HIGHLIGHTS: How can parents make children feel more loved by them in the moment? We theorize that these feelings can be cultivated through reciprocal self-disclosure. In a proof-of-concept experiment, we examined effects of reciprocal self-disclosure versus small talk in 218 parent-child dyads, with children aged 8-13. Self-disclosure (vs. small talk) made children feel more loved during the conversation. Linguistically, self-disclosure instigated conversations that were more emotionally charged, social, reflective, and meaningful. This research provides an experimental method to study self-disclosure in parent-child dyads and suggests that self-disclosure can make children feel more loved in the moment.

Preliminary data on oxytocin modulation of neural reactivity in women to emotional stimuli of children depending on childhood emotional neglect.

Sensitivity for rewarding cues and distress signals from children is fundamental to human caregiving and modulated by the neuropeptide oxytocin. In a functional magnetic resonance imaging study, we investigated whether oxytocin regulates neural responses to reward or distress cues form children. In a placebo-controlled, within-subject design, we measured neural responses to positive, negative, and neutral cues from children in 22 healthy female subjects who received oxytocin (24 IU) versus placebo. Further, based on current literature, we hypothesized that oxytocin effects are modulated by experiences of childhood trauma. The task elicited valence-specific effects-positive images activated the ventromedial prefrontal cortex, left anterior cingulate cortex, and right putamen, and images of children in distress activated the bilateral amygdala, hippocampus, and right medial superior frontal cortex. The effects of oxytocin depended on subjective reports of childhood emotional neglect. Self-reported neglect interacted with oxytocin administration in the amygdala, hippocampus, and prefrontal areas. In individuals with higher scores of emotional neglect, oxytocin increased neural reactivity of limbic structures to positive and neutral images. Our findings need replication in larger samples and can therefore be considered preliminary but are in line with the recent literature on the modulating effect of childhood adversity on the sensitivity to oxytocin administration.

Oxytocin system gene methylation is associated with empathic responses towards children.

Empathy is an essential component of sensitive caregiving behavior, which in turn is an important predictor of children's healthy social-emotional development. The oxytocin (OXT) system plays a key role in promoting sensitive parenting and empathy. In this study, we investigated how OXT system gene methylation was associated with empathic processes in nulliparous women (M age = 23.60, SD =0.44)-measuring both physiological facial muscle responses and ratings of compassion and positive affect to affective images depicting children. Linear mixed effects analyses demonstrated that lower methylation levels in the OXT and OXTR genes were related to enhanced empathic responses. The effect of OXT system gene methylation on empathic processes was partly qualified by an interaction with individual variations in women's care motivation. Our findings provide experimental evidence for an association between the methylation of OXT system genes and empathy.

Unzipping empathy in psychopathy: Empathy and facial affect processing in psychopaths.

Psychopathy is a neurodevelopmental disorder that has a highly deleterious effect upon both individuals and society at large. Psychopaths grossly neglect and disrespect the interests of others. Their antisocial behavior is thought to originate from a lack of empathy. However, empathy is multidimensional in nature, as evidenced by the considerable heterogeneity in extant theorizing on the subject. Here, we present the "Zipper model of empathy" that reconsiders how both its affective and cognitive components converge in mature empathic behavior. Furthermore, the Zipper model of empathy is expedient for explaining the empathy deficits in psychopathy, insofar as it brings together current theories on the dysfunctional affective components of empathy, violence inhibition, and automatic versus goal-directed attention. According to the literature, the neurobiological underpinnings of these theories are amygdala-centered; however, this article traces this specifically to the basolateral and central amygdala subregions. When viewed together, the cognitive and affective components of empathy are zipped together in a natural fashion in healthy empathic behavior, whereas psychopaths leave the zipper substantially unzipped in pursuit of their purely self-centered goals.

Preliminary data on increased reactivity towards children in distress after testosterone administration in women: A matter of protection?

Emotional reactivity to others' distress is a vital prerequisite for a caring response. Testosterone, in contrast, is mostly associated with protection of personal dominance and decreased responsiveness to others' needs. However, experimental work also indicates that rising testosterone levels in response to infant distress can potentially facilitate protection. We assessed the impact of testosterone administration on participants' emotional reactivity to infants in distress, measuring their facial responses on the corrugator supercilii forehead muscle ('frowning') and the zygomaticus major ('smiling') as an index of emotional responses towards children. Moreover, we probed whether the effect of testosterone is moderated by participants' self-reported nurturance and protective tendencies. Our preliminary results showed that testosterone not only increased emotional reactivity to empathy eliciting images of children, but that this increase was strongest in participants with strong protective tendencies. Our administration study is the first to link testosterone to infant protection.

A mu-opioid feedback model of human social behavior.

Since the discovery of pain relieving and rewarding properties of opiates such as morphine or heroin, the human mu-opioid system has been a target for medical research on pain processing and addiction. Indeed, pain and pleasure act mutually inhibitory on each other and the mu-opioid system has been suggested as an underlying common neurobiological mechanism. Recently, research interest extended the role of the endogenous mu-opioid system beyond the hedonic value of pain and pleasure towards human social-emotional behavior. Here we propose a mu-opioid feedback model of social behavior. This model is based upon recent findings of opioid modulation of human social learning, bonding and empathy in relation to affiliative and protective tendencies. Fundamental to the model is that the mu-opioid system reinforces socially affiliative or protective behavior in response to positive and negative social experiences with long-term consequences for social behavior and health. The functional implications for stress, anxiety, depression and attachment behaviors are discussed.

Climbing up or falling down: Narcissism predicts physiological sensitivity to social status in children and their parents.

Children's narcissism may be rooted in sensitivity to social status (i.e., prominence, respect, and influence in a social group), and this sensitivity might be shared with parents. Testing this idea, a randomized experiment examined how children with high narcissism levels and their parents respond to gains and losses of social status. On a simulated social media platform, children (N = 123, ages 8-13) competed with fictitious peers for status and were randomly assigned to gain or lose status. Unbeknownst to children, parents viewed the course of the task. Children's and parents' affective reactions during the task were measured with facial electromyography, which detects spontaneous facial muscle activity linked to positive affect (i.e., zygomaticus major activity, involved in smiling) and negative affect (i.e., corrugator supercilii activity, involved in frowning). Children with higher narcissism levels showed steeper increases in negative affect during status loss and steeper increases in both positive and negative affect during status gain. Their parents mirrored the steeper increase in positive affect during their child's status gain, but they did not mirror the increase in negative affect. These results suggest that children with high narcissism levels and their parents show intensified affective-motivational responses to children's status-relevant experiences. These responses may be transmitted from one generation to the other (e.g., genetically or through parent-child socialization).

Methylation of oxytocin related genes and early life trauma together shape the N170 response to human faces.

Childhood trauma fundamentally shapes social cognition and basic processing of social cues, which frequently cascade into adverse behavioral outcomes. Recent studies indicate that epigenetic changes in oxytocin functioning might contribute to these long-term effects, although a deeper understanding of the underlying mechanisms is still lacking. The electroencephalographic N170 response to faces might capture a neural response at the core of these interactive effects of oxytocin gene methylation and childhood adversity, given that this response is considered to reflect fundamental face processing, to be susceptible to oxytocin administration and also to be a biomarker of various psychiatric disorders. We assessed the N170 response to neutral faces in relation to participant's (81, women) recalled childhood trauma, methylation of their oxytocin structural (OXTg) and oxytocin receptor (OXTRg) genes, and endogenous levels of cortisol and testosterone. Additionally, we investigated the interactive effect of OXTg methylation and CTQ across three face sets of varying maturity. Methylation of OXTg relates to a weakened N170 response towards adults, children and infants. Moreover, methylation of both OXTRg and OXTg shaped the directionality of adversity effects, predicting a weakened N170 response in those with high methylation and hyper-vigilance with participants with low methylation. Our results are the first to relate OXT(R)g methylation to the N170 response. They shed light on biological processes linking childhood adversity and epigenetic marks to altered behavior and potentially psychopathologies.

Neural correlates of self- and other-referential processing in young adolescents and the effects of testosterone and peer similarity.

During adolescence, self-concept develops profoundly, accompanied by major changes in hormone levels. Self-evaluations become more complex, and peers and their opinions increasingly salient. Neuroimaging studies have investigated self- and other-related processing in adolescents, however, the influence of similarity of peers on these processes is still unclear, as well as functional connectivity underlying such processes. We investigated the effect of peer similarity on neural activity and connectivity underlying self- and other-referential processing, by distinguishing between a similar and dissimilar peer when making other-evaluations. Moreover, we explored the association between testosterone and brain activity during self-evaluations. Sixty-six young adolescents underwent functional MRI while performing a trait judgement task in which they indicated whether an adjective described themselves, a similar or a dissimilar classmate. The ventral medial prefrontal cortex (MPFC) showed increased engagement in self-referential processing, and the posterior cingulate cortex and right temporal parietal junction during other-evaluations. However, activity did not differ between the similar and dissimilar other conditions. Functional connectivity of the ventral MPFC included the striatum when evaluating the similar peer and frontoparietal regions when evaluating the dissimilar peer. Furthermore, inter-individual differences in testosterone levels were positively associated with dorsal MPFC activity in males. This study provides insight into the influence of peer similarity on activity and connectivity underlying other-referential processing in young adolescents, and suggests that testosterone affects neural correlates of self-referential processing.

Pictures of preterm infants elicit increased affective responses and reduced reward-motivation or perspective taking in the maternal brain.

Preterm-birth increases the risk of several physical, cognitive, neuromotor, and psychosocial problems in children, and is also related to difficulties in the parent-child relationship. Research suggests that the development of early parent-child interactions in general is affected by deviations from typical infant facial characteristics, which may also be important in the case of small, preterm born infants. Therefore, we examined mothers' (N = 22, of whom 17 had no direct experience with preterm birth) neural responses to pictures of preterm and full-term infants using functional magnetic resonance imaging (fMRI). We also explored whether neural responses to preterm and full-term infants correlated with mothers' self-reported tendencies to be nurturing and protective with children, and with mothers' ratings of affection or aversion toward pictures of preterm infants. Results revealed that, compared to pictures of full-term infants, those of preterm infants elicited more activity in specific areas of the brain (dmPFC, right insula, left caudate, hippocampi, parahippocampi, and PAG), that have previously been associated with processing of negative emotions and with empathy. In addition, less activity was seen in one area of the brain (vmPFC) known to be associated with reward-motivation or mental state understanding and perspective-taking. Higher self-reported maternal nurturance was associated with increased activity to pictures of preterm infants vs full-term infants in the caudate, which might reflect approach- or reward-related processing. To conclude, neural responses to preterm infants are related to reward-motivation, mentalizing, negative emotions, and empathy. Future studies should examine whether such neural processing of preterm infant stimuli might underlie difficulties in the parent-child relationship of parents with a preterm child.

What a cute baby! Preliminary evidence from a fMRI study for the association between mothers' neural responses to infant faces and activation of the parental care system.

Infant facial characteristics, i.e., baby schema, are thought to automatically elicit parenting behavior and affective orientation toward infants. Only a few studies, conducted in non-parents, have directly examined the neural underpinnings of this baby schema effect by manipulating distinctiveness of baby schema in infant faces. This study aims to further our understanding of the intuitive nature of parenting, by studying the baby schema effect in mothers of young children (at least one child aged between 2 and 6 years old). Functional magnetic resonance imaging (fMRI) was used to examine mothers' (N = 23) neural responses to unfamiliar infant faces varying in distinctiveness of baby schema. Also, it was studied how this neural activation to infant faces was associated with maternal nurturance. Results revealed that infant faces elicited widespread activation in bilateral visual cortices, the hippocampus, sensory-motor areas, parietal and frontal cortices, and the insula, which was not modulated by the distinctiveness of baby schema in the infant faces. Furthermore, higher self-reported maternal nurturance was related to increased neural responses to infant faces in the putamen and amygdala, brain regions known to be associated with reward and salience processing. These findings could suggest that in our small sample of mothers some of the core networks involved in reward and salience processing might be less sensitive to variation in distinctiveness of baby schema. Also, unfamiliar infant faces seem to be rewarding only for mothers who report high nurturance. These findings should be considered preliminary, because they need to be replicated in studies with larger samples.

Neural responses in the pain matrix when observing pain of others are unaffected by testosterone administration in women.

There is evidence of testosterone having deteriorating effects on cognitive and affective empathic behaviour in men and women under varying conditions. However, whether testosterone influences empathy for pain has not yet been investigated. Therefore, we tested neural responses to witnessing others in pain in a within-subject placebo-controlled testosterone administration study in healthy young women. Using functional magnetic resonance imaging, we provide affirming evidence that an empathy-inducing paradigm causes changes in the activity throughout the pain circuitry, including the bilateral insula and anterior cingulate cortex. Administration of testosterone, however, did not influence these activation patterns in the pain matrix. Testosterone has thus downregulating effects on aspects of empathic behaviour, but based on these data does not seem to influence neural responses during empathy for others' pain. This finding gives more insight into the role of testosterone in human empathy.

Boys' toys, girls' toys: An fMRI study of mothers' neural responses to children violating gender expectations.

This study examined 1) mothers' neural responses to pictures of boys and girls who confirmed or violated social expectations regarding toy preferences, and 2) whether neural sensitivity to targets that violated gendered expectations interacted with mothers' gender stereotypes. In an event-related fMRI experiment, 23 mothers of a 2-6 year-old child viewed and evaluated pictures of boys or girls with their favorite toy. Next, mothers gender stereotypes about children's toys and behavior, and internal motivation to behave without prejudice were assessed. Several neural processes were underlying parents' responses to children's behavior that violates gender-role expectations. Brain regions involved in mentalizing or storage of social knowledge, understanding goal-directed behavior, behavioral control, and conflict monitoring were activated when viewing child targets that violated gender expectations. In these brain areas, increased neural responses to targets that violated traditional gender expectations were associated with more stereotyped expectations about boys' and girls' toys and behavior.

Neural processing of gendered information is more robustly associated with mothers' gendered communication with children than mothers' implicit and explicit gender stereotypes.

Processes like gender socialization (the ways in which parents convey information to their children about how girls and boys should behave) often happen unconsciously and might therefore be studied best with neuroscientific measures. We examined whether neural processing of gender-stereotype-congruent and incongruent information is more robustly related to mothers' gendered socialization of their child than mothers' implicit and explicit gender stereotypes. To this end, we examined event-related potentials (ERPs) of mothers (N = 35) completing an implicit gender-stereotype task and mothers' gender stereotypes in relation to observed gendered communication with their child (2-6 years old) in a naturalistic picture-book-reading setting. Increased N2 activity (previously related to attentional processes) to gender stimuli in the implicit gender-stereotype task was associated with mothers' positive evaluation of similar gendered behaviors and activities in the picture book they read with their child. Increased P300 activity (previously related to attention to unexpected events) to incongruent trials in the gender-stereotype task was associated with a more positive evaluation of congruent versus incongruent pictures. Compared to mothers' gender stereotypes, neural processing of gendered information was more robustly related to how mothers talk to their children about boys' and girls' stereotype-congruent and incongruent behavior, and masculine and feminine activities.

Parental touch reduces social vigilance in children.

The sense of touch develops in utero and enables parent-child communication from the earliest moments of life. Research shows that parental touch (e.g., licking and grooming in rats, skin-to-skin care in humans) has organizing effects on the offspring's stress system. Little is known, however, about the psychological effects of parental touch. Building on findings from ethology and psychology, we propose that parental touch-even as subtle as a touch on the shoulder-tells children that their environment is safe for exploration, thus reducing their social vigilance. We tested this hypothesis in late childhood (ages 8-10) and early adolescence (ages 11-14) in 138 parent-child dyads. Parents were randomly assigned to touch or not touch their child briefly and gently on the shoulder, right below the deltoid. Parental touch lowered children's implicit attention to social threat. While parental touch lowered trust among socially non-anxious children, it raised trust among those who needed it the most: socially anxious children. The effects were observed only in late childhood, suggesting that parental touch loses its safety-signaling meaning upon the transition to adolescence. Our findings underscore the power of parental touch in childhood, especially for children who suffer from social anxiety.

Epigenetic variability in the human oxytocin receptor (OXTR) gene: A possible pathway from early life experiences to psychopathologies.

The human oxytocin (OXT) system is implicated in the regulation of complex social behaviors, as well as in psychopathologies characterized by social deficits. Emerging evidence suggests that variation in epigenetic regulation of the oxytocin receptor gene (OXTR) provides the oxytocin system with flexibility in response to environmental events, especially those occurring during early childhood. Changes in DNA methylation patterns of OXTR associated with these events may reflect biological alterations of social sensitivity. This is often related to an increased risk of developing mental disorders later in life. Here, we systematically reviewed all human studies (n = 30) discussing OXTR methylation in relation to socio-behavioral phenotypes. As such, we provide a complete and up-to-date overview of the literature that will aid future research in the interdisciplinary field of epigenetics and socio-behavioral sciences.

The Basolateral Amygdala Is Essential for Rapid Escape: A Human and Rodent Study.

Rodent research delineates how the basolateral amygdala (BLA) and central amygdala (CeA) control defensive behaviors, but translation of these findings to humans is needed. Here, we compare humans with natural-selective bilateral BLA lesions to rats with a chemogenetically silenced BLA. We find, across species, an essential role for the BLA in the selection of active escape over passive freezing during exposure to imminent yet escapable threat (Timm). In response to Timm, BLA-damaged humans showed increased startle potentiation and BLA-silenced rats demonstrated increased startle potentiation, freezing, and reduced escape behavior as compared to controls. Neuroimaging in humans suggested that the BLA reduces passive defensive responses by inhibiting the brainstem via the CeA. Indeed, Timm conditioning potentiated BLA projections onto an inhibitory CeA pathway, and pharmacological activation of this pathway rescued deficient Timm responses in BLA-silenced rats. Our data reveal how the BLA, via the CeA, adaptively regulates escape behavior from imminent threat and that this mechanism is evolutionary conserved across rodents and humans.

Oxytocin reduces neural activation in response to infant faces in nulliparous young women.

Infant faces have distinctive features that together are described as baby schema, a configuration that facilitates caregiving motivation and behavior, and increases the perception of cuteness. In the current functional magnetic resonance imaging (fMRI) study, we investigated the effect of a within-subjects intranasal oxytocin administration (24 IU) and caregiving motivation on neural responses to infant faces of varying baby schema in 23 healthy nulliparous women. Overall, infant faces elicited activation in several brain regions involved in reward and salience processing, including the ventral tegmental area (VTA), putamen, amygdala, anterior cingulate cortex (ACC), and insula, and this activation was related to self-reported caregiving motivation. Critically, whereas we hypothesized enhanced neural caregiving-related responses after oxytocin administration, we observed reduced activation in the VTA, putamen and amygdala after oxytocin compared to placebo. In nulliparous women, oxytocin has been shown to reduce neural responses in the same regions in response to social stimuli using other paradigms. Oxytocin might affect neural activation toward social stimuli depending on elicited arousal and personal characteristics. The current study is the first to demonstrate this effect in response to infant faces and thereby adds to specify the role of oxytocin in human social information processing.