Stability and change: Stress responses and the shaping of behavioral phenotypes over the life span

In mammals, maternal signals conveyed via influences on hypothalamic-pituitary-adrenal (HPA) activity may shape behavior of the young to be better adapted for prevailing environmental conditions. However, the mother's influence extends beyond classic stress response systems. In guinea pigs, several hours (h) of separation from the mother activates not only the HPA axis, but also the innate immune system, which effects immediate behavioral change, as well as modifies behavioral responsiveness in the future. Moreover, the presence of the mother potently suppresses the behavioral consequences of this innate immune activation. These findings raise the possibility that long-term adaptive behavioral change can be mediated by the mother's influence on immune-related activity of her pups. Furthermore, the impact of social partners on physiological stress responses and their behavioral outcomes are not limited to the infantile period. A particularly crucial period for social development in male guinea pigs is that surrounding the attainment of sexual maturation. At this time, social interactions with adults can dramatically affect circulating cortisol concentrations and social behavior in ways that appear to prepare the male to best cope in its likely future social environment. Despite such multiple social influences on the behavior of guinea pigs at different ages, inter-individual differences in the magnitude of the cortisol response remain surprisingly stable over most of the life span. Together, it appears that throughout the life span, physiological stress responses may be regulated by social stimuli. These influences are hypothesized to adjust behavior for predicted environmental conditions. In addition, stable individual differences might provide a means of facilitating adaptation to less predictable conditions.     

Culture Shapes Efficiency of Facial Age Judgments

Background

Cultural differences in socialization can lead to characteristic differences in how we perceive the world. Consistent with this influence of differential experience, our perception of faces (e.g., preference, recognition ability) is shaped by our previous experience with different groups of individuals.

Methodology/Principal Findings

Here, we examined whether cultural differences in social practices influence our perception of faces. Japanese, Chinese, and Asian-Canadian young adults made relative age judgments (i.e., which of these two faces is older?) for East Asian faces. Cross-cultural differences in the emphasis on respect for older individuals was reflected in participants'' latency in facial age judgments for middle-age adult faces—with the Japanese young adults performing the fastest, followed by the Chinese, then the Asian-Canadians. In addition, consistent with the differential behavioural and linguistic markers used in the Japanese culture when interacting with individuals younger than oneself, only the Japanese young adults showed an advantage in judging the relative age of children''s faces.

Conclusions/Significance

Our results show that different sociocultural practices shape our efficiency in processing facial age information. The impact of culture may potentially calibrate other aspects of face processing.     

Follow my eyes: the gaze of politicians reflexively captures the gaze of ingroup voters

Studies in human and non-human primates indicate that basic socio-cognitive operations are inherently linked to the power of gaze in capturing reflexively the attention of an observer. Although monkey studies indicate that the automatic tendency to follow the gaze of a conspecific is modulated by the leader-follower social status, evidence for such effects in humans is meager. Here, we used a gaze following paradigm where the directional gaze of right- or left-wing Italian political characters could influence the oculomotor behavior of ingroup or outgroup voters. We show that the gaze of Berlusconi, the right-wing leader currently dominating the Italian political landscape, potentiates and inhibits gaze following behavior in ingroup and outgroup voters, respectively. Importantly, the higher the perceived similarity in personality traits between voters and Berlusconi, the stronger the gaze interference effect. Thus, higher-order social variables such as political leadership and affiliation prepotently affect reflexive shifts of attention.     

Reactions to Ingroup and Outgroup Deviants: An Experimental Group Paradigm for Black Sheep Effect

In the classic black sheep effect (BSE) an ingroup deviant member is usually evaluated more negatively than the corresponding outgroup deviant. This effect is usually obtained by using scenarios and asking people to imagine the situation as vividly as possible. The present study proposes a new method to investigate the BSE by considering the behavioral and physiological reactions to unfair behavior (aggressive game behavior) in a realistic experimental group-setting. The study involved 52 university students in a minimal group setting who performed a modified version of the competitive reaction time (CRT) task adapted to be played in groups of four people. The classic BSE was replicated for evaluation but not for the behavioral reactions (retaliate to aggression) to deviants. More interestingly, a negative relationship emerged in the ingroup deviant condition between the level of behavioral derogation and the systolic blood pressure level.     

Human Infant Faces Provoke Implicit Positive Affective Responses in Parents and Non-Parents Alike

Human infants'' complete dependence on adult caregiving suggests that mechanisms associated with adult responsiveness to infant cues might be deeply embedded in the brain. Behavioural and neuroimaging research has produced converging evidence for adults'' positive disposition to infant cues, but these studies have not investigated directly the valence of adults'' reactions, how they are moderated by biological and social factors, and if they relate to child caregiving. This study examines implicit affective responses of 90 adults toward faces of human and non-human (cats and dogs) infants and adults. Implicit reactions were assessed with Single Category Implicit Association Tests, and reports of childrearing behaviours were assessed by the Parental Style Questionnaire. The results showed that human infant faces represent highly biologically relevant stimuli that capture attention and are implicitly associated with positive emotions. This reaction holds independent of gender and parenthood status and is associated with ideal parenting behaviors.     

Behavioral Immune System and Ingroup Derogation: The Effects of Infectious Diseases on Ingroup Derogation Attitudes

From evolutionary reasoning, we derived a novel hypothesis that ingroup derogation is an evolved response of behavioral immune system which follows the smoke detector principle and the functional flexibility principle. This hypothesis was tested and supported across three experiments. In Experiment 1, participants’ group membership was manipulated by using a minimal group paradigm. The results indicated that mere social categorization alone — a heuristic cue that implies the differentiation between "us" and "them" — was sufficient to elicit ingroup derogation among Chinese participants, and, such an intergroup bias was positively associated with the perceived vulnerability to diseases, which was also more consistently associated with ingroup attitudes. Experiment 2 extended and partially replicated Experiment 1 by showing that when there were cues of diseases in the immediate physical environment, Chinese participants exaggerated their attitudes of ingroup derogation. The results also showed that this effect was mainly driven by outgroup attraction. Experiment 3 changed the method of disease manipulation, and found that Chinese participants responded more strongly to disease cues originating from ingroup members and that they endorsed more ingroup derogation attitudes even when the ingroup and outgroup members were both displaying cues of diseases. Taken together, these results reveal the previously unexplored effects of infectious diseases on ingroup derogation attitudes, and suggest an interesting linkage between the evolved behavioral immune system and the ingroup derogation.     

Intergroup bias in third-party punishment stems from both ingroup favoritism and outgroup discrimination

Social norms pervade almost every aspect of social interaction. If they are violated, not only legal institutions, but other members of society as well, punish, i.e., inflict costs on the wrongdoer. Sanctioning occurs even when the punishers themselves were not harmed directly and even when it is costly for them. There is evidence for intergroup bias in this third-party punishment: third-parties, who share group membership with victims, punish outgroup perpetrators more harshly than ingroup perpetrators. However, it is unknown whether a discriminatory treatment of outgroup perpetrators (outgroup discrimination) or a preferential treatment of ingroup perpetrators (ingroup favoritism) drives this bias. To answer this question, the punishment of outgroup and ingroup perpetrators must be compared to a baseline, i.e., unaffiliated perpetrators. By applying a costly punishment game, we found stronger punishment of outgroup versus unaffiliated perpetrators and weaker punishment of ingroup versus unaffiliated perpetrators. This demonstrates that both ingroup favoritism and outgroup discrimination drive intergroup bias in third-party punishment of perpetrators that belong to distinct social groups.     

Does Competition Really Bring Out the Worst? Testosterone,Social Distance and Inter-Male Competition Shape Parochial Altruism in Human Males

Parochial altruism, defined as increased ingroup favoritism and heightened outgroup hostility, is a widespread feature of human societies that affects altruistic cooperation and punishment behavior, particularly in intergroup conflicts. Humans tend to protect fellow group members and fight against outsiders, even at substantial costs for themselves. Testosterone modulates responses to competition and social threat, but its exact role in the context of parochial altruism remains controversial. Here, we investigated how testosterone influences altruistic punishment tendencies in the presence of an intergroup competition. Fifty male soccer fans played an ultimatum game (UG), in which they faced anonymous proposers that could either be a fan of the same soccer team (ingroup) or were fans of other teams (outgroups) that differed in the degree of social distance and enmity to the ingroup. The UG was played in two contexts with varying degrees of intergroup rivalry. Our data show that unfair offers were rejected more frequently than fair proposals and the frequency of altruistic punishment increased with increasing social distance to the outgroups. Adding an intergroup competition led to a further escalation of outgroup hostility and reduced punishment of unfair ingroup members. High testosterone levels were associated with a relatively increased ingroup favoritism and also a change towards enhanced outgroup hostility in the intergroup competition. High testosterone concentrations further predicted increased proposer generosity in interactions with the ingroup. Altogether, a significant relation between testosterone and parochial altruism could be demonstrated, but only in the presence of an intergroup competition. In human males, testosterone may promote group coherence in the face of external threat, even against the urge to selfishly maximize personal reward. In that way, our observation refutes the view that testosterone generally promotes antisocial behaviors and aggressive responses, but underlines its rather specific role in the fine-tuning of male social cognition.     

The Impact of Hispanic and White Group Cues on Attitudes Towards the Violation of Generic Norms

While much work in political science has examined the impact of racial cues on individual perceptions, we know little about how individuals evaluate members of minority outgroups on issues that are not linked to stereotypes. We measure the impacts of Hispanic and White cues on individual assessments related to a stereotype-independent norm violation: alcoholism. We test three competing theories – cognition, intergroup emotions, and social identity – using a population-based vignette experiment included in the General Social Survey. Our results contradict much of the literature, but keep with social identity theory''s predictions. Hispanic alcoholics, when Hispanics constitute the outgroup, are assessed less negatively than White alcoholics in the ingroup, the latter experiencing what is called the black sheep effect. The black sheep effect occurs when ingroup members are more punitive towards members of the ingroup than the outgroup. However, the black sheep effect does not extend to measures that are more consistent with outgroup stereotypes, such as violence or money mismanagement; Hispanic alcoholics are evaluated more negatively than Whites on these measures. The implication is that the effect of racial cues depends strongly on issue linkages to group stereotypes.     

Children aged 7–9 prefer cuteness in baby faces,and femininity in women's faces

Infant facial features are typically perceived as “cute,” provoking caretaking behaviours. Previous research has focused on adults' perceptions of baby cuteness, and examined how these perceptions are influenced by events of the adult reproductive lifespan, such as ovulation and menopause. However, globally, individuals of all ages, including pre-pubertal children, provide notable proportions of infant care. In this study, we recruited participants in and around northern England, and tested 330 adults and 65 children aged 7–9 using a forced-choice paradigm to assess preferences for infant facial cuteness in two stimulus sets and (as a control task) preferences for femininity in women's faces. We analysed the data with Hierarchical Bayesian Regression Models. The adults and children successfully identified infants who had been manipulated to appear cuter, although children's performance was poorer than adults' performance, and children reliably identified infant cuteness in only one of the two infant stimuli sets. Children chose the feminised over masculinised women's faces as more attractive, although again their performance was poorer than adults' performance. There was evidence for a female advantage in the tasks: girls performed better than boys when assessing the woman stimuli and one of the infant stimulus sets, and women performed better than men when assessing one of the infant stimulus sets. There was no evidence that cuteness judgements differed depending upon exposure to infants (children with siblings aged 0–2; adults with a baby caregiving role), or depending upon being just younger or older than the average age of menopause. Children and grandparents provide notable portions of infant caretaking globally, and cuteness perceptions could direct appropriate caregiving behaviour in these age groups, as well as in adults of reproductive age.     

Attention to Eye Contact in the West and East: Autonomic Responses and Evaluative Ratings

Eye contact has a fundamental role in human social interaction. The special appearance of the human eye (i.e., white sclera contrasted with a coloured iris) implies the importance of detecting another person''s face through eye contact. Empirical studies have demonstrated that faces making eye contact are detected quickly and processed preferentially (i.e., the eye contact effect). Such sensitivity to eye contact seems to be innate and universal among humans; however, several studies suggest that cultural norms affect eye contact behaviours. For example, Japanese individuals exhibit less eye contact than do individuals from Western European or North American cultures. However, how culture modulates eye contact behaviour is unclear. The present study investigated cultural differences in autonomic correlates of attentional orienting (i.e., heart rate) and looking time. Additionally, we examined evaluative ratings of eye contact with another real person, displaying an emotionally neutral expression, between participants from Western European (Finnish) and East Asian (Japanese) cultures. Our results showed that eye contact elicited stronger heart rate deceleration responses (i.e., attentional orienting), shorter looking times, and higher ratings of subjective feelings of arousal as compared to averted gaze in both cultures. Instead, cultural differences in the eye contact effect were observed in various evaluative responses regarding the stimulus faces (e.g., facial emotion, approachability etc.). The rating results suggest that individuals from an East Asian culture perceive another''s face as being angrier, unapproachable, and unpleasant when making eye contact as compared to individuals from a Western European culture. The rating results also revealed that gaze direction (direct vs. averted) could influence perceptions about another person''s facial affect and disposition. These results suggest that cultural differences in eye contact behaviour emerge from differential display rules and cultural norms, as opposed to culture affecting eye contact behaviour directly at the physiological level.     

A specific and rapid neural signature for parental instinct

Darwin originally pointed out that there is something about infants which prompts adults to respond to and care for them, in order to increase individual fitness, i.e. reproductive success, via increased survivorship of one's own offspring. Lorenz proposed that it is the specific structure of the infant face that serves to elicit these parental responses, but the biological basis for this remains elusive. Here, we investigated whether adults show specific brain responses to unfamiliar infant faces compared to adult faces, where the infant and adult faces had been carefully matched across the two groups for emotional valence and arousal, as well as size and luminosity. The faces also matched closely in terms of attractiveness. Using magnetoencephalography (MEG) in adults, we found that highly specific brain activity occurred within a seventh of a second in response to unfamiliar infant faces but not to adult faces. This activity occurred in the medial orbitofrontal cortex (mOFC), an area implicated in reward behaviour, suggesting for the first time a neural basis for this vital evolutionary process. We found a peak in activity first in mOFC and then in the right fusiform face area (FFA). In mOFC the first significant peak (p<0.001) in differences in power between infant and adult faces was found at around 130 ms in the 10-15 Hz band. These early differences were not found in the FFA. In contrast, differences in power were found later, at around 165 ms, in a different band (20-25 Hz) in the right FFA, suggesting a feedback effect from mOFC. These findings provide evidence in humans of a potential brain basis for the "innate releasing mechanisms" described by Lorenz for affection and nurturing of young infants. This has potentially important clinical applications in relation to postnatal depression, and could provide opportunities for early identification of families at risk.     

Effects of environmental enrichment on reproduction

Although there have been few demonstrations of a direct empirical relationship between environmental enrichment and reproductive success in captive animals, indirect and anecdotal evidence indicates the importance of physical and temporal complexity for reproduction. We discuss three major mechanisms through which environmental enrichment that specifically increases the complexity of an animal's surroundings may influence reproductive physiology and behavior: developmental processes, modulation of stress and arousal, and modification of social interactions. In complex environments developing animals learn that performing active behavior produces appropriate functional outcomes. Learning to control their environment influences their ability to adapt to novel situations, which may profoundly influence their reproductive behavior as adults in breeding situations. Chronic stress may compromise reproductive physiology and behavior; enrichment reduces stress by providing increased opportunity for behavioral coping responses. However, some degree of acute stress may be beneficial for reproduction by maintaining an animal's level of responsiveness to socio-sexual stimuli necessary for sexual arousal and reproductive activation. Finally, environmental enrichment may influence reproductive success by stabilizing social groups, reducing aggression and increasing affiliative and play behaviors. It is concluded that multi-variate multi-institutional behavioral research in zoos will play an increasingly important role in the successful captive propagation of many species by closely examining relationships between environmental variables and reproductive potential of individual animals. © 1994 Wiley-Liss, Inc.     

Parasite primes make foreign-accented English sound more distant to people who are disgusted by pathogens (but not by sex or morality)

To avoid disease, people should maintain close ties with ingroup members but maintain distance from outgroup members who possess novel pathogens. Consistent with this disease-avoidance hypothesis, pathogenic stimuli, as well as increased personal vulnerability to disease, are associated with xenophobic and ethnocentric attitudes. Researchers assume that this disease-avoidance process is an automatic emotional response that compels negative attitudes and behavioral avoidance. However, when outgroup contact can represent fitness costs or benefits, and when group membership is an uncertain cue to infection risk, it becomes a fitness advantage for a social perceiver to track group membership and thus infection risk. Given that accents can be a cue to group membership, we predicted that the perception of linguistic similarity to ingroup speakers and dissimilarity from outgroup speakers would increase with individual differences in pathogen disgust, and that this association would be most apparent when threat of disease was salient. This hypothesis was confirmed in two experiments. Further, the mechanism was domain specific—disgust due to sexual acts and moral violations did not moderate perceived linguistic distance. The disease-avoidance mechanism is not just an automatic disgust-based reaction; it also operates through the cognitive appraisal of social distance.     

Regional brain responses in nulliparous women to emotional infant stimuli

Infant cries and facial expressions influence social interactions and elicit caretaking behaviors from adults. Recent neuroimaging studies suggest that neural responses to infant stimuli involve brain regions that process rewards. However, these studies have yet to investigate individual differences in tendencies to engage or withdraw from motivationally relevant stimuli. To investigate this, we used event-related fMRI to scan 17 nulliparous women. Participants were presented with novel infant cries of two distress levels (low and high) and unknown infant faces of varying affect (happy, sad, and neutral) in a randomized, counter-balanced order. Brain activation was subsequently correlated with scores on the Behavioral Inhibition System/Behavioral Activation System scale. Infant cries activated bilateral superior and middle temporal gyri (STG and MTG) and precentral and postcentral gyri. Activation was greater in bilateral temporal cortices for low- relative to high-distress cries. Happy relative to neutral faces activated the ventral striatum, caudate, ventromedial prefrontal, and orbitofrontal cortices. Sad versus neutral faces activated the precuneus, cuneus, and posterior cingulate cortex, and behavioral activation drive correlated with occipital cortical activations in this contrast. Behavioral inhibition correlated with activation in the right STG for high- and low-distress cries relative to pink noise. Behavioral drive correlated inversely with putamen, caudate, and thalamic activations for the comparison of high-distress cries to pink noise. Reward-responsiveness correlated with activation in the left precentral gyrus during the perception of low-distress cries relative to pink noise. Our findings indicate that infant cry stimuli elicit activations in areas implicated in auditory processing and social cognition. Happy infant faces may be encoded as rewarding, whereas sad faces activate regions associated with empathic processing. Differences in motivational tendencies may modulate neural responses to infant cues.     

Brain responses to the acquired moral status of faces

We examined whether neural responses associated with judgments of socially relevant aspects of the human face extend to stimuli that acquire their significance through learning in a meaningful interactive context, specifically reciprocal cooperation. During fMRI, subjects made gender judgments on faces of people who had been introduced as fair (cooperators) or unfair (defector) players through repeated play of a sequential Prisoner's Dilemma game. To manipulate moral responsibility, players were introduced as either intentional or nonintentional agents. Our behavioral (likebility ratings and memory performance) as well as our imaging data confirm the saliency of social fairness for human interactions. Relative to neutral faces, faces of intentional cooperators engendered increased activity in left amygdala, bilateral insula, fusiform gyrus, STS, and reward-related areas. Our data indicate that rapid learning regarding the moral status of others is expressed in altered neural activity within a system associated with social cognition.     

Collective action in culturally similar and dissimilar groups: an experiment on parochialism,conditional cooperation,and their linkages

This study examines the effects of ingroup favoritism and outgroup hostility (“parochialism”), as well as of conditionally cooperative strategies, in explaining contributions to experimental public goods games. The experimental conditions vary group composition along two culturally inheritable traits (political party preference and religious affiliation) and one trivial, “minimal” trait (birth season). We contrast ingroup, outgroup, and random group conditions and investigate the relation between the own contribution to the public good and the expectations about other group members' behavior in each one of them. We find evidence for ingroup favoritism but no support for a separate tendency towards outgroup hostility. Further, conditional cooperation and ingroup bias are, to some extent, linked. Subjects had higher expectations of the contributions of ingroup members, and their own behavior was more strongly conditioned on other group members' expected behavior in the ingroup conditions. In ingroup contexts, subjects displayed a form of “strong reciprocity” by giving more than they expected others to at high expectation levels but less at low expectation levels. Once these interactions are taken into account, we do not find a direct effect of ingroup bias anymore. We discuss these results in the light of theories of cultural group selection and conclude that too much emphasis may have been laid on direct intergroup conflict. Our results suggest that differential cooperativeness, rather than parochialism, may characterize the behavior of individuals in cultural ingroups and outgroups.     

Developmental and Individual Differences in the Neural Processing of Dynamic Expressions of Pain and Anger

We examined the processing of facial expressions of pain and anger in 8-month-old infants and adults by measuring event-related brain potentials (ERPs) and frontal EEG alpha asymmetry. The ERP results revealed that while adults showed a late positive potential (LPP) to emotional expressions that was enhanced to pain expressions, reflecting increased evaluation and emotional arousal to pain expressions, infants showed a negative component (Nc) to emotional expressions that was enhanced to angry expressions, reflecting increased allocation of attention to angry faces. Moreover, infants and adults showed opposite patterns in their frontal asymmetry responses to pain and anger, suggesting developmental differences in the motivational processes engendered by these facial expressions. These findings are discussed in the light of associated individual differences in infant temperament and adult dispositional empathy.     

Neural responses to ingroup and outgroup members' suffering predict individual differences in costly helping

Little is known about the neurobiological mechanisms underlying prosocial decisions and how they are modulated by social factors such as perceived group membership. The present study investigates the neural processes preceding the willingness to engage in costly helping toward ingroup and outgroup members. Soccer fans witnessed a fan of their favorite team (ingroup member) or of a rival team (outgroup member) experience pain. They were subsequently able to choose to help the other by enduring physical pain themselves to reduce the other's pain. Helping the ingroup member was best predicted by anterior insula activation when seeing him suffer and by associated self-reports of empathic concern. In contrast, not helping the outgroup member was best predicted by nucleus accumbens activation and the degree of negative evaluation of the other. We conclude that empathy-related insula activation can motivate costly helping, whereas an antagonistic signal in nucleus accumbens reduces the propensity to help.     

The psychology of deterrence explains why group membership matters for third-party punishment

Humans regularly intervene in others' conflicts as third-parties. This has been studied using the third-party punishment game: A third-party can pay a cost to punish another player (the “dictator”) who treated someone else poorly. Because the game is anonymous and one-shot, punishers are thought to have no strategic reasons to intervene. Nonetheless, punishers often punish dictators who treat others poorly. This result is central to a controversy over human social evolution: Did third-party punishment evolve to maintain group norms or to deter others from acting against one's interests? This paper provides a critical test. We manipulate the ingroup/outgroup composition of the players while simultaneously measuring the inferences punishers make about how the dictator would treat them personally. The group norm predictions were falsified, as outgroup defectors were punished most harshly, not ingroup defectors (as predicted by ingroup fairness norms) and not outgroup members generally (as predicted by norms of parochialism). The deterrence predictions were validated: Punishers punished the most when they inferred that they would be treated the worst by dictators, especially when better treatment would be expected given ingroup/outgroup composition.