Social cognition under stress: Differential effects of stress-induced cortisol elevations in healthy young men and women

Humans as social beings often have to perform complex social cognitive tasks while under stress (e.g., during a social conflict). Previous research has established that the brain regions responsible for social cognitive tasks are target regions for stress hormones. However, little experimental research has been done testing the acute effects of stress on social cognition. Here, we investigated whether stress exposure and the ensuing glucocorticoid (i.e., cortisol) elevations affect social cognition. Thirty-two men and 32 women were exposed to either a psychosocial stress or a non-stressful control test before assessing their social cognition using the Reading the Mind in the Eyes Test (RMET) and the Movie for the Assessment of Social Cognition (MASC). Results showed differential effects of stress-induced cortisol responses among men and women for the MASC, but not the RMET. Among men, high cortisol responders displayed elevated MASC scores compared with low cortisol responders. Moreover, for stressed men a positive association between the magnitude of the cortisol responses to the stressor and MASC scores emerged. Among women, enhanced MASC scores were found for low cortisol responders relative to high cortisol responders and non-stressed controls. A strong negative association between cortisol reactivity and MASC scores was found among women. These results imply sex specific effects of glucocorticoids on social cognition and partially support the idea of sex differences in biobehavioral stress responses, with men engaging in fight-or-flight responses while women may react to stress with tending and befriending behavior.     

Sex differences in indirect aggression: Psychological evidence from young adults

Many studies have found differences in the types of aggression used by males and females, at least in children and adolescents. Boys tend to use direct physical or verbal aggression, whereas girls tend to use more indirect forms of aggression that prominently feature gossip. Evolutionary theories of sex differences in indirect aggression propose selection pressures that would have acted on older teenagers and adults. Evidence for sex differences in indirect aggression in adults, however, is equivocal. Virtually all studies of adults have found a sex difference in physical aggression, but most have failed to find sex differences in the use of the more indirect forms of aggression. Almost all of these studies have measured indirect aggression using self-reports of aggressive behavior. We investigated sex differences in the psychology of indirect aggression by exposing young adult women and men to the same aggression-evoking stimulus. As evolutionary models predict, we found that women had a stronger desire than men to aggress indirectly, even after controlling for perceptions of social norms and approval. Future work on both evolutionary and social norm models of indirect aggression is warranted.     

Sex differences in cortisol's regulation of affiliative behavior

A contribution to a special issue on Hormones and Human Competition.A stress perspective is used to illuminate how competitive defeat and victory shape biology and behavior. We report a field study examining how change in cortisol following perceived defeat (vs. victory) in a competition—in this case, a dog agility competition—relates to affiliative behavior. Following competition, we measured cortisol change and the extent to which dog handlers directed affiliative behaviors toward their dogs. We found striking sex differences in affiliation. First, men were more affiliative toward their dogs after victory, whereas women were more affiliative after defeat. Second, the greater a female competitor's increase in cortisol, the more time she spent affiliating with her dog, whereas for men, the pattern was the exact opposite: the greater a male competitor's increase in cortisol, the less time he spent affiliating with his dog. This pattern suggests that, in the wake of competition, men and women's affiliative behavior may serve different functions—shared celebration for men; shared consolation for women. These sex differences show not only that men and women react very differently to victory and defeat, but also that equivalent changes in cortisol across the sexes are associated with strikingly different behavioral consequences for men and women.     

Sex difference in testosterone response to a video game contest

Testosterone (T) and cortisol (C) were assayed from saliva samples given by young men (n = 28) and women (n = 32) before, during, and after competing with a same-sex partner in a video game. The T response to the competition is different in each sex; the C response is the same. Male results confirm prior reports of a precontest rise in testosterone. Male results did not confirm previous findings that, after a contest, the testosterone of winners is higher than that of losers, perhaps because the video game contest produced little mood difference between male winners and losers. Unlike male testosterone, female testosterone generally decreased throughout the experiment. Trends in T and C are parallel in women but not in men. Apparently T works differently in competition between men than between women.     

Sex differences in salivary cortisol in response to acute stressors among healthy participants, in recreational or pathological gamblers, and in those with posttraumatic stress disorder

Sex differences in incidence and severity of some stress-related, neuropsychiatric disorders are often reported to favor men, suggesting that women may be more vulnerable to aberrant hypothalamic-pituitary-adrenal (HPA) axis responses to stress. In this review, we discuss several investigations that we, and others, have conducted assessing salivary cortisol as a measure of HPA function. We have examined basal cortisol among healthy men and women and also following acute exposure to stressors. Among healthy participants, men had higher basal cortisol levels than did women. In response to acute stressors, such as carbon dioxide or noise, respectively, cortisol levels were comparable between men and women or higher among women. We have also examined cortisol levels among those with problem eating, gambling, or posttraumatic stress disorder (PTSD). Women with restrained eating habits have higher basal cortisol levels than do women without restrained eating habits. Pathological gamblers have more aberrant stress response to gambling stimuli than do recreational gamblers, and these effects are more prominent among men than women. Men who have motor vehicle accident related PTSD, demonstrate more aberrant cortisol function, than do their female counterparts. Although these sex differences in cortisol seem to vary with type of stress exposure and/or pathophysiological status of the individual, other hormones may influence cortisol response. To address this, cortisol levels among boys and girls with different stress-related experiences, will be the subject of future investigation.     

Cortisol and GH secretory dynamics, and their interrelationships, in healthy aged women and men

We studied 130 healthy aged women (n = 57) and men (n = 73), age 65-88 yr, with age-related reductions in insulin-like growth factor I and gonadal steroid levels to assess the interrelationships between cortisol and growth hormone (GH) secretion and whether these relationships differ by sex. Blood was sampled every 20 min from 8:00 PM to 8:00 AM; cortisol was measured by RIA and GH by immunoradiometric assay, followed by deconvolution analyses of hormone secretory parameters and assessment of approximate entropy (ApEn) and cross-ApEn. Cortisol mass/burst, cortisol production rate, and mean and integrated serum cortisol concentrations (P < 0.0005), and overnight basal GH secretion (P < 0.05), were elevated in women vs. men. Integrated cortisol concentrations were directly related to most measures of GH secretion in women (P < 0.01) and with mean and integrated GH concentrations in men (P < 0.05). Integrated GH concentrations were directly related to mean and integrated cortisol levels in women (P < 0.005) and men (P < 0.05), with no sex differences. There were no sex differences in cortisol or GH ApEn values; however, the cross-ApEn score was greater in women (P < 0.05), indicating reduced GH-cortisol pattern synchrony in aged women vs. men. There were no significant relationships of integrated cortisol secretion with GH ApEn, or vice versa, in either sex. Thus postmenopausal women appear to maintain elevated cortisol production in patterns that are relatively uncoupled from those of GH, whereas mean hormone outputs remain correlated.     

Interpersonal Aggression among Aka Hunter-Gatherers of the Central African Republic

Sex differences in physical and indirect aggression have been found in many societies but, to our knowledge, have not been studied in a population of hunter-gatherers. Among Aka foragers of the Central African Republic we tested whether males physically aggressed more than females, and whether females indirectly aggressed more than males, as has been seen in other societies. We also tested predictions of an evolutionary theory of physical strength, anger, and physical aggression. We found a large male bias in physical aggression. Controlling for anger, we found an adult female bias in indirect aggression. Physical strength predicted anger, which predicted hitting, although results were sensitive to the inclusion or exclusion of traditional healers, who were physically and emotionally distinct from other Aka. With some important caveats, our results generally support the predicted sex differences in physical aggression and indirect aggression, and the predicted relationships among anger, strength, and aggression.     

Sex Differences in Reconciliation and Post-Conflict Anxiety in Bonnet Macaques

Rates of reconciliation vary widely between different types of opponents, and post‐conflict anxiety has been proposed to mediate individual variation in reconciliation rates. We investigated the form and function of reconciliation in a wild, provisioned group of bonnet macaques (Macaca radiata) with the prediction that sex differences in post‐conflict anxiety would be associated with sex differences in conciliatory tendency. Individuals in the study group had a conciliatory tendency of 29.3%. Victims avoided their former opponents at a higher rate following aggression than during matched‐control samples, and reconciliation decreased the rate of avoidance. Although victims showed a higher rate of anxiety‐related behavior than did aggressors, anxiety‐related behavior was elevated after aggression and reduced following reconciliation in both victims and aggressors. Female–female opponents showed higher rates of anxiety‐related behavior before reconciliation than they did following unreconciled aggression. In contrast, male–male and female–male opponents showed increased anxiety‐related behavior following aggression regardless of the occurrence of reconciliation. Moreover, female–female opponents had a higher conciliatory tendency than did female–male opponents. The elevated post‐conflict anxiety shown by female–female opponents before reconciliation, along with their high conciliatory tendency, suggests that post‐conflict anxiety promotes reconciliation. In sum, the sex differences in post‐conflict behavior found in this study support the hypothesis that variation in post‐conflict anxiety mediates differential rates of reconciliation.     

Sex differences in mushroom gathering: men expend more energy to obtain equivalent benefits

Some of the strongest evidence for sex differences in human cognition relate to spatial abilities, with men traditionally reported to outperform women. Recently, however, such differences have been shown to be task dependent. Supporting the argument that a critical factor selecting for sex differences in spatial abilities during human evolution is likely to have been the division of labor during the Pleistocene, evidence is accumulating that women excel on tasks appropriate to gathering immobile plant resources, while men excel on tasks appropriate to hunting mobile, unpredictable prey. Most research, with the exception of some recent experimental field studies, has been conducted in the laboratory, with little information available on how men and women actually forage under natural conditions. In a first study, we GPS-tracked the foraging pathways of 21 pairs of men and women from an indigenous Mexican community searching for mushrooms in a natural environment. Measures of costs, benefits and general search efficiency were analyzed and related to differences between the two sexes in foraging patterns. Although men and women collected similar quantities of mushrooms, men did so at significantly higher cost. They traveled further, to greater altitudes, and had higher mean heart rates and energy expenditure (kcal). They also collected fewer species and visited fewer collection sites. These findings are consistent with arguments in the literature that differences in spatial ability between the sexes are domain dependent, with women performing better and more readily adopting search strategies appropriate to a gathering lifestyle than men.     

Sex,gender, and difference

Empirical research has demonstrated that women’s aggressive behavior is widespread and displays regularities across societies. Until recently, however, discussions about the aggressive behavior of women and gender differences in aggressive behavior have been based largely on data from nonhuman primates, children, or laboratory experiments. Using a unique corpus of naturalistic data on aggressive human interactions both between and among men and women, I explore the complexity of our questions about sex differences in aggression and further illuminate the ways in which men and women may use aggression in human interactions. In this paper I compare the aggressive behavior of men and women in an Australian Aboriginal community. In doing so I argue for the continuing use of a “sex differences” framework for organizing our understanding of gender relations and gender hierarchy. I believe, however, that this form of analysis benefits from, if not requires, a sensitivity to the most taken-for-granted aspects of our gender ideology and a commitment to attend to evidence that challenges our convictions about men and women.     

Killing the competition

Sex- and age-specific rates of killing unrelated persons of one’s own sex were computed for Canada (1974–1983), England/Wales (1977–1986), Chicago (1965–1981), and Detroit (1972) from census information and data archives of all homicides known to police. Patterns in relation to sex and age were virtually identical among the four samples, although the rates varied enormously (from 3.7 per million citizens per annum in England/Wales to 216.3 in Detroit). Men’s marital status was related to the probability of committing a same-sex, nonrelative homicide, but age effects remained conspicuous when married and unmarried men were distinguished. These findings and the treatment of age and sex effects by criminologists are discussed in the light of contemporary evolutionary psychological models of sex differences and life-span development. Same-sex homicides in which killer and victim are unrelated can be interpreted as an assay of competitive conflict. In every human society for which relevant information exists, men kill one another vastly more often than do women. Lethal interpersonal competition is especially prevalent among young men, which accords with many other aspects of life-span development in suggesting that sexual selection has maximized male competitive prowess and inclination in young adulthood.     

Cortisol alters reward processing in the human brain

Dysfunctional reward processing is known to play a central role for the development of psychiatric disorders. Glucocorticoids that are secreted in response to stress have been shown to attenuate reward sensitivity and thereby might promote the onset of psychopathology. However, the underlying neurobiological mechanisms mediating stress hormone effects on reward processing as well as potential sex differences remain elusive. In this neuroimaging study, we administered 30 mg cortisol or a placebo to 30 men and 30 women and subsequently tested them in the Monetary Incentive Delay Task. Cortisol attenuated anticipatory neural responses to a verbal and a monetary reward in the left pallidum and the right anterior parahippocampal gyrus. Furthermore, in men, activation in the amygdala, the precuneus, the anterior cingulate, and in hippocampal regions was reduced under cortisol, whereas in cortisol-treated women a signal increase was observed in these regions. Behavioral performance also indicated that reward learning in men is impaired under high cortisol concentrations, while it is augmented in women. These findings illustrate that the stress hormone cortisol substantially diminishes reward anticipation and provide first evidence that cortisol effects on the neural reward system are sensitive to sex differences, which might translate into different vulnerabilities for psychiatric disorders.     

Testosterone reactivity to facial display of emotions in men and women

Previous studies have examined testosterone's role in regulating the processing of facial displays of emotions (FDEs). However, the reciprocal process – the influence of FDEs, an evolutionarily ancient and potent class of social signals, on the secretion of testosterone – has not yet been studied. To address this gap, we examined the effects of emotional content and sex of facial stimuli in modulating endogenous testosterone fluctuations, as well as sex differences in the endocrine responses to faces. One hundred and sixty-four young healthy men and women were exposed, in a between-subjects design, to happy or angry same-sex or opposite-sex facial expressions. Results showed that in both men (n = 85) and women (n = 79), extended exposure to faces of the opposite sex, regardless of their apparent emotional content, was accompanied by an accumulation in salivary testosterone when compared to exposure to faces of the same sex. Furthermore, testosterone change in women exposed to angry expressions was greater than testosterone change in women exposed to happy expressions. These results add emotional facial stimuli to the collection of social signals that modulate endocrine status, and are discussed with regard to the evolutionary roles of testosterone.     

Sex differences in intrasexual aggression among sex-role-reversed,cooperatively breeding cichlid fish <Emphasis Type="Italic">Julidochromis regani</Emphasis>

In sex-role-reversed species, females compete for resources (e.g., mates) more intensively than do males. However, it remains unclear whether these species exhibit sex differences in the intensity of aggressive behavior in the context of within-sex contests. Cichlid fish in the genus Julidochromis exhibit intraspecific variation in mating systems, ranging from monogamy to cooperative polyandry with sex-role reversal. In the study reported here, we observed aggressive interactions among three same-sex individuals in Julidochromis regani in the laboratory and tested whether inter-female aggression was more intense than inter-male aggression. Although difference in body size strongly determined the direction of aggression in fish, aggression by a smaller-sized individuals toward larger ones was occasionally observed. This type of aggression was common between individuals of a similar body size (≤5 mm) and occurred more frequently among females than males. In contrast, differences in body size and sex did not affect the frequency of aggression by larger-sized individuals against smaller ones. Bidirectional aggression (i.e., mouth fighting) occurred frequently when two individuals had similar body size, and there was no difference in its frequency between sexes. However, temporal analysis showed that females performed bidirectional aggression more persistently than males. These sex differences in the intensity of intrasexual aggression could be the behavioral mechanisms underpinning cooperative polyandry.     

Sex Differences in Genetic Architecture of Complex Phenotypes?

We examined sex differences in familial resemblance for a broad range of behavioral, psychiatric and health related phenotypes (122 complex traits) in children and adults. There is a renewed interest in the importance of genotype by sex interaction in, for example, genome-wide association (GWA) studies of complex phenotypes. If different genes play a role across sex, GWA studies should consider the effect of genetic variants separately in men and women, which affects statistical power. Twin and family studies offer an opportunity to compare resemblance between opposite-sex family members to the resemblance between same-sex relatives, thereby presenting a test of quantitative and qualitative sex differences in the genetic architecture of complex traits. We analyzed data on lifestyle, personality, psychiatric disorder, health, growth, development and metabolic traits in dizygotic (DZ) same-sex and opposite-sex twins, as these siblings are perfectly matched for age and prenatal exposures. Sample size varied from slightly over 300 subjects for measures of brain function such as EEG power to over 30,000 subjects for childhood psychopathology and birth weight. For most phenotypes, sample sizes were large, with an average sample size of 9027 individuals. By testing whether the resemblance in DZ opposite-sex pairs is the same as in DZ same-sex pairs, we obtain evidence for genetic qualitative sex-differences in the genetic architecture of complex traits for 4% of phenotypes. We conclude that for most traits that were examined, the current evidence is that same the genes are operating in men and women.     

Sex-specific difference in the interconversion of cortisol and cortisone in men and women

Objective: Our objective was to demonstrate that the smaller oxoreductase activity of 11β‐HSD1 in women would shift the interconversion of cortisol and cortisone toward cortisone, resulting in a larger amount of generated labeled cortisone in healthy women than in healthy men. Research Methods and Procedures: Using mass spectrometry, the amount of cortisone generated from a continuous infusion (8 am to 6 pm ) of stable‐labeled cortisol (1α,2α‐d‐cortisol) was determined in non‐obese and in obese (BMI >35 kg/m²) men and women during steady‐state conditions (from 2 pm to 6 pm ). In this setting, the amount of generated labeled cortisone (expressed as % of the achieved steady‐state concentrations of labeled cortisol) reflects the sum of the bi‐directional conversion of cortisol into cortisone (and vice versa) by 11β‐hydroxysteroid dehydrogenase. Results: The amount of generated labeled cortisone was higher in men than in women (p < 0.0001). This sex difference was higher in obese than in non‐obese patients (p = 0.0062). Conclusions: The interconversion of cortisol and cortisone during steady‐state conditions is shifted toward cortisol in men as compared with women. This suggests a higher overall oxoreductase activity of 11β‐hydroxysteroid dehydrogenase type 1 in men than in women. This sex‐specific difference is maintained in obesity.     

Social exchange and solidarity: in-group love or out-group hate?

Men exhibit a stronger tendency to favor the in-group over the out-group compared to women. We examined whether this male-specific “coalitional psychology” represents in-group love or out-group hate. One hundred thirty-three college freshmen played a prisoner's dilemma game with a member of their own group and a member of another group. Both groups consisted of same-sex participants. An in-group bias (cooperation with the in-group at a level higher than cooperation with the out-group) based on expectations of cooperation from the in-group was observed for both men and women. When such expectations were experimentally eliminated, women did not show any in-group bias, whereas men still exhibited an in-group bias. This male-specific in-group bias was found to be a product of intragroup cooperation (in-group love) rather than a product of intergroup competition (out-group hate). These findings suggest that the male-specific coalitional psychology caters more toward the promotion of within-group solidarity than aggression against the out-group.     

2D:4D finger-length ratios in children and adults with gender identity disorder

Previous research suggests that prenatal testosterone affects the 2D:4D finger ratio in humans, and it has been speculated that prenatal testosterone also affects gender identity differentiation. If both things are true, then one would expect to find an association between the 2D:4D ratio and gender identity. We measured 2D:4D in two samples of patients with gender identity disorder (GID). In Study 1, we compared the 2D:4D ratios of 96 adult male and 51 female patients with GID to that of 90 heterosexual male and 112 heterosexual female controls. In Study 2, we compared the 2D:4D ratios of 67 boys and 34 girls with GID to that of 74 control boys and 72 control girls. In the sample of adults with GID, we classified their sexual orientation as either homosexual or non-homosexual (in relation to their birth sex) to examine whether or not there were any within-group differences as a function of sexual orientation. In the sample of adult men with GID (both homosexual and non-homosexual) and children with GID, we found no evidence of an altered 2D:4D ratio relative to same-sex controls. However, women with GID had a significantly more masculinized ratio compared to the control women. This last finding was consistent with the prediction that a variance in prenatal hormone exposure contributes to a departure from a sex-typical gender identity in women.     

Adaptive allocation of attention: effects of sex and sociosexuality on visual attention to attractive opposite-sex faces

We tested the hypothesis that, compared with sociosexually restricted individuals, those with an unrestricted approach to mating would selectively allocate visual attention to attractive opposite-sex others. We also tested for sex differences in this effect. Seventy-four participants completed the Sociosexual Orientation Inventory and performed a computer-based task that assessed the speed with which they detected changes in attractive and unattractive male and female faces. Differences in reaction times served as indicators of selective attention. Results revealed a Sex×Sociosexuality interaction: Compared with sociosexually restricted men, unrestricted men selectively allocated attention to attractive opposite-sex others; no such effect emerged among women. This finding was specific to opposite-sex targets and did not occur in attention to same-sex others. These results contribute to a growing literature on the adaptive allocation of attention in social environments.