Age, sex, and dominance-related mushroom body plasticity in the paperwasp Mischocyttarus mastigophorus

Social Hymenoptera are important models for analyzing functional brain plasticity. These insects provide the opportunity to learn how individuals' social roles are related to flexible investment in different brain regions. We assessed how age, sex, and individual behavior influence brain development in a primitively eusocial paper wasp, Mischocyttarus mastigophorus. Previous research in other species has demonstrated experience-dependent changes in central and primary sensory centers in the brain. The mushroom body (MB) calyx is a central processing region involved in sensory integration, learning and memory and may be particularly relevant to social behavior. We extend earlier cross-sectional studies of female brain/behavior associations by measuring sex- and age-related differences in MB calyx volume, and by quantifying optic lobe and antennal lobe development. Age did predict MB development: calyx neuropils increased in volume with age. We show that MB development differs between the sexes. Males, who frequently depart to seek mating opportunities, have larger MB calyx collars (which receive optic input) than females. In contrast, females have augmented predominantly antenna-innervated MB calyx lips, which may be useful for nestmate recognition and interactions on the nest. Sex differences in MB development increased with age. After accounting for age and sex effects, social aggression was positively correlated with MB calyx volume for both sexes. We found little evidence for relationships among sex, age, or behavior and the volumes of peripheral sensory processing structures. We discuss the implications of gender- and age-related effects on brain volume in relation to male and female life history and reproductive success.     

In Others' Shoes: Do Individual Differences in Empathy and Theory of Mind Shape Social Preferences?

Abundant evidence across the behavioral and social sciences suggests that there are substantial individual differences in pro-social behavior. However, little is known about the psychological mechanisms that underlie social preferences. This paper investigates whether empathy and Theory of Mind shape individual differences in pro-social behavior as conventionally observed in neutrally framed social science experiments. Our results show that individual differences in the capacity for empathy do not shape social preferences. The results qualify the role of Theory of Mind in strategic interaction. We do not only show that fair individuals exhibit more accurate beliefs about the behavior of others but that Theory of Mind can be effectively used to pursue both self-interest and pro-social goals depending on the principle objectives of a person.     

Pharmacological Cognitive Enhancement in Healthy Individuals: A Compensation for Cognitive Deficits or a Question of Personality?

The ongoing bioethical debate on pharmacological cognitive enhancement (PCE) in healthy individuals is often legitimated by the assumption that PCE will widely spread and become desirable for the general public in the near future. This assumption was questioned as PCE is not equally save and effective in everyone. Additionally, it was supposed that the willingness to use PCE is strongly personality-dependent likely preventing a broad PCE epidemic. Thus, we investigated whether the cognitive performance and personality of healthy individuals with regular nonmedical methylphenidate (MPH) use for PCE differ from stimulant-naïve controls. Twenty-five healthy individuals using MPH for PCE were compared with 39 age-, sex-, and education-matched healthy controls regarding cognitive performance and personality assessed by a comprehensive neuropsychological test battery including social cognition, prosocial behavior, decision-making, impulsivity, and personality questionnaires. Substance use was assessed through self-report in an interview and quantitative hair and urine analyses. Recently abstinent PCE users showed no cognitive impairment but superior strategic thinking and decision-making. Furthermore, PCE users displayed higher levels of trait impulsivity, novelty seeking, and Machiavellianism combined with lower levels of social reward dependence and cognitive empathy. Finally, PCE users reported a smaller social network and exhibited less prosocial behavior in social interaction tasks. In conclusion, the assumption that PCE use will soon become epidemic is not supported by the present findings as PCE users showed a highly specific personality profile that shares a number of features with illegal stimulant users. Lastly, regular MPH use for PCE is not necessarily associated with cognitive deficits.     

Second-to-Fourth Digit Ratio and Impulsivity: A Comparison between Offenders and Nonoffenders

Personality characteristics, particularly impulsive tendencies, have long been conceived as the primary culprit in delinquent behavior. One crucial question to emerge from this line of work is whether impulsivity has a biological basis. To test this possibility, 44 male offenders and 46 nonoffenders completed the Eysenck Impulsivity Questionnaire, and had their 2D∶4D ratio measured. Offenders exhibited smaller right hand digit ratio measurements compared to non-offenders, but higher impulsivity scores. Both impulsivity and 2D∶4D ratio measurements significantly predicted criminality (offenders vs. nonoffenders). Controlling for education level, the 2D∶4D ratio measurements had remained a significant predictor of criminality, while impulsivity scores no longer predicted criminality significantly. Our data, thus, indicates that impulsivity but not 2D∶4D ratio measurements relate to educational attainment. As offenders varied in their number of previous convictions and the nature of their individual crimes, we also tested for differences in 2D∶4D ratio and impulsivity among offenders. Number of previous convictions did not correlate significantly with the 2D∶4D ratio measurements or impulsivity scores. Our study established a link between a biological marker and impulsivity among offenders (and lack thereof among non-offenders), which emphasise the importance of studying the relationship between biological markers, impulsivity and criminal behavior.     

Methylphenidate to adolescent rats drives enduring changes of accumbal Htr7 expression: implications for impulsive behavior and neuronal morphology

Methylphenidate (MPH) administration to adolescent rodents produces persistent region-specific changes in brain reward circuits and alterations of reward-based behavior. We show that these modifications include a marked increment of serotonin (5-hydroxy-tryptamine) receptor type 7 (Htr7) expression and synaptic contacts, mainly in the nucleus accumbens , and a reduction of basal behavioral impulsivity. We show that neural and behavioral consequences are functionally related: administration of a selective Htr7 antagonist fully counteracts the MPH-reduced impulsive behavior and enhances impulsivity when administered alone in naive rats. Agonist-induced activation of endogenous Htr7 significantly increases neurite length in striatal neuron primary cultures, thus suggesting plastic remodeling of neuronal morphology. The mixed Htr (1a/7) agonist, 8-OH-DPAT, reduces impulsive behavior in adolescent rats and in naive adults, whose impulsivity is enhanced by the Htr7 antagonist. In summary, behavioral pharmacology experiments show that Htr7 mediates self-control behavior, and brain primary cultures experiments indicate that this receptor may be involved in the underlying neural plasticity, through changes in neuronal cytoarchitecture.     

Is impulsive behavior adaptive in harsh and unpredictable environments? A formal model

Evolutionary social scientists have argued that impulsive behavior is adaptive in harsh and unpredictable conditions. Is this true? This paper presents a mathematical model that computes the optimal level of impulsivity in environments varying in harshness and unpredictability. We focus on information impulsivity, i.e., choosing to act without gathering or considering information about the consequences of one's actions. We explore two notions of harshness: the mean level of resources (e.g., food) and the mean level of extrinsic events (e.g., being the victim of a random attack). We explore three notions of unpredictability: variation in resources, variation in extrinsic events, and the interruption risk (the chance that a resource becomes unavailable). We also explore interactions between harshness and unpredictability. Our general model suggests four broad conclusions. First, impulsive behavior is not always adaptive in harsh and unpredictable conditions; rather, this depends on the exact definitions of harshness, unpredictability, and impulsivity. Second, impulsive behavior may be adaptive in environments in which the quality of resources is low or high, but is less likely to be adaptive when their quality is moderate. Third, impulsive behavior may be adaptive when resource encounters are likely to be interrupted. Fourth, extrinsic events have only a limited effect on whether impulsive behavior is adaptive. We discuss the implications of these findings for future research, consider limitations, and suggest future directions.     

Effects of in ovo treatment with PACAP antagonist on general activity, motor and social behavior of chickens

Pituitary adenylate cyclase activating polypeptide (PACAP) has been shown to influence nervous system development. The aim of the present study was to investigate the effects of in ovo treatment with the PACAP antagonist PACAP6-38 during embryonic life (E8 and E16) on motor activity and social behavior in chicken. Our results showed that a single injection of PACAP6-38 during the first half of embryonic life caused subtle transient changes in general behavior and motor control when compared to saline-treated controls. Increased activity and reduced anxiety were observed also in a novel environment at 2 days after hatching. However, most of these behavioral differences disappeared by 2 weeks. PACAP6-38-treatment during the first half of embryonic life resulted in markedly reduced social behavior, which was still present at 2 weeks of age. Treatment during the second half of embryonic life resulted in no behavioral differences between control and PACAP6-38-treated chicken. PACAP content in different brain areas was not different between control and PACAP6-38-treated chicken at 5 days or 3 weeks of age, but it decreased significantly with age in both groups. In summary, our results show that PACAP6-38 treatment at E8 caused transient changes in motor behavior, and long-lasting reduction in social behavior.     

Temporal discounting and heart rate reactivity to stress

Temporal discounting is the reduction of the value of a reinforcer as a function of increasing delay to its presentation. Impulsive individuals discount delayed consequences more rapidly than self-controlled individuals, and impulsivity has been related to substance abuse, gambling, and other problem behaviors. A growing body of literature has identified biological correlates of impulsivity, though little research to date has examined relations between delay discounting and markers of poor health (e.g., cardiovascular reactivity to stress). We evaluated the relation between one aspect of impulsivity, measured using a computerized temporal discounting task, and heart rate reactivity, measured as a change in heart rate from rest during a serial subtraction task. A linear regression showed that individuals who were more reactive to stress responded more impulsively (i.e., discounted delayed reinforcers more rapidly). When results were stratified by gender, the effect was observed for females, but not for males. This finding supports previous research on gender differences in cardiovascular reactivity and suggests that this type of reactivity may be an important correlate of impulsive behavior.     

Adolescent impulsivity predicts adult dominance attainment in male vervet monkeys

Adolescence is characterized by behavioral and physiological changes that prepare individuals for the transition to adulthood. The purpose of this study was to evaluate the effects of behavioral, morphological, neurobiological, and developmental characteristics of adolescent male vervets in predicting later dominance attainment. Thirty-six adolescent male vervets were tested for social impulsivity by means of the Intruder Challenge test while they were still living in their natal groups. Body weight and cerebrospinal fluid (CSF) metabolites of serotonin, dopamine, and norepinephrine were measured before they were introduced into new matrilineal breeding groups at age 5. Stable adult dominance rank was determined at age 6, 1 year following introduction. The results indicated that body weight, adolescent impulsivity, and levels of 5-hydroxyindoleacetic acid (5-HIAA) and homovanillic acid (HVA) in CSF predicted adult dominance attainment. As expected, males that were above average in body weight prior to introduction were significantly more likely to become dominant. Males that were high in impulsivity as adolescents, and low in 5-HIAA prior to introduction were more likely to achieve stable alpha male status 1 year following introduction. The combination of these three factors resulted in correct prediction of rank attainment for 92% (33/36) of the males. Two other factors-maternal dominance rank and a measure of social anxiety from the Intruder Challenge test-were not related to adult dominance attainment in this sample. These results support the idea that there are benefits of a high-risk, high-gain strategy is beneficial for adolescent and young adult male vervets. They also demonstrate that adolescent impulsivity is age-limited. Males that achieved high rank moderated their behavior as adults, and no longer scored high in impulsivity relative to their age peers.     

Differential Responses of Brain,Gonad and Muscle Steroid Levels to Changes in Social Status and Sex in a Sequential and Bidirectional Hermaphroditic Fish

Sex steroids can both modulate and be modulated by behavior, and their actions are mediated by complex interactions among multiple hormone sources and targets. While gonadal steroids delivered via circulation can affect behavior, changes in local brain steroid synthesis also can modulate behavior. The relative steroid load across different tissues and the association of these levels with rates of behavior have not been well studied. The bluebanded goby (Lythrypnus dalli) is a sex changing fish in which social status determines sexual phenotype. We examined changes in steroid levels in brain, gonad and body muscle at either 24 hours or 6 days after social induction of protogynous sex change, and from individuals in stable social groups not undergoing sex change. For each tissue, we measured levels of estradiol (E₂), testosterone (T) and 11-ketotestosterone (KT). Females had more T than males in the gonads, and more E₂ in all tissues but there was no sex difference in KT. For both sexes, E₂ was higher in the gonad than in other tissues while androgens were higher in the brain. During sex change, brain T levels dropped while brain KT increased, and brain E₂ levels did not change. We found a positive relationship between androgens and aggression in the most dominant females but only when the male was removed from the social group. The results demonstrate that steroid levels are responsive to changes in the social environment, and that their concentrations vary in different tissues. Also, we suggest that rapid changes in brain androgen levels might be important in inducing behavioral and/or morphological changes associated with protogynous sex change.     

What Shall We Talk about in Farsi?

Previous empirical studies have suggested that language is primarily used to exchange social information, but our evidence on this derives mainly from English speakers. We present data from a study of natural conversations among Farsi (Persian) speakers in Iran and show that not only are conversation groups the same size as those observed in Europe and North America, but people also talk predominantly about social topics. We argue that these results reinforce the suggestion that language most likely evolved for the transmission of information about the social world. We also explore sex differences in conversational behavior: while the pattern is broadly similar between the sexes, men may be more sensitive than women are to discussing some topics in the presence of many other people.     

To detect and correct: norm violations and their enforcement

Compliance with social norms requires neural signals related both to the norm and to deviations from it. Recent work using economic games between two interacting subjects has uncovered brain responses related to norm compliance and to an individual's strategic outlook during the exchange. These brain responses possess a provocative relationship to those associated with negative emotional outcomes, and hint at computational depictions of emotion processing.     

Sex differences and similarities in the neuroendocrine regulation of social behavior in an African cichlid fish

An individual's position in a social hierarchy profoundly affects behavior and physiology through interactions with community members, yet little is known about how the brain contributes to status differences between and within the social states or sexes. We aimed to determine sex-specific attributes of social status by comparing circulating sex steroid hormones and neural gene expression of sex steroid receptors in dominant and subordinate male and female Astatotilapia burtoni, a highly social African cichlid fish. We found that testosterone and 17β-estradiol levels are higher in males regardless of status and dominant individuals regardless of sex. Progesterone was found to be higher in dominant individuals regardless of sex. Based on pharmacological manipulations in males and females, progesterone appears to be a common mechanism for promoting courtship in dominant individuals. We also examined expression of androgen receptors, estrogen receptor α, and the progesterone receptor in five brain regions that are important for social behavior. Most of the differences in brain sex steroid receptor expression were due to sex rather than status. Our results suggest that the parvocellular preoptic area is a core region for mediating sex differences through androgen and estrogen receptor expression, whereas the progesterone receptor may mediate sex and status behaviors in the putative homologs of the nucleus accumbens and ventromedial hypothalamus. Overall our results suggest sex differences and similarities in the regulation of social dominance by gonadal hormones and their receptors in the brain.     

Effects of advanced paternal age on trajectories of social behavior in offspring

Our study is the first investigation of the effects of advanced paternal age (APA) on the developmental trajectory of social behavior in rodent offspring. Given the strong epidemiological association between APA and sexually dimorphic neurodevelopmental disorders that are characterized by abnormalities in social behavior (autism, schizophrenia), we assessed sociability in male and female inbred mice (C57BL/6J) across postnatal development (N = 104) in relation to paternal age. We found differences in early social behavior in both male and female offspring of older breeders, with differences in this social domain persisting into adulthood in males only. We showed that these social deficits were not present in the fathers of these offspring, confirming a de novo origin of an altered social trajectory in the offspring generation. Our results, highly novel in rodent research, support the epidemiological observations in humans and provide evidence for a causal link between APA, age‐related changes in the paternal sperm DNA and neurodevelopmental disorders in their offspring.     

Starving honeybees lose self-control

Impulsivity, the widespread preference for a smaller and more immediate reward over a larger and more delayed reward, is known to vary across species, and the metabolic and social hypotheses present contrasting explanations for this variation. However, this presents a paradox for an animal such as the honeybee, which is highly social, yet has a high metabolic rate. We test between these two competing hypotheses by investigating the effect of hunger on impulsivity in bees isolated from their social environment. Using an olfactory conditioning assay, we trained individuals to associate a small and a large reward with or without a delay, and we tested their choice between the two rewards at different levels of starvation. We found an increase in impulsive behaviour and an associated increase in dopamine levels in the brain with increasing starvation. These results suggest that the energetic state of an individual, even in a eusocial group, is a critical driver of impulsivity, and that the social harmony of a group can be threatened when the energetic states of the group members are in conflict.     

Individual attachment style modulates human amygdala and striatum activation during social appraisal

Adult attachment style refers to individual personality traits that strongly influence emotional bonds and reactions to social partners. Behavioral research has shown that adult attachment style reflects profound differences in sensitivity to social signals of support or conflict, but the neural substrates underlying such differences remain unsettled. Using functional magnetic resonance imaging (fMRI), we examined how the three classic prototypes of attachment style (secure, avoidant, anxious) modulate brain responses to facial expressions conveying either positive or negative feedback about task performance (either supportive or hostile) in a social game context. Activation of striatum and ventral tegmental area was enhanced to positive feedback signaled by a smiling face, but this was reduced in participants with avoidant attachment, indicating relative impassiveness to social reward. Conversely, a left amygdala response was evoked by angry faces associated with negative feedback, and correlated positively with anxious attachment, suggesting an increased sensitivity to social punishment. Secure attachment showed mirror effects in striatum and amygdala, but no other specific correlate. These results reveal a critical role for brain systems implicated in reward and threat processing in the biological underpinnings of adult attachment style, and provide new support to psychological models that have postulated two separate affective dimensions to explain these individual differences, centered on the ventral striatum and amygdala circuits, respectively. These findings also demonstrate that brain responses to face expressions are not driven by facial features alone but determined by the personal significance of expressions in current social context. By linking fundamental psychosocial dimensions of adult attachment with brain function, our results do not only corroborate their biological bases but also help understand their impact on behavior.     

Impulsivity and the 5-HTTLPR polymorphism in a non-clinical sample

Background

Impulsivity has been associated with serotonergic system functions. However, few researchers have investigated the relationship between a polymorphism in the promoter of the serotonin transporter gene (5-HTTLPR) and the different components of impulsivity in a non-clinical population. The aim of this study was to investigate the relationship between a polymorphism in the promoter region of the serotonin transporter gene (5-HTTLPR) and the different components of impulsivity in a non-clinical population.

Methodology/Principal Findings

We administered two neuropsychological tests, the Continuous Performance Task and the Iowa Gambling Task, to 127 healthy participants to measure their levels of motor, attentional and non-planning impulsivity. Then, these participants were grouped by genotype and gender, and their scores on impulsivity measures were compared. There were no significant differences between group scores on attentional, motor and non-planning impulsivity.

Conclusions/Significance

Our results suggest that 5-HTTLPR genotype is not significantly associated with subsets of impulsive behavior in a non-clinical sample when measured by neuropsychological tests. These findings are discussed in terms of the sensitivity of neuropsychological tests to detect impulsivity in a non-clinical population and the role of gender and race in the relationship between the 5-HTTLPR and impulsivity.     

Queen Dominance May Reduce Worker Mushroom Body Size in a Social Bee

The mushroom body (MB) is an area of the insect brain involved in learning, memory, and sensory integration. Here, we used the sweat bee Megalopta genalis (Halictidae) to test for differences between queens and workers in the volume of the MB calyces. We used confocal microscopy to measure the volume of the whole brain, MB calyces, optic lobes, and antennal lobes of queens and workers. Queens had larger brains, larger MB calyces, and a larger MB calyces:whole brain ratio than workers, suggesting an effect of social dominance in brain development. This could result from social interactions leading to smaller worker MBs, or larger queen MBs. It could also result from other factors, such as differences in age or sensory experience. To test these explanations, we next compared queens and workers to other groups. We compared newly emerged bees, bees reared in isolation for 10 days, bees initiating new observation nests, and bees initiating new natural nests collected from the field to queens and workers. Queens did not differ from these other groups. We suggest that the effects of queen dominance over workers, rather than differences in age, experience, or reproductive status, are responsible for the queen–worker differences we observed. Worker MB development may be affected by queen aggression directly and/or manipulation of larval nutrition, which is provisioned by the queen. We found no consistent differences in the size of antennal lobes or optic lobes associated with differences in age, experience, reproductive status, or social caste.     

period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type

Changes in circadian rhythms of behavior are related to age-based division of labor in honey bee colonies. The expression of the clock gene period (per) in the bee brain is associated with age-related changes in circadian rhythms of behavior, but previous efforts to firmly associate per brain expression with division of labor or age have produced variable results. We explored whether this variability was due to differences in light and flight experience, which vary with division of labor, or differences in colony environment, which are known to affect honey bee behavioral development. Our results support the hypothesis that per mRNA expression in the bee brain is developmentally regulated. One-day-old bees had the lowest levels of expression and rarely showed evidence of diurnal fluctuation, while foragers and forager-age bees (> 21 days of age) always had high levels of brain per and strong and consistent diurnal patterns. Results from laboratory and field experiments do not support the hypothesis that light, flight experience, and colony type influence per expression. Our results suggest that the rate of developmental elevation in per expression is influenced by factors other than the ones studied in our experiments, and that young bees are more sensitive to these factors than foragers.     

Mathematically gifted adolescents have deficiencies in social valuation and mentalization

Many mathematically gifted adolescents are characterized as being indolent, underachieving and unsuccessful despite their high cognitive ability. This is often due to difficulties with social and emotional development. However, research on social and emotional interactions in gifted adolescents has been limited. The purpose of this study was to observe differences in complex social strategic behaviors between gifted and average adolescents of the same age using the repeated Ultimatum Game. Twenty-two gifted adolescents and 24 average adolescents participated in the Ultimatum Game. Two adolescents participate in the game, one as a proposer and the other as a responder. Because of its simplicity, the Ultimatum Game is an apt tool for investigating complex human emotional and cognitive decision-making in an empirical setting. We observed strategic but socially impaired offers from gifted proposers and lower acceptance rates from gifted responders, resulting in lower total earnings in the Ultimatum Game. Thus, our results indicate that mathematically gifted adolescents have deficiencies in social valuation and mentalization.