Japanese macaques (Macaca fuscata) social development: Sex differences in Juvenile behavior

We have quantitatively documented the development of sex differences in the behavior of juvenile Japanese macaques (1 to 2 years of age). Mothers treated their offspring differently by sex, i.e., mothers of males broke contact with them more frequently than did mothers of females. Juvenile males played more, and mounted other macaques more frequently; juvenile females groomed their mothers more and were also punished by other group members more frequently than were males. Males showed a pattern of decreasing interactions with their mothers, but females increased the frequency of their maternal interactions. These patterns appear to presage the life histories of the sexes. However, comparisons with other species of nonhuman primates indicate that although sex differences in behavior are common, the variability among species severely limits cross-specific generalizations.     

Behavioral Differences of the Insect Morimus funereus (Coleoptera,Cerambycidae) Exposed to an Extremely Low Frequency Magnetic Field

Changes in the behavior of Morimus funereus individuals were investigated as early manifestations of the contact of a living system with a changed environment primarily established via the nervous system. These experiments were aimed at revealing possible behavioral differences of a laboratory population of cerambycid beetle M. funereus in an “open field” before and after exposure to an extremely low frequency magnetic field (ELF‐MF, 50 Hz, 2 mT). The experimental groups were divided into several activity categories and exposed to ELF‐MF. The results showed that the activity increased in the groups with medium and low motor activity, but decreased in highly active individuals. High individual variability was found in the experimental groups, as well as differences in motor activities between the sexes, both before and after exposure to ELF‐MF. According to preliminary results, we assume the changes of activity in both sexes after exposure to ELF‐MF. The results showed a tendency toward locomotor activity decrease, the affect being more pronounced in females. As opposed to this type of activity, stereotypic activity of males was increased after the exposure, whereas females maintained the expected tendency of decrease. However, we did not obtain statistically significant differences because of a high individual variability and a low total number of individuals in the experiment (N = 28). Only a detailed analysis of the locomotor activity at 1‐min intervals showed some statistically significant differences in behavior between the sexes.     

Dominant-subordinate relationships in hamsters: sex differences in reactions to familiar opponents

In the majority of mammalian species, males are dominant over and more aggressive than females. In contrast, some reports suggest that female golden hamsters are more aggressive than males but systematic comparisons using the same methods for both sexes are rare. We observed same-sexed pairs of hamsters over repeated trials to assess whether sex differences existed in the level of agonistic behavior and in the development and maintenance of dominant-subordinate relationships with familiar partners. There were no sex differences in measures of agonistic behavior or fear responses (fleeing) during the initial series of three trials on the first day of testing. Following a four-day interval, males that had lost in session 1 showed fearful responses to a familiar dominant male and were not likely to engage in a fight with him. In contrast, females that lost the initial fights were not fearful and fought vigorously with the familiar winner in subsequent encounters. Although the amount of agonistic behavior engaged in by females did decrease over the course of the three sessions, females that lost did not demonstrate an increase in fear, as measured by the latency to flee. Males that lost fights did show increased fear during later trials and sessions. These results suggest that female hamsters are less affected by losing fights than males are and thus that females are less likely than males to develop highly polarized dominant-subordinate relationships. Further work is needed to understand the mechanisms underlying these sex differences.     

Intranasal administration of testosterone increased immobile-sniffing, exploratory behavior, motor behavior and grooming behavior in rats

Currently, testosterone (T) replacement therapy is typically provided by oral medication, injectable T esters, surgically implanted T pellets, transdermal patches and gels. However, most of these methods of administration are still not ideal for targeting the central nervous system. Recently, therapeutic intranasal T administration (InT) has been considered as another option for delivering T to the brain. In the present study, the effects of 21-day InT treatment were assessed on open field behavior in gonadectomized (GDX) rats and intact rats. Subcutaneous injections of T at same dose were also tested in GDX rats. A total of 12 behavioral events were examined in GDX groups with or without T and in intact groups with or without InT. Significant decreases in open field activity were observed in rats after GDX without InT compared to sham-operated rats. The open field activity scores for most tests significantly increased with InT treatment in GDX rats and in intact rats compared with the corresponding GDX rats and intact rats. Intranasal administration of T improved the reduced behaviors resulted from T deficiency better than subcutaneous injection of T, demonstrating that T can be delivered to the brain by intranasal administration. Our results suggest that intranasal T delivery is an effective option for targeting the central nervous system.     

High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: A model of post-partum stress and possible depression

Post-partum stress and depression (PPD) have a significant effect on child development and behavior. Depression is associated with hypercortisolism in humans, and the fluctuating levels of hormones, including corticosterone, during pregnancy and the post-partum, may contribute to PPD. The present study was developed to investigate the effects of high-level corticosterone (CORT) post-partum in the mother on postnatal neurogenesis and behavior in the offspring. Sprague-Dawley dams were treated with either CORT (40 mg/kg) or sesame oil injections daily for 26 days beginning the day after giving birth. Dams were tested in the forced swim test (FST) and in the open field test (OFT) on days 24-26 post-partum. Results showed that the dams exposed to CORT expressed "depressive-like" behavior compared to controls, with decreased struggling behavior and increased immobility in the FST. To investigate the effects of treatment on hippocampal postnatal cell proliferation and survival in the offspring, males and females from treated dams were injected with BrdU (50 mg/kg) on postnatal day 21 and perfused either 24 h (cell proliferation) or 21 days (cell survival) later. Furthermore, male and female offspring from each litter were tested in adulthood on various behavioral tests, including the forced swim test, open field test, resistance to capture test and elevated plus maze. Intriguingly, male, but not female, offspring of CORT-treated dams exhibited decreased postnatal cell proliferation in the dentate gyrus. Both male and female offspring of CORT-treated dams showed higher resistance to capture and greater locomotor activity as assessed in the open field test. As high levels of CORT may be a characteristic of stress and/or depression, these findings support a model of 'CORT-induced' post-partum stress and possibly depression and demonstrate that the offspring of affected dams can exhibit changes in postnatal neurogenesis and behavior in adulthood.     

Dysregulation of neonatal hippocampal cell genesis in the androgen insensitive Tfm rat

The first two weeks of life are a critical period for hippocampal development. At this time gonadal steroid exposure organizes sex differences in hippocampal sensitivity to activational effects of steroids, hippocampal cell morphology and hippocampus dependent behaviors. Our laboratory has characterized a robust sex difference in neonatal neurogenesis in the hippocampus that is mediated by estradiol. Here, we extend our knowledge of this sex difference by comparing the male and female hippocampus to the androgen insensitive testicular feminized mutant (Tfm) rat. In the neonatal Tfm rat hippocampus, fewer newly generated cells survive compared to males or females. This deficit in cell genesis is partially recovered with the potent androgen DHT, but is more completely recovered following estradiol administration. Tfm rats do not differ from males or females in the level of endogenous estradiol in the neonatal hippocampus, suggesting other mechanisms mediate a differential sensitivity to estradiol in male, female and Tfm hippocampus. We also demonstrate disrupted performance on a hippocampal-dependent contextual fear discrimination task. Tfm rats generalize fear across contexts, and do not exhibit significant loss of fear during extinction exposure. These results extend prior reports of exaggerated response to stress in Tfm rats, and following gonadectomy in normal male rats.     

Is there an effect of prenatal testosterone on aggression and other behavioral traits? A study comparing same-sex and opposite-sex twin girls

Men and women differ in temperament and personality traits, such as aggression and sensation seeking. The sex hormone testosterone could play a role in the origin of these differences, but it remains unclear how and when testosterone could have these effects. One way to investigate the prenatal exposure effect of testosterone is to compare opposite-sex (OS) and same-sex (SS) female twins. It has been suggested that OS twin girls are exposed prenatally to elevated testosterone levels and that this may result in some masculinization of their personality and behavior. We measured sexually dimorphic traits and circulating testosterone levels in 13-year-old OS (n = 74) and SS (n = 55) twins. Testosterone levels showed a clear circadian rhythm, with higher levels in the morning than in the afternoon. Testosterone was higher in boys than girls, but similar in OS and SS twin girls. Testosterone was not in any way systematically related to the different personality traits. However, a sex difference in aggression proneness was observed, and OS girls showed a more masculine pattern of aggression proneness than the SS girls. It is argued that it is unlikely that this difference is due to social factors, such as a gender-specific upbringing.     

Impairment of spatial learning by estradiol treatment in female mice is attenuated by estradiol exposure during development

High doses of estradiol (E(2)) can impair spatial learning in the Morris water maze, in ovariectomized mice, but the same dose has no effect on adult castrated males. Here, we test the hypothesis that this sex difference is caused by neonatal actions of E(2). In Experiment 1, C57BL/6J pups were given daily estradiol benzoate (EB) or oil injections from the day of birth until postnatal Day 3. Adults were gonadectomized and received EB (s.c.) or oil 28 h before the first day of training, and 4 h before each of four daily training sessions on the Morris water maze. Females given oil as neonates, and EB prior to training displayed the poorest performance. Females that received EB as neonates and EB prior to training were insensitive to the deleterious effects of adult EB and performed better than males given the same hormone treatments. We conducted a second experiment using aromatase enzyme knockout (ArKO) mice. Adult male and female ArKO and wild-type (WT) littermates were gonadectomized and received either injections of oil or EB prior to and during water maze training (as described above). Hormone treatment failed to affect performance, yet, female but not male ArKO mice showed impaired learning compared to WT littermates. Thus, exposure to estradiol during neonatal development can counteract the deleterious effects of EB on adult spatial learning.     

Sex hormones, central nervous system and pain

The aim of the present review, which highlights some relationships between sex hormones, the CNS and pain, is to provide reference points for discussion on one of the most intriguing aspects of pain pathophysiology: the presence of sex differences in the response threshold to phasic painful stimuli and in the incidence of chronic pain syndromes. The first part of the review deals with sex steroids and their mechanisms of action. In the second part, the connections between sex steroids, the CNS and pain are illustrated to introduce possible areas of discussion in the study of sex differences in experimental and clinical pain.     

Homebase behavior of zebrafish in novelty-based paradigms

Zebrafish (Danio rerio) are emerging as a promising model species in neuroscience research. Many traditional rodent behavioral paradigms may be adapted for zebrafish testing. Exposing zebrafish to three different “open field” tanks for 30 min, we showed that fish display robust homebase behavior, in which one area of the tank is chosen as a preferred point of reference during the test, which the fish frequently return to and spend a longer duration in. This phenotype strikingly resembles rodent homebase behavior, confirming that both species use homebases as “reference points” for their exploration. Our study introduces a simple method for zebrafish homebase phenotyping, and further supports the utility of these fish in neurobehavioral and cognitive research.     

Applying Stereotactic Injection Technique to Study Genetic Effects on Animal Behaviors

Stereotactic injection is a useful technique to deliver high titer lentiviruses to targeted brain areas in mice. Lentiviruses can either overexpress or knockdown gene expression in a relatively focused region without significant damage to the brain tissue. After recovery, the injected mouse can be tested on various behavioral tasks such as the Open Field Test (OFT) and the Forced Swim Test (FST). The OFT is designed to assess locomotion and the anxious phenotype in mice by measuring the amount of time that a mouse spends in the center of a novel open field. A more anxious mouse will spend significantly less time in the center of the novel field compared to controls. The FST assesses the anti-depressive phenotype by quantifying the amount of time that mice spend immobile when placed into a bucket of water. A mouse with an anti-depressive phenotype will spend significantly less time immobile compared to control animals. The goal of this protocol is to use the stereotactic injection of a lentivirus in conjunction with behavioral tests to assess how genetic factors modulate animal behaviors.     

Estrogens and relationship jealousy

The relation between sex hormones and responses to partner infidelity was explored in two studies reported here. The first confirmed the standard sex difference in relationship jealousy, that males (n=133) are relatively more distressed by a partner’s sexual infidelity and females (n=159) by a partner’s emotional infidelity. The study also revealed that females using hormone-based birth control (n=61) tended more toward sexual jealousy than did other females, and reported more intense affective responses to partner infidelity (n=77). In study two, 47 females were assessed four times across one month. Patterns of response to partner infidelity did not vary by week of menstrual cycle, but significant relations between salivary estradiol level and jealousy responses were obtained during the time of rising and high fertility risk. The implications, at least for females, are that any evolved psychological, affective, or behavioral dispositions regarding reproduction-related relationships are potentially moderated by estradiol, and that the use of synthetic hormones may disrupt this relation. David C. Geary is the Frederick A. Middlebush Professor of Psychological Sciences at the University of Missouri at Columbia. He has published nearly 100 articles and chapters across a wide range of topics, including cognitive and developmental psychology, education, evolutionary biology, and medicine. His two books, Children’s Mathematical Development (1984) and Male, Female: The Evolution of Human Sex Differences (1988), have been published by the American Psychological Association. M. Catherine DeSoto recently completed her Ph.D. in psychological sciences at the University of Missouri at Columbia and is currently assistant professor of psychobiology at the University of Northern Iowa. Her research primarily focuses on the interface between biology and behavior, including the relation between sex hormones and personality disorders. Mary K. Hoard is completing her Ph.D. studies in psychological sciences at the University of Missouri at Columbia and is currently a research specialist in the Department of Psychological Sciences. Her research interests focus on children’s cognitive development, as well as the relation between sleep and cognitive and psychological functioning. Melanie Skaggs Sheldon is a graduate student in the Department of Psychological Sciences at the University of Missouri at Columbia. Her research interests include social cooperation, sexual behavior, and personality, as understood from an evolutionary perspective. M. Lynne Cooper is a professor of psychological sciences and director of the training program in social psychology at the University of Missouri at Columbia. She is an associate editor of the Journal of Personality and the author of more than 60 articles and chapters in the areas of personality and social psychology. Her primary research efforts involve directing a longitudinal study of risky sexual behavior of adolescents and young adults.     

The emergence of gonadal hormone influences on dopaminergic function during puberty

Adolescence is the developmental epoch during which children become adults—intellectually, physically, hormonally and socially. Brain development in critical areas is ongoing. Adolescents are risk-taking and novelty-seeking and they weigh positive experiences more heavily and negative experiences less than adults. This inherent behavioral bias can lead to risky behaviors like drug taking. Most drug addictions start during adolescence and early drug-taking is associated with an increased rate of drug abuse and dependence.The hormonal changes of puberty contribute to physical, emotional, intellectual and social changes during adolescence. These hormonal events do not just cause maturation of reproductive function and the emergence of secondary sex characteristics. They contribute to the appearance of sex differences in non-reproductive behaviors as well. Sex differences in drug use behaviors are among the latter. The male predominance in overall drug use appears by the end of adolescence, while girls develop the rapid progression from first use to dependence (telescoping) that represent a female-biased vulnerability. Sex differences in many behaviors including drug use have been attributed to social and cultural factors. A narrowing gap in drug use between adolescent boys and girls supports this thesis. However, some sex differences in addiction vulnerability reflect biologic differences in brain circuits involved in addiction. The purpose of this review is to summarize the contribution of sex differences in the function of ascending dopamine systems that are critical to reinforcement, to briefly summarize the behavioral, neurochemical and anatomical changes in brain dopaminergic functions related to addiction that occur during adolescence and to present new findings about the emergence of sex differences in dopaminergic function during adolescence.     

Evaluating the twin testosterone transfer hypothesis: a review of the empirical evidence

In this paper we review the evidence that fetuses gestated with a male co-twin are masculinized in development, perhaps due to the influence of prenatal androgens: the so-called twin testosterone transfer (TTT) hypothesis. Evidence from studies of behavioral, perceptual, cognitive, morphological and physiological traits in same- and opposite-sex human twins is considered. Apart from two studies reporting increases in aspects of sensation-seeking for females with a male rather than a female co-twin, there is sparse evidence supporting the TTT hypothesis in behavioral studies. Outcomes from studies of perception (in particular otoacoustic emissions) and cognition (in particular vocabulary acquisition and visuo-spatial ability) provide more consistent evidence in support of masculinized performance in twins with a male co-twin compared to twins with a female co-twin. The outcomes favorable to the TTT hypothesis for otoacoustic emissions and visuo-spatial ability are restricted to females. Studies of physiology and morphology (e.g., brain volume, tooth size and 2D:4D ratio) also show some influence of co-twin sex, but again these effects are often restricted to female twins. Because females produce little endogenous testosterone, the effects of gestation with a male co-twin may be more pronounced in females than males. Thus, while uneven, the evidence for the TTT hypothesis is sufficient to warrant further investigation, ideally using large samples of same- and opposite-sex twins, along with control groups of same- and opposite-sex siblings when the characteristics assessed are potentially open to social influences.     

Estrogens influence behavioral responses in a kainic acid model of neurotoxicity

The behavioral and neuroprotective effects of 17beta-estradiol (E2), on ovariectomized rats treated with a subconvulsive dose (7 mg/kg bw, ip) of kainic acid (KA), were examined. Estradiol was administered either acutely (150 mug/rat, ip) along with KA, 14 days post-ovariectomy, or chronically (sc capsules providing proestrus estrogen levels in serum) starting at ovariectomy. Exploratory behavior, as deduced by sniffing in the open field test, was reduced in KA-treated rats. Both hormonal schemes partially restored sniffing behavior in KA-lesioned subjects. Moreover, acute and chronic E2 administration in KA-treated rats resulted in increased vertical and horizontal activity of these animals in the open field test. Memory for object recognition was reduced following KA and was not restored by hormonal treatments. Acute, but not chronic, E2 coadministration with KA significantly impaired spatial performance in the water maze task, while KA alone had no effect. Both acute and chronic estradiol administration rescued hilar and CA1 neurons from KA-induced cell death. Chronic, but not acute, E2 increased neurofilament immunoreactivity in the mossy fibers of the dentate gyrus neurons, similarly to KA. Our results show that although estradiol administration in KA-treated rats has beneficial effects on cell survival, it has diverse effects on exploratory behavior, object, and spatial memory. Estradiol effects on KA-lesioned animals depended on the duration and timing of exposure to the hormone, implying different mechanisms of hormone actions.     

An RFLP linkage map of Lycopersicon peruvianum

In order to map genes determining resistance to bacterial canker in tomato, backcrosses were made between a resistant and a susceptible Lycopersicon peruvianum accession. The linkage study with RFLP markers yielded a genetic map of L. Peruvianum. This map was compared to that derived from a L. esculentum x L. pennellii F₂ population, based on 70 shared RFLP markers. The maps showed a good resemblance in both the order of markers and the length of the chromosomes, with the exception of just one relocated marker on chromosome 9. Because backcrosses were made with the F₁, either as the pollen parent or as the pistil parent, linkage maps from male and female meioses could be estimated. It was concluded that recombination at male meiosis was reduced, and that gametophytic selection for parental genotypes at more than one locus per chromosome might be partly responsible for the reduction of the estimated male map length.