Between- and within-person effects of stress on emotional eating in women: a longitudinal study over 49 days.

BACKGROUND: Stress is associated with binge eating and emotional eating (EE) cross-sectionally. However, few studies have examined stress longitudinally, limiting understanding of how within-person fluctuations in stress influence EE over time and whether stress is a risk factor or consequence of EE. Additionally, little is known regarding how the biological stress response relates to EE. METHODS: We used an intensive, longitudinal design to examine between-person and within-person effects of major life stress, daily stress, and cortisol on EE in a population-based sample of women (N = 477; ages 15-30; M = 21.8; s.d. = 3.0) from the Michigan State University Twin Registry. Participants reported past year major life stress, then provided daily ratings of EE and stress for 49 consecutive days. Hair cortisol concentration (HCC) was collected as a longitudinal biological stress measure. RESULTS: Women reported greater EE when they experienced greater mean stress across days (between-person effects) or greater stress relative to their own average on a given day (within-person effects). Daily stress was more strongly associated with EE than major life stress. However, the impact of daily stress on EE was amplified in women with greater past year major life stress. Finally, participants with lower HCC had increased EE. CONCLUSIONS: Findings confirm longitudinal associations between stress and EE in women, and highlight the importance of within-person shifts in stress in EE risk. Results also highlight HCC as a novel biological stress measure that is significantly associated with EE and may overcome limitations of prior physiological stress response indicators.

Ovarian Hormones and Reward Processes in Palatable Food Intake and Binge Eating.

Ovarian hormones are associated with risk for binge eating in women. Recent animal and human studies suggest that food-related reward processing may be one set of neurobiological factors that contribute to these relationships, but additional studies are needed to confirm and extend findings.

Gonadal Hormone Influences on Sex Differences in Binge Eating Across Development.

PURPOSE OF REVIEW: Binge eating is a transdiagnostic symptom that disproportionately affects females. Sexually dimorphic gonadal hormones (e.g., estradiol, testosterone) substantially impact eating behavior and may contribute to sex differences in binge eating. We examine recent evidence for the role of gonadal hormones in binge eating risk across development. RECENT FINDINGS: Both organizational (long-lasting impact on the central nervous system (CNS)) and activational (transient influences on the CNS) hormone effects may contribute to sex differences in binge eating. Gonadal hormones also impact within-sex variability in binge eating, with higher estradiol levels in females and higher testosterone levels in males protective across development. Emerging evidence suggests that the impact of gonadal hormones may be greatest for people with other risk factors, including genetic, temperamental (e.g., high negative affect), and psychosocial (e.g., exposure to weight-based teasing) risk. Gonadal hormones contribute to sex differences and within-sex variability in binge eating across development.

Low testosterone is associated with dysregulated eating symptoms in young adult men.

OBJECTIVE: Extant animal and human data indicate that natural variation in circulating levels of testosterone may contribute to differential risk for dysregulated eating among males. Indeed, testosterone ablation in postpubertal male rodents results in stimulatory effects on sweet-taste preferences, and lower levels of circulating testosterone in adolescent boys have been found to predict dysregulated eating symptoms during mid-to-late puberty. Nonetheless, no prior study has examined whether lower testosterone is associated with dysregulated eating in adulthood. The current study examined this possibility. METHOD: Participants were 154 young adult men (ages = 18-33) from a large Southwestern University. The Eating Disorder Examination Questionnaire, Eating Pathology Symptoms Inventory, and Loss of Control Over Eating Scale were used to assess three types of dysregulated eating symptoms: eating concerns, binge eating, and loss-of-control eating. Afternoon saliva samples were assayed for testosterone using high-sensitive enzyme immunoassays. RESULTS: Consistent with animal data and prior research in adolescent boys, men with lower testosterone reported significantly higher levels of dysregulated eating symptoms even after controlling for depressive symptoms, body mass index, and age. DISCUSSION: Lower testosterone concentrations might serve as a sex-specific biological factor that contributes to dysregulated eating among men.

Associations between ovarian hormones and emotional eating across the menstrual cycle: Do ovulatory shifts in hormones matter?

OBJECTIVE: Elevated ovarian hormone levels are associated with increased risk for binge eating (BE) and emotional eating (EE) during the midluteal phase of the menstrual cycle. However, past studies have not examined whether pronounced hormonal changes that precede the midluteal phase (i.e., the dramatic decrease in estradiol and increase in progesterone during/after ovulation) also influence midluteal increases in binge-related symptoms. Past theories and studies of phenotypes strongly related to BE (e.g., depression) suggest that these pronounced hormonal changes may also contribute. This study examined this possibility in 375 female twins (aged 15-25 years) from the Michigan State University Twin Registry. METHODS: Daily ratings of EE (assessed with the Dutch Eating Behavior Questionnaire) and daily saliva samples of estradiol and progesterone were collected for 45 consecutive days. RESULTS: No significant associations were found between pronounced changes in estradiol or progesterone across ovulation and changes in EE scores in the midluteal phase. Results remained unchanged after controlling for body mass index and negative affect and examining participants with clinical BE episodes or more extreme hormonal fluctuations. DISCUSSION: In aggregate, the current findings and past data suggest that hormone levels are more significant predictors of EE than pronounced hormonal changes across the menstrual cycle.

Exploring reward system responsivity in the nucleus accumbens across chronicity of binge eating in female rats.

OBJECTIVE: Research has highlighted the importance of reward-based processes in binge eating (BE). However, both increased and decreased activation have been observed in reward related brain regions for BE. Differences may be similar to addiction research, where the reward system is initially hyper-responsive at early stages of use, but becomes hypo-responsive with prolonged drug/alcohol use. This study was the first to examine differences in reward system responsivity at early versus chronic BE stages. METHOD: Using an animal model, Sprague-Dawley female rats were identified as BE prone (BEP) or BE resistant (BER) and randomly assigned to an early or chronic stage group. Neural activation (via Fos protein) was quantified in the nucleus accumbens core (NAC) and shell (NAS). RESULTS: Early stage BEP rats had the highest levels of Fos expression of all of the study groups. By contrast, chronic stage BEP rats exhibited decreased activation in the NAS and NAC that was similar to the activation in chronic stage BER rats. DISCUSSION: Findings are significant in suggesting hyper-neural activation to reward in the early stages of BE and decreased activation in later stages of BE. Additional studies are needed to elucidate how these differences may impact risk for and maintenance of BE.

Sex Differences in Binge Eating: Gonadal Hormone Effects Across Development.

Eating disorders are highly sexually differentiated disorders that exhibit a female predominance in risk. Most theories focus on psychosocial explanations to the exclusion of biological/genetic influences. The purpose of this descriptive review is to evaluate evidence from animal and human studies in support of gonadal hormone effects on sex differences in binge eating. Although research is in its nascent stages, findings suggest that increased prenatal testosterone exposure in males appears to protect against binge eating. Although pubertal testosterone may exert additional protective effects, the prenatal period is likely critical for the decreased risk observed in males. By contrast, studies indicate that, in females, it is the lack of prenatal testosterone coupled with the organizational effects of pubertal ovarian hormones that may lead to increased binge eating. Finally, twin data suggest that changes in genetic risk may underlie these hormone influences on sex differences across development.

Pubertal pair-housing facilitates adult sexual behavior in male rats.

This study examined the effects of pubertal testosterone (T) and social housing manipulations on male sexual behavior in adult rats. Prepubertal rats were castrated at 21 days of age (P21) and implanted with either blank or T-releasing pellets. At the onset of puberty, P28, half the rats in each treatment group were either single- or pair-housed with a male of the same hormone condition through P56, at which time pellets were removed and all rats were single-housed. In adulthood (P84), all rats received T replacement and were tested for sexual behavior. Rats pair-housed during adolescence showed more sexual behavior and greater improvement of sexual performance over repeated tests than single-housed rats, regardless of pubertal T status. Pubertal T, however, did facilitate the frequency of anogenital investigation. Thus, in male rats, social interactions during adolescence are more important than exposure to pubertal T in enhancing adult sexual behavior.

Pubertally born neurons and glia are functionally integrated into limbic and hypothalamic circuits of the male Syrian hamster.

During puberty, the brain goes through extensive remodeling, involving the addition of new neurons and glia to brain regions beyond the canonical neurogenic regions (i.e., dentate gyrus and olfactory bulb), including limbic and hypothalamic cell groups associated with sex-typical behavior. Whether these pubertally born cells become functionally integrated into neural circuits remains unknown. To address this question, we gave male Syrian hamsters daily injections of the cell birthdate marker bromodeoxyuridine throughout puberty (postnatal day 28-49). Half of the animals were housed in enriched environments with access to a running wheel to determine whether enrichment increased the survival of pubertally born cells compared with the control environment. At 4 wk after the last BrdU injection, animals were allowed to interact with a receptive female and were then killed 1 h later. Triple-label immunofluorescence for BrdU, the mature neuron marker neuronal nuclear antigen, and the astrocytic marker glial fibrillary acidic protein revealed that a proportion of pubertally born cells in the medial preoptic area, arcuate nucleus, and medial amygdala differentiate into either mature neurons or astrocytes. Double-label immunofluorescence for BrdU and the protein Fos revealed that a subset of pubertally born cells in these regions is activated during sociosexual behavior, indicative of their functional incorporation into neural circuits. Enrichment affected the survival and activation of pubertally born cells in a brain region-specific manner. These results demonstrate that pubertally born cells located outside of the traditional neurogenic regions differentiate into neurons and glia and become functionally incorporated into neural circuits that subserve sex-typical behaviors.

Examining associations between negative urgency and key components of objective binge episodes.

OBJECTIVE: Negative urgency (NU; tendency to act impulsively when experiencing negative emotions) is a risk factor for binge eating, although few studies have examined interviewer-assessed objective binge episodes (OBEs). Moreover, research has not investigated how NU relates to the core components of OBEs: loss of control (LOC) eating and objective overeating (OO). Understanding the relationship between NU and these core components will enhance etiologic models of eating disorder development. Thus, the current study examined the associations between NU, OBEs, and the components of OBEs by comparing levels of NU in women with OBEs, LOC eating only, and OO only to women with no pathological eating. METHOD: Participants were 612 women who endorsed lifetime OBEs (5.4%), LOC eating outside of OBEs (5.7%), OO only (2.8%), or none of these eating episodes (85.9%). RESULTS: Women with OBEs, LOC only, and OO only had significantly higher levels of NU than women without these episodes, suggesting that NU is associated with both the LOC and OO components of OBEs. DISCUSSION: NU relates to the spectrum of pathology present in women with OBEs. Future research should examine the mechanisms underlying these associations, including impaired behavioral/psychological control and/or increased reward sensitivity in response to negative affect.

The effects of ovarian hormones and emotional eating on changes in weight preoccupation across the menstrual cycle.

OBJECTIVE: Previous research has shown that fluctuations in ovarian hormones (i.e., estradiol and progesterone) predict the changes in binge eating and emotional eating across the menstrual cycle. However, the extent to which other eating disorder symptoms fluctuate across the menstrual cycle and are influenced by ovarian hormones remains largely unknown. This study sought to examine whether the levels of weight preoccupation vary across the menstrual cycle and whether the changes in ovarian hormones and/or other factors (i.e., emotional eating and negative affect) account for menstrual cycle fluctuations in this eating disorder phenotype. METHOD: For 45 consecutive days, 352 women (age, 15-25 years) provided daily ratings of weight preoccupation, negative affect, and emotional eating. Saliva samples were also collected on a daily basis and assayed for levels of estradiol and progesterone using enzyme immunoassay techniques. RESULTS: Weight preoccupation varied significantly across the menstrual cycle, with the highest levels in the premenstrual and menstrual phases. However, ovarian hormones did not account for within-person changes in weight preoccupation across the menstrual cycle. Instead, the most significant predictor of menstrual cycle changes in weight preoccupation was the change in emotional eating. DISCUSSION: Fluctuations in weight preoccupation across the menstrual cycle appear to be influenced primarily by emotional eating rather than ovarian hormones. Future research should continue to examine the relationships among ovarian hormones, weight preoccupation, emotional eating, and other core eating disorder symptoms (e.g., body dissatisfaction, compensatory behaviors) in an effort to more fully understand the role of these biological and behavioral factors for the full spectrum of eating pathology.

Primary amenorrhea in anorexia nervosa: impact on characteristic masculine and feminine traits.

Animal studies indicate that gonadal hormones at puberty have an effect on the development of masculine and feminine traits. However, it is unknown whether similar processes occur in humans. We examined whether women with anorexia nervosa (AN), who often experience primary amenorrhea, exhibit attenuated feminization in their psychological characteristics in adulthood due to the decrease/absence of gonadal hormones at puberty. Women with AN were compared on a number of psychological characteristics using general linear models on the basis of the presence/absence of primary amenorrhea. Although women with primary amenorrhea exhibited lower anxiety scores than those without primary amenorrhea, in general, results did not provide evidence of attenuated feminization in women with AN with primary amenorrhea. Future research should utilize novel techniques and direct hormone measurement to explore the effects of pubertal gonadal hormones on masculine and feminine traits.

Adolescent gain in positive valence of a socially relevant stimulus: engagement of the mesocorticolimbic reward circuitry.

A successful transition from childhood to adulthood requires adolescent maturation of social information processing. The neurobiological underpinnings of this maturational process remain elusive. This research employed the male Syrian hamster as a tractable animal model for investigating the neural circuitry involved in this critical transition. In this species, adult and juvenile males display different behavioral and neural responses to vaginal secretions, which contain pheromones essential for expression of sexual behavior in adulthood. These studies tested the hypothesis that vaginal secretions acquire positive valence over adolescent development via remodeling of neural circuits underlying sexual reward. Sexually naïve adult, but not juvenile, hamsters showed a conditioned place preference for vaginal secretions. Differences in behavioral response to vaginal secretions between juveniles and adults correlated with a difference in the vaginal secretion-induced neural activation pattern in mesocorticolimbic reward circuitry. Fos immunoreactivity increased in response to vaginal secretions in the medial amygdala and ventral tegmental dopaminergic cells of both juvenile and adult males. However, only in adults was there a Fos response to vaginal secretions in non-dopaminergic cells in interfascicular ventral tegmental area, nucleus accumbens core and infralimbic medial prefrontal cortex. These results demonstrate that a socially relevant chemosensory stimulus acquires the status of an unconditioned reward during adolescence, and that this adolescent gain in social reward is correlated with experience-independent engagement of specific cell groups in reward circuitry.

Sexual differentiation of the adolescent rodent brain: hormonal influences and developmental mechanisms.

This article is part of a Special Issue "Puberty and Adolescence". Sexual differentiation is the process by which the nervous system becomes structurally and functionally dissimilar in females and males. In mammals, this process has been thought to occur during prenatal and early postnatal development, when a transient increase in testosterone secretion masculinizes and defeminizes the developing male nervous system. Decades of research have led to the views that structural sexual dimorphisms created during perinatal development are passively maintained throughout life, and that ovarian hormones do not play an active role in feminization of the nervous system. Furthermore, perinatal testosterone was thought to determine sex differences in neuron number by regulating cell death and cell survival, and not by regulating cell proliferation. As investigations of neural development during adolescence became more prominent in the late 20th century and revealed the extent of brain remodeling during this time, each of these tenets has been challenged and modified. Here we review evidence from the animal literature that 1) the brain is further sexually differentiated during puberty and adolescence; 2) ovarian hormones play an active role in the feminization of the brain during puberty; and 3) hormonally modulated, sex-specific addition of new neurons and glial cells, as well as loss of neurons, contribute to sexual differentiation of hypothalamic, limbic, and cortical regions during adolescence. This architectural remodeling during the adolescent phase of sexual differentiation of the brain may underlie the known sex differences in vulnerability to addiction and psychiatric disorders that emerge during this developmental period.

Sex differences in binge eating patterns in male and female adult rats.

OBJECTIVE: Several efforts are underway to model binge eating in animals in order to advance neurobiological models of risk. However, knowledge of sex differences in these models is currently lacking. The goal of the present study was to examine sex differences in binge eating phenotypes using a well-established rodent model (i.e., the binge eating resistant/binge eating prone model). METHOD: Thirty male and 30 female adult Sprague-Dawley rats were exposed to feeding tests consisting of intermittent access to palatable food (PF). Rats were then categorized as binge eating prone (BEP) based on the amount and consistency of PF consumption across tests. RESULTS: Across multiple methods for BEP classification, rates of BEP phenotypes were two to six times higher in female than male rats. DISCUSSION: Findings provide support for sex differences in rodent models of binge eating and highlight the promise of the BER/BEP model for understanding neurobiological mechanisms underlying sex differences in risk.

Ovarian hormones and emotional eating associations across the menstrual cycle: an examination of the potential moderating effects of body mass index and dietary restraint.

OBJECTIVE: Associations between within-person changes in ovarian hormones and dysregulated eating (binge eating, emotional eating) have been observed across the menstrual cycle. However, studies have not examined moderators that may contribute to differential associations between individuals. We investigated body-weight regulation variables [body mass index (BMI), dietary restraint] that have theoretical relevance by virtue of their associations with both phenotypes. METHOD: Women (N = 196) provided emotional eating ratings and saliva samples for 45 days. BMI and restraint were assessed at three time points and averaged. RESULTS: Results showed significant estradiol × progesterone interactions in the prediction of within-subject changes in emotional eating. Neither BMI nor restraint moderated these relationships, although a trend-level dietary restraint × estradiol interaction was observed where estradiol's effects were enhanced in high restraint scorers. DISCUSSION: Findings confirm a role for hormones in changes in emotional eating and suggest that restraint might enhance hormone effects in severegroups.

Ovarian Hormones and Binge Eating in Adulthood: Summary of Findings and Implications for Individual Differences in Risk in Women.

Ovarian hormone influences on general food intake have been studied in animals for 60+ years. Yet, extensions of these data to key eating disorder symptoms in humans (e.g., binge eating (BE)) have only recently occurred. In this article, we summarize findings from studies examining the effects of ovarian hormones on BE. Findings suggest ovarian hormones contribute to BE in animals and humans, although studies are few in number, and effects are not present in all women or all animals exposed to high-risk hormonal milieus. Differences in susceptibility may be due to gene x hormone interactions that can explain why some, but not all, women/females develop BE in the presence of risky hormonal environments.

The organizational role of ovarian hormones during puberty on risk for binge-like eating in rats.

Puberty is a high-risk period for the development of dysregulated eating, including binge eating. While risk for binge eating in animals and humans increases in both males and females during puberty, the increased prevalence is significantly greater in females. Emerging data suggest that the organizational effects of gonadal hormones may contribute to the female preponderance of binge eating. In this narrative review, we discuss studies conducted in animals that have examined these organizational effects as well as the neural systems that may serve as intermediary mechanisms. Relatively few studies have been conducted, but data thus far suggest that pubertal estrogens may organize risk for binge eating, potentially by altering key circuits in brain reward pathways. These promising results highlight the need for future studies to directly test organizational effects of pubertal hormones using hormone replacement techniques and circuit-level manipulations that can identify pathways contributing to binge eating across development.

Maturation of social reward in adult male Syrian hamsters does not depend on organizational effects of pubertal testosterone.

The rewarding value of female sexual stimuli develops across puberty, as sexually-naïve adult, but not prepubertal, male hamsters show a conditioned place preference (CPP) for both vaginal secretions and a receptive female. Similarly, only adults show an endogenous testosterone surge when they encounter vaginal secretions. Testosterone by itself can condition a place preference in male rodents. Therefore, Experiment 1 assessed whether the endogenous testosterone surge elicited by vaginal secretions is necessary to show a CPP. Both gonad-intact and gonadectomized, testosterone-treated adult males showed a CPP for vaginal secretions, indicating that the rewarding value of this social cue is independent of an endogenous testosterone surge. However, organizational effects of pubertal testosterone could be necessary for adolescent development of social reward, as pubertal testosterone organizes adult-typical expression of sexual behavior. To investigate this possibility, in Experiment 2, sexually-naïve prepubertal and adult male hamsters were gonadectomized and received testosterone-filled capsules four weeks later. Testing began after two weeks of testosterone replacement. Adult males showed a CPP for both vaginal secretions and a receptive female, whether or not they experienced pubertal testosterone. Thus, the acquisition of positive valence of sexual stimuli is not organized by pubertal testosterone. Taken together, the ability of female sexual stimuli to serve as an unconditioned reward to adult male hamsters is independent of the chemosensory-induced endogenous testosterone surge and also organizational effects of pubertal testosterone. Instead, sexual reward may be dependent either on activational effects of testosterone or gonadal hormone-independent mechanisms.

Differential associations between ovarian hormones and disordered eating symptoms across the menstrual cycle in women.

OBJECTIVE: We examined changes in drive for thinness, body dissatisfaction, and dietary restraint across the menstrual cycle and associations between these symptoms and ovarian hormones in two independent samples of women (N = 10 and 8 women, respectively) drawn from the community. METHOD: Daily self-report measures of disordered eating and negative affect were completed for 35-65 days. Daily saliva samples were assayed for estradiol and progesterone in Study 2 only. RESULTS: Levels of body dissatisfaction and drive for thinness were highest during the mid-luteal/pre-menstrual phases in both studies and were negatively associated with estradiol, and positively associated with progesterone. By contrast, dietary restraint showed less variation across the menstrual cycle and weaker associations with ovarian hormones. DISCUSSION: Differential associations between ovarian hormones and specific disordered eating symptoms point to distinct etiological processes within the broader construct of disordered eating.