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.

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.

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.

Sex differences in proliferation and attrition of pubertally born cells in the rat posterior dorsal medial amygdala.

The rodent posterodorsal medial amygdala (MePD) evaluates and assigns valence to social sensory stimuli. The perception of social stimuli evolves during puberty, when the focus of social interactions shifts from kin to peers. Using the cell birthdate marker bromo-deoxyuridine (BrdU), we previously discovered that more pubertally born cells are added to the rat MePD in males than females. Here we addressed several questions that remained unanswered by our previous work. First, to determine whether there are sex differences in cell proliferation within the MePD, we examined BrdU-immunoreactive (-ir) cells at 2 and 4 h following BrdU administration on postnatal day 30 (P30). The density of BrdU-ir cells was greater in males than in females, indicating greater proliferation in males. Proliferation was substantiated by double-label immunohistochemistry showing that MePD BrdU-ir cells colocalize proliferating cell nuclear antigen, but not the cell death marker Caspase3. We next studied longer time points (2-21 days) following BrdU administration on P30 and found that the rate of cell attrition is higher in males. Finally, triple-label immunohistochemistry of P30-born MePD cells revealed that some of these cells differentiate into neurons or astrocytes within three weeks of cell birth, with no discernable sex differences. The demonstration of pubertal neuro- and glio-genesis in the MePD of male and female rats adds a new dimension to developmental plasticity of the MePD that may contribute to pubertal changes in the perception of social stimuli in both sexes.

The effects of the COVID-19 pandemic on disordered eating symptoms in women: A 49-day, daily study before and during the outbreak in the United States.

Longitudinal data are needed to examine effects of the COVID-19 pandemic on disordered eating. We capitalized on an ongoing, longitudinal study collecting daily data to examine changes in disordered eating symptoms in women across 49 days that spanned the time before and during the COVID-19 outbreak in the United States. Women from the Michigan State University Twin Registry (N = 402) completed daily questionnaires assessing a range of symptoms (e.g., binge eating, weight/shape concerns, liking/wanting of palatable food (PF) and whole foods, hunger). Dates of the first US COVID-19 case, first case in each participant's state, and onset of the initial stay-at-home orders (SHOs) were used to categorize women into those who completed all daily assessments prior to, during, or after these dates. We used mixed linear models and specification-curve analysis to examine between-person (i.e., differences between women assessed before vs during/after COVID-19) and within-person (i.e., changes in symptoms from days before to days after the dates) effects of the pandemic. Results showed significantly higher levels of binge-related pathology (e.g., odds of binge eating, liking/wanting of PF) in women who completed assessments during/after COVID-19 events, and significantly increased liking/wanting of PF in the days following the pandemic onset. By contrast, minimal between- or within-person differences were observed for other variables, including weight/shape concerns, compensatory behaviors, hunger, or liking/wanting whole foods. Overall, results suggest a specific effect of the pandemic on binge-related phenotypes in women. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Pubertal Emergence of Testosterone Effects on Depressive Symptoms in Boys.

Background: Puberty-driven increases in the secretion of testosterone may be a biological factor that protects males against the development of depression. Although all males produce testosterone, there are substantial between-person differences that could contribute to differential vulnerability to depression among pre-adolescent and adolescent boys, particularly after pubertal onset. Indeed, experimental animal and human data have shown that low testosterone increases risk for depressive-like symptoms in males, whereas higher levels of testosterone may be protective; however, prior studies have primarily investigated these effects in adulthood. This study investigated whether lower circulating levels of testosterone predict depressive symptoms in pre-adolescent and adolescent boys, and in particular, whether the testosterone-depression association becomes prominent with advancing pubertal maturation. Methods: Male twins (N = 213; ages 10-15 years) from the Michigan State University Twin Registry self-reported their depressive symptoms and pubertal status using the Children's Depression Inventory and the Pubertal Development Scale, respectively. Salivary testosterone was assayed using high-sensitivity enzyme immunoassays. Mixed Linear Models (MLMs), which could account for the non-independence of twin data, were used for analyses. Results: As expected, lower testosterone concentrations were associated with higher depressive symptoms, and the magnitude of this effect increased with advancing pubertal status. In contrast, boys with higher levels of testosterone showed low levels of depressive symptomatology at all stages of pubertal maturation. Conclusions: Overall, these findings enhance understanding of within-sex variability in risk for depression in boys - average-to-high testosterone levels may underlie the general male resilience to depression after pubertal onset, whereas lower levels may increase vulnerability during/after puberty.

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.

Trait negative affect interacts with ovarian hormones to predict risk for emotional eating.

Ovarian hormones significantly influence dysregulated eating in females. However, most women do not develop appreciable disordered eating, suggesting that ovarian hormones may not affect all women equally. We examined whether individual differences in trait negative affect (NA) moderate ovarian hormone-dysregulated eating associations in 446 women who provided saliva samples for hormone measurements and ratings of NA and emotional eating daily for 45 consecutive days. Women were at greatest risk for emotional eating when they had high trait NA and experienced a hormonal milieu characterized by low estradiol or high progesterone. While effects were evident in all women, the combination of high trait NA and high progesterone was particularly risky for women with a history of clinically significant binge eating episodes. These findings provide initial evidence that affective and hormonal risk interact to promote emotional eating, and that effects may be amplified in women with clinically significant binge eating.

The effects of puberty and ovarian hormone removal on developmental trajectories of palatable food and chow intake in female rats.

OBJECTIVE: Palatable food (PF) intake is significantly greater in females than males and increases during adolescence. Previous data suggest that puberty and ovarian hormones may contribute to these sex and developmental differences, but few studies have examined this possibility. The aim of the current study was to address these gaps by examining trajectories of PF and chow intake during pre-puberty, puberty, and adulthood in intact female rats (Study 1) as well as in those receiving pre-pubertal ovariectomies (P-OVX) (Study 2). METHOD: We examined our study aims using archival data from 66 intact Sprague-Dawley female rats (Study 1) and 77 P-OVX and 79 intact Sprague-Dawley female rats (Study 2). PF and chow intake were measured using a free-choice, intermittent exposure paradigm in which rats were exposed to both food types starting in pre-puberty and continuing into adulthood. RESULTS: Mixed linear models revealed a specific effect of puberty on PF intake in both studies. PF intake increased substantially during puberty in all rats, but increases were particularly pronounced in P-OVX rats in Study 2. By contrast, chow intake increased significantly during pre-puberty (rather than puberty) in both studies, and these increases were relatively unaffected by P-OVX. DISCUSSION: Findings confirm a specific effect of puberty and ovarian hormone removal on PF intake in female rats. Differential trajectories of PF versus chow intake highlight potential reward-based processes in pubertal and ovarian hormone effects on PF intake in females.

A Narrative Review of Sex Differences in Eating Disorders: Is There a Biological Basis?

PURPOSE: Eating disorders and their core symptoms (eg, binge eating, body weight/shape concerns) disproportionately affect females, and these sex-differentiated effects become prominent during and after puberty. Although psychosocial influences such as heightened sociocultural pressures for thinness in girls and women contribute to this sex imbalance, biological factors could also play an important role. METHODS: This narrative review summarizes evidence of biological factors underlying the sex-differentiated prevalence of eating pathology as well as within-sex variability in risk. FINDINGS: There are sex differences in the pubertal emergence of genetic effects on eating pathology (adrenarche in males; gonadarche in females), and at least some genetic contributions to eating pathology seem to vary between the sexes. Furthermore, sex steroid hormones (eg, testosterone, estradiol, progesterone) are leading contributors to differential risk for eating pathology in males and females across the life span. Emerging data suggest that between-sex and within-sex variability in risk might occur via hormone-driven modulation (activation/deactivation) of genetic influences and neural responsiveness to food-related cues. IMPLICATIONS: There is a biological basis to heightened risk for eating pathology in females, relative to males, as well as unique biological influences within each sex. Findings from this review highlight the importance of studying both sexes and considering sex-specific biological mechanisms that may underlie differential risk for eating pathology.

Consensus Parameter: Research Methodologies to Evaluate Neurodevelopmental Effects of Pubertal Suppression in Transgender Youth.

Purpose: Pubertal suppression is standard of care for early pubertal transgender youth to prevent the development of undesired and distressing secondary sex characteristics incongruent with gender identity. Preliminary evidence suggests pubertal suppression improves mental health functioning. Given the widespread changes in brain and cognition that occur during puberty, a critical question is whether this treatment impacts neurodevelopment. Methods: A Delphi consensus procedure engaged 24 international experts in neurodevelopment, gender development, puberty/adolescence, neuroendocrinology, and statistics/psychometrics to identify priority research methodologies to address the empirical question: is pubertal suppression treatment associated with real-world neurocognitive sequelae? Recommended study approaches reaching 80% consensus were included in the consensus parameter. Results: The Delphi procedure identified 160 initial expert recommendations, 44 of which ultimately achieved consensus. Consensus study design elements include the following: a minimum of three measurement time points, pubertal staging at baseline, statistical modeling of sex in analyses, use of analytic approaches that account for heterogeneity, and use of multiple comparison groups to minimize the limitations of any one group. Consensus study comparison groups include untreated transgender youth matched on pubertal stage, cisgender (i.e., gender congruent) youth matched on pubertal stage, and an independent sample from a large-scale youth development database. The consensus domains for assessment includes: mental health, executive function/cognitive control, and social awareness/functioning. Conclusion: An international interdisciplinary team of experts achieved consensus around primary methods and domains for assessing neurodevelopmental effects (i.e., benefits and/or difficulties) of pubertal suppression treatment in transgender youth.

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.

The Disruptive Effects of Estrogen Removal before Puberty on Risk for Binge Eating in Female Rats.

Recent research suggests that estrogen is protective against binge eating in adult females, and that pubertal estrogen may be critical for these effects. Nonetheless, to date, no study has examined the role of pubertal estrogen in adult binge eating phenotypes in females, potentially due to difficulties experimentally manipulating estrogen in humans to examine causal effects. We used a novel animal model to examine whether estrogen removal prior to puberty (via pre-pubertal ovariectomy (P-OVX)) increases rates of binge eating prone (BEP) phenotypes in adulthood in females. A total of 77 P-OVX and 79 intact rats were followed from pre-puberty into adulthood and phenotyped for BEP status in adulthood. Results showed significantly increased rates (~2-8x higher) of adult BEP phenotypes in P-OVX as compared to intact rats. Findings confirm that estrogen removal substantially increases later risk for binge eating in females, potentially by disrupting typical adolescent brain development.

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.

Reduced Medial Prefrontal Control of Palatable Food Consumption Is Associated With Binge Eating Proneness in Female Rats.

Binge eating is the core, maladaptive eating behavior that cuts across several major types of eating disorders. Binge eating is associated with a significant loss of control over palatable food (PF) intake, and deficits in behavioral control mechanisms, subserved by the prefrontal cortex (PFC), may underlie binge eating. Few studies, to date, have examined whether the PFC is directly involved in the expression of binge eating. As such, the present study investigated the functional role of the medial PFC (mPFC) in PF consumption, using an individual differences rat model of binge eating proneness. Here, we tested the hypothesis that binge eating proneness (i.e., high levels of PF consumption) is associated with reduced mPFC-mediated behavioral control over PF intake. In experiment 1, we quantified PF-induced Fos expression in both excitatory and inhibitory neurons within the mPFC in binge eating prone (BEP) and binge eating resistant (BER) female rats. In experiment 2, we pharmacologically inactivated the mPFC of BEP and BER female rats, just prior to PF exposure, and subsequently quantified PF intake and scores of feeding behavior. While most Fos-expressing neurons of the mPFC in both BEPs and BERs were of the excitatory phenotype, fewer excitatory neurons were engaged by PF in BEPs than in BERs. Moreover, pharmacological inactivation of the mPFC led to a significant increase in PF intake in both BEPs and BERs, but the rise in PF consumption was stronger in BEPs than in BERs. Thus, these data suggest that lower, PF-induced excitatory tone in the mPFC of BEP rats may lead to a weaker, mPFC-mediated behavioral "brake" over excessive PF intake.

Gonadal hormone contributions to individual differences in eating disorder risk.

PURPOSE OF REVIEW: Females experience eating disorders at substantially higher rates than males. Although sociocultural factors have traditionally been thought to underlie this sex disparity, accumulating evidence implicates differential exposure to gonadal hormones early in life. Gonadal hormones also impact within-sex variability in disordered eating, helping to explain why not all women develop an eating disorder, and some men do. We review recent findings regarding these gonadal hormone effects and their implications for the etiology of eating disorders. RECENT FINDINGS: Males are exposed to significantly higher testosterone levels than females perinatally, and this exposure appears to protect against later binge eating in males relative to females. Within-sex, higher estradiol levels among females and higher testosterone levels among males appear to be protective. Progesterone exhibits minimal direct phenotypic effects on disordered eating but appears to counteract the protective effects of estrogen in adult females. Importantly, gonadal hormone effects may be moderated by psychosocial factors. SUMMARY: Evidence suggests that gonadal hormones play a critical role in the etiology of disordered eating. Overall, higher testosterone and estrogen appear to be protective across development. Additional research is needed to identify mechanisms underlying these effects and further explore interactions between hormonal and psychosocial risk.

Pubertal Testosterone Programs Adult Behavioral Adaptations to Sexual Experience through Infralimbic Cortex ΔFosB.

Acquisition of social proficiency entails behavioral adaptations to social experience, including both behavioral flexibility and inhibition of behaviors inappropriate in specific social contexts. Here, we investigated the contributions of testosterone and ΔFosB, a transcription factor linked to experience-dependent neural plasticity, to the adolescent maturation of social proficiency in male-female social interactions. To determine whether pubertal testosterone organizes circuits underlying social proficiency, we first compared behavioral adaptations to sexual experience in male Syrian hamsters that were deprived of testosterone during puberty (prepubertal castration; NoT@P) to those of males deprived of testosterone for an equivalent period of time in adulthood (postpubertal castration; T@P). All males were given testosterone replacement in adulthood for two weeks before sexual behavior testing, where males were allowed to interact with a receptive female once per week for five consecutive weeks. T@P males showed the expected decrease in ectopic (mis-directed) mounts with sexual experience, whereas NoT@P males did not. In addition, sexual experience induced FosB gene products expression in the infralimbic cortex (IL) in T@P, but not NoT@P, males. Overexpression of ΔFosB via an adeno-associated viral (AAV) vector in the IL of NoT@P males prior to sexual behavior testing was sufficient to produce a behavioral phenotype similar to that of experienced T@P males. Finally, overexpression of ΔFosB in IL increased the density of immature spines on IL dendrites. Our findings provide evidence that social proficiency acquired through sexual experience is organized by pubertal testosterone through the regulation of ΔFosB in the IL, possibly through increasing synaptic lability.

Stress as a potential moderator of ovarian hormone influences on binge eating in women.

Previous research has demonstrated significant associations between increased levels of ovarian hormones and increased rates of binge eating (BE) in women. However, whereas all women experience fluctuations in ovarian hormones across the menstrual cycle, not all women binge eat in response to these fluctuations, suggesting that other factors must contribute. Stress is one potential contributing factor. Specifically, it may be that hormone-BE associations are stronger in women who experience high levels of stress, particularly as stress has been shown to be a precipitant to BE episodes in women. To date, no studies have directly examined stress as a moderator of hormone-BE associations, but indirect data (that is, associations between BE and stress and between ovarian hormones and stress) could provide initial clues about moderating effects. Given the above, the purpose of this narrative review was to evaluate these indirect data and their promise for understanding the role of stress in hormone-BE associations. Studies examining associations between all three phenotypes (that is, ovarian hormones, stress, and BE) in animals and humans were reviewed to provide the most thorough and up-to-date review of the literature on the potential moderating effects of stress on ovarian hormone-BE associations. Overall, current evidence suggests that associations between hormones and BE may be stronger in women with high stress levels, possibly via altered hypothalamic-pituitary-adrenal axis response to stress and increased sensitivity to and altered effects of ovarian hormones during stress. Additional studies are necessary to directly examine stress as a moderator of ovarian hormone-BE associations and identify the mechanisms underlying these effects.

Reduced sensitivity to devaluation for instrumental but not consummatory behaviors in binge eating prone rats.

Binge eating is characterized by the consumption of a large amount of palatable food in a short period of time and is a core feature of many eating disorders. Patients with eating disorders are also known to display impairments in inhibitory control, cognition and decision-making, which may promote and maintain binge eating symptomology. In the current study, we examined whether rats that were subsequently characterized as displaying a higher propensity to binge eat would show pre-existing deficits in reinforcer devaluation-a paradigm used to examine decision-making following reductions in the value of a food reinforcer. Female rats were first trained to respond on two levers for the delivery of two food reinforcers (sucrose and maltodextrin solutions). At the test stage, rats were provided 1 h access to one of the two reinforcers to allow for devaluation via sensory specific satiety, immediately followed by an extinction test with both levers. Normal rats typically show reductions in responding on the lever associated with the devalued reinforcer (i.e., intact goal-directed responding). Subsequently, we used intermittent access to palatable food to identify high (BE prone [BEP]; n = 14), intermediate (BE neutral [BEN]; n = 48), and low (BE resistant [BER]; n = 13) phenotypes of binge eating. Prior reinforcer devaluation performance showed BEN and BER rats suppressed responding on the lever associated with the devalued reinforcer while BEP rats did not. This insensitivity to instrumental reinforcer devaluation in BEP rats did not reflect impaired sensory-specific satiety as during a food choice test, BEP rats showed a more robust alteration in food preferences following devaluation. Additionally, across all rats sensory specific satiety was correlated with subsequent intake of palatable food. Collectively, these findings suggest dissociable effects of devaluation procedures on instrumental actions and consummatory behaviors in BEP rats, and may indicate that pre-existing differences in goal-directed behavior and sensory-specific satiety contribute to the propensity to overeat palatable food.

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.