Mothering revisited: A role for cortisol?

This selective review first describes the involvement of the maternal hypothalamic-pituitary-adrenal (HPA) axis during pregnancy and the postpartum period, and the relation between peripartum HPA axis function and maternal behavior, stress reactivity and emotional dysregulation in human mothers. To provide experimental background to this correlational work, where helpful, animal studies are also described. It then explores the association between HPA axis function in mothers and their infants, under ongoing non-stressful conditions and during stressful challenges, the moderating role of mothers' sensitivity and behavior in the mother-child co-regulation and the effects of more traumatic risk factors on these relations. The overarching theme being explored is that the HPA axis - albeit a system designed to function during periods of high stress and challenge - also functions to promote adaptation to more normative processes, shown in the new mother who experiences both high cortisol and enhanced attraction and attention to and recognition of, their infants and their cues. Hence the same HPA system shows positive relations with behavior at some time points and inverse ones at others. However, the literature is not uniform and results vary widely depending on the number, timing, place, and type of samplings and assessments, and, of course, the population being studied and, in the present context, the state, the stage, and the stress levels of mother and infant.

Maternal symptoms of depression and sensitivity mediate the relation between maternal history of early adversity and her child temperament: The inheritance of circumstance.

We examined maternal depression and maternal sensitivity as mediators of the association between maternal childhood adversity and her child's temperament in 239 mother-child dyads from a longitudinal, birth cohort study. We used an integrated measure of maternal childhood adversity that included the Childhood Trauma Questionnaire and the Parental Bonding Index. Maternal depression was assessed with the Edinburgh Postnatal Depression Scale at 6 months postpartum. Maternal sensitivity was assessed with the Ainsworth maternal sensitivity scales at 6 months. A measure of "negative emotionality/behavioral dysregulation" was derived from the Early Childhood Behaviour Questionnaire administered at 36 months. Bootstrapping-based mediation analyses revealed that maternal depression mediated the effect of maternal childhood adversity on offspring negative emotionality/behavioral dysregulation (95% confidence interval [0.026, 0.144]). We also found a serial, indirect effect of maternal childhood adversity on child negative emotionality/behavioral mediated first by maternal depression and then by maternal sensitivity (95% confidence interval [0.031, 0.156]). Results suggest the intergenerational transmission of the effects of maternal childhood adversity to the offspring occurs through a two-step, serial pathway, involving maternal depression and maternal sensitivity.

The role of breastfeeding in the association between maternal and infant cortisol attunement in the first postpartum year.

AIM: To explore the role of breastfeeding as a possible link between maternal and infant cortisol attunement across the first postpartum year. METHODS: Mothers (n = 93) provided salivary samples for cortisol levels over a two-day period during mid-pregnancy and at three, six and 12 months and infants at six and 12 months postpartum. Breastfeeding status was established at these same time points. RESULTS: Among breastfeeding mothers, positive correlations were found between maternal cortisol levels during pregnancy and at three months postpartum and infant cortisol at six or 12 months postpartum. Among nonbreastfeeding mothers, these same maternal and infant cortisol relations were inverse and less pronounced. Further, in breastfeeding mothers, the relationship between maternal prenatal cortisol and infant cortisol at 12 months was mediated through maternal cortisol at three months postpartum. CONCLUSION: These results suggest that maternal cortisol levels are positively associated with cortisol levels of the infant, among mothers who breastfeed. This relationship persists over a one-year period.

Fetal growth interacts with multilocus genetic score reflecting dopamine signaling capacity to predict spontaneous sugar intake in children.

BACKGROUND: We have shown that intrauterine growth restriction (IUGR) leads to increased preference for palatable foods at different ages in both humans and rodents. In IUGR rodents, altered striatal dopamine signaling associates with a preference for palatable foods. OBJECTIVES: Our aim was to investigate if a multilocus genetic score reflecting dopamine-signaling capacity is differently associated with spontaneous palatable food intake in children according to the fetal growth status. METHODS: 192 four-year old children from a community sample from Montreal and Hamilton, Canada, were classified according to birth weight and administered a snack test meal containing regular as well as palatable foods. Intrauterine growth restriction was based on the birth weight ratio below 0.85; children were genotyped for polymorphisms associated with dopamine (DA) signaling, with the hypofunctional variants (TaqIA-A1 allele, DRD2-141C Ins/Ins, DRD4 7-repeat, DAT1-10-repeat, Met/Met-COMT) receiving the lowest scores, and a composite score was calculated reflecting the total number of the five genotypes. Macronutrient intake during the Snack Test was the outcome. RESULTS: Adjusting for z-score BMI at 48 months and sex, there was a significant interaction of the genetic profile and fetal growth on sugar intake [߈ = -4.56, p = 0.04], showing a positive association between the genetic score and sugar intake in IUGR children, and no association in non-IUGR children. No significant interactions were seen in other macronutrients. CONCLUSIONS: Variations in a genetic score reflecting DA signaling are associated with differences in sugar intake only in IUGR children, suggesting that DA function is involved in this behavioral feature in these children. This may have important implications for obesity prevention in this population.

Both maternal care received and genotype influence stress-related phenotype in female rats.

Rat dams differ naturally in the level of maternal care they provide to their offspring within the same litter. We explored possible mechanisms of differential maternal care focused on genetic variation. We examined single nucleotide polymorphisms in the glucocorticoid receptor, FK506-binding protein, and serotonin transporter genes in two separate cohorts, and the relationship between differential maternal care received, genotype, and offspring phenotype. Allelic variation in all three genes was significantly associated with levels of maternal care received by offspring and behavioral and endocrine stress responses in adulthood. Differences in pup behavior were also associated with allelic variation in these genes. Together, these results indicate that the dam/pup interaction is dynamic and implicate the genotype of the offspring in influencing the level of maternal care received. They further suggest that some genotypes may have a dampening effect on the impact of maternal care on stress-related phenotypes in adulthood.

Executive function in teen and adult women: Association with maternal status and early adversity.

The aim of this study was to determine the impact of maternal age on executive function and the moderating effects of women's maternal status and early-life experiences. Four groups of women were assessed as a function of their age (teens vs. adults) and maternal status (mothers vs. nonmothers). Participants completed executive function tests, including Spatial Working Memory (SWM), Intra-Extra-Dimensional-Set-Shift (IED), and Stockings of Cambridge (SOC). Women also completed the Childhood Trauma Questionnaire to assess their experiences of early adversity. Results showed that for the IED-task, there were main effects of age and maternal status and an interaction between the two; adults performed better than teens, mothers performed better than nonmothers, and teen nonmothers performed the least well of all groups. For the SWM-task, adults performed better than teens. Our results indicate that although age is an important factor for proper executive functioning, different tasks are affected differently and other factors such as maternity and adverse childhood experiences moderate this functioning.

An Attachment-Based Model of the Relationship Between Childhood Adversity and Somatization in Children and Adults.

OBJECTIVE: An attachment model was used to understand how maternal sensitivity and adverse childhood experiences are related to somatization. METHODS: We examined maternal sensitivity at 6 and 18 months and somatization at 5 years in 292 children in a longitudinal cohort study. We next examined attachment insecurity and somatization (health anxiety, physical symptoms) in four adult cohorts: healthy primary care patients (AC1, n = 67), ulcerative colitis in remission (AC2, n = 100), hospital workers (AC3, n = 157), and paramedics (AC4, n = 188). Recall of childhood adversity was measured in AC3 and AC4. Attachment insecurity was tested as a possible mediator between childhood adversity and somatization in AC3 and AC4. RESULTS: In children, there was a significant negative relationship between maternal sensitivity at 18 months and somatization at age 5 years (B = -3.52, standard error = 1.16, t = -3.02, p = .003), whereas maternal sensitivity at 6 months had no significant relationship. In adults, there were consistent, significant relationships between attachment insecurity and somatization, with the strongest findings for attachment anxiety and health anxiety (AC1, ß = 0.51; AC2, ß = 0.43). There was a significant indirect effect of childhood adversity on physical symptoms mediated by attachment anxiety in AC3 and AC4. CONCLUSIONS: Deficits in maternal sensitivity at 18 months of age are related to the emergence of somatization by age 5 years. Adult attachment insecurity is related to somatization. Insecure attachment may partially mediate the relationship between early adversity and somatization.

The Drosophila foraging gene human orthologue PRKG1 predicts individual differences in the effects of early adversity on maternal sensitivity.

There is variation in the extent to which childhood adverse experience affects adult individual differences in maternal behavior. Genetic variation in the animal foraging gene, which encodes a cGMP-dependent protein kinase, contributes to variation in the responses of adult fruit flies, Drosophila melanogaster, to early life adversity and is also known to play a role in maternal behavior in social insects. Here we investigate genetic variation in the human foraging gene (PRKG1) as a predictor of individual differences in the effects of early adversity on maternal behavior in two cohorts. We show that the PRKG1 genetic polymorphism rs2043556 associates with maternal sensitivity towards their infants. We also show that rs2043556 moderates the association between self-reported childhood adversity of the mother and her later maternal sensitivity. Mothers with the TT allele of rs2043556 appeared buffered from the effects of early adversity, whereas mothers with the presence of a C allele were not. Our study used the Toronto Longitudinal Cohort (N=288 mother-16 month old infant pairs) and the Maternal Adversity and Vulnerability and Neurodevelopment Cohort (N=281 mother-18 month old infant pairs). Our findings expand the literature on the contributions of both genetics and gene-environment interactions to maternal sensitivity, a salient feature of the early environment relevant for child neurodevelopment.

The more things change, the more things stay the same: maternal attitudes 3 to 18 months postpartum.

AIM: Becoming a parent precipitates changes in new mothers' psychological and social domains. Previous literature has focused exclusively on pregnancy and the early postpartum, but parenting is an evolving process, necessitating adaption to changing circumstances. We extended previous literature and investigate the changes in the postpartum from 3 to 18 months that occur in maternal attitudes. METHODS: Using the Childbearing Attitudes Questionnaire, we collected data on mothers' ratings of maternal worries, self-efficacy, mother-infant bonding, relationship with the partner and interest in sex (n = 171 women). Data were analysed with a latent growth curve. RESULTS: Results demonstrated stability in all maternal attitudes after 3 months postpartum. Further, different maternal attitudes are affected by different variables. Maternal worries and self-efficacy are associated with parity, postpartum depression and child temperament. Interestingly, a negative evaluation of the relationship with the partner was only associated with breastfeeding status, while interest in sex was associated with parity, socio-economic status (SES) and depressive symptoms. CONCLUSION: Despite general stability, different maternal attitudes related to different sets of variables. These patterns of attitudes in relation to relevant variables are discussed in terms of the literature on self-efficacy and gender roles, with important implications for clinical interventions.

Common and divergent psychobiological mechanisms underlying maternal behaviors in non-human and human mammals.

Maternal interactions with young occupy most of the reproductive period for female mammals and are absolutely essential for offspring survival and development. The hormonal, sensory, reward-related, emotional, cognitive and neurobiological regulators of maternal caregiving behaviors have been well studied in numerous subprimate mammalian species, and some of the importance of this body of work is thought to be its relevance for understanding similar controls in humans. We here review many of the important biopsychological influences on maternal behaviors in the two best studied non-human animals, laboratory rats and sheep, and directly examine how the conceptual framework established by some of the major discoveries in these animal "models" do or do not hold for our understanding of human mothering. We also explore some of the limits for extrapolating from non-human animals to humans. We conclude that there are many similarities between non-human and human mothers in the biological and psychological factors influencing their early maternal behavior and that many of the differences are due to species-characteristic features related to the role of hormones, the relative importance of each sensory system, flexibility in what behaviors are exhibited, the presence or absence of language, and the complexity of cortical function influencing caregiving behaviors.

Using cross-species comparisons and a neurobiological framework to understand early social deprivation effects on behavioral development.

Building upon the transactional model of brain development, we explore the impact of early maternal deprivation on neural development and plasticity in three neural systems: hyperactivity/impulsivity, executive function, and hypothalamic-pituitary-adrenal axis functioning across rodent, nonhuman primate, and human studies. Recognizing the complexity of early maternal-infant interactions, we limit our cross-species comparisons to data from rodent models of artificial rearing, nonhuman primate studies of peer rearing, and the relations between these two experimental approaches and human studies of children exposed to the early severe psychosocial deprivation associated with institutional care. In addition to discussing the strengths and limitations of these paradigms, we present the current state of research on the neurobiological impact of early maternal deprivation and the evidence of sensitive periods, noting methodological challenges. Integrating data across preclinical animal models and human studies, we speculate about the underlying biological mechanisms; the differential impact of deprivation due to temporal factors including onset, offset, and duration of the exposure; and the possibility and consequences of reopening of sensitive periods during adolescence.

Maternal anxiety from pregnancy to 2 years postpartum: transactional patterns of maternal early adversity and child temperament.

The aims of this study were to examine the anxiety trajectories of women from pregnancy to 2 years postpartum and to assess the influence of their early life experiences and the temperament of the child on these trajectories. We evaluated state anxiety (State-Trait Anxiety Inventory) at pregnancy and 3, 6, 12, 18, and 24 months postpartum and determined its course as a function of self-reported early adverse experiences (Childhood Trauma Questionnaire) and the temperament of the child at 18 months (Early Child Behavior Questionnaire). Based on growth curve modeling, we found that anxiety followed a general U-shape pattern from gestation to 2 years postpartum, which was modified by early life experience of women. Greater early adversity was associated with higher gestational anxiety, followed by a marked decrease once the baby was born, and subsequent increase during the later postpartum period. The temperament of the child also modulated anxiety trajectories. Thus, mothers of children high in negative affectivity and who also experienced greater early adversity had elevated and flat anxiety trajectories, while child extraversion was associated with increasing anxiety courses approaching 2 years postpartum. These results show that maternal anxiety dynamically changes through the postpartum period with a course that is affected by previous and current experiences.

Breastfeeding and maternal sensitivity predict early infant temperament.

AIM: Research findings are inconclusive when it comes to whether breastfeeding is associated with the mother-infant relationship or infant temperament. We examined the association between breastfeeding at three months postpartum and infant temperament at 18 months postpartum and whether this link was affected by the mothers' anxiety and mediated by her sensitivity. METHODS: We assessed 170 mothers for breastfeeding and anxiety using the Spielberger State-Trait Anxiety Inventory (STAI) at three months postpartum, maternal sensitivity using the Ainsworth Sensitivity Scale at six months postpartum and infant temperament using the Early Childhood Behaviour Questionnaire at 18 months postpartum. RESULTS: Mothers who breastfed at three months postpartum were more sensitive in their interactions with their infants at six months postpartum, and elevated sensitivity, in turn, predicted reduced levels of negative affectivity in infant temperament at 18 months postpartum. This indirect mediation persisted after controlling for confounders (effect ab = -0.0312 [0.0208], 95% CI = -0.0884 to -0.0031). A subsequent analysis showed that the mediation through sensitivity only occurred in women experiencing higher anxiety, with a STAI score ≥33.56 at three months (ab = -0.0250 [0.0179], 95% CI = -0.0759 to -0.0013). CONCLUSION: Our results suggest that breastfeeding and maternal sensitivity may have a positive impact on the early development of infant temperament.

Establishment and consolidation of the sleep-wake cycle as a function of attachment pattern.

The development of sleep-wake regulation in infants depends upon brain maturation as well as various environmental factors. The aim of the present study was to evaluate sleep duration and quality as a function of child attachment to the mother. One hundred and thirty-four mother-child dyads enrolled in the Maternal Adversity, Vulnerability and Neurodevelopment (MAVAN) project were included in this study. Attachment was assessed with the Strange Situation procedure at 36 months and maternal sleep reports were collected at 6, 12, 24 and 36 months. Differences in sleep characteristics were assessed with mixed models with one factor (attachment group) and one repeated measure (age). Children classified as disorganized had a significantly lower duration of nocturnal sleep, went to bed later, signaled more awakenings, had shorter periods of uninterrupted sleep (only at 12 months) and had shorter periods of time in bed (only at 6 months) than children classified as secure and/or ambivalent (p < 0.05). This is the first study to show that children with insecure disorganized attachment present a distinct sleep pattern in comparison with those with secure or ambivalent attachment between 6 and 36 months of age. Sleep disturbances could exacerbate difficulties in these families that are already considered vulnerable.

Distal pup cues evoke dopamine responses in hormonally primed rats in the absence of pup experience or ongoing maternal behavior.

During the early postpartum period or following estrogen/progesterone administration, pups elicit maternal behavior accompanied by a robust dopamine (DA) response in the nucleus accumbens (NAC) of female rats (Afonso et al., 2009). To determine whether DA responds to ostensibly "salient" stimuli in the absence of consummatory behaviors, we examined NAC shell DA responses during restricted (stimuli placed in a perforated box), and unrestricted access to pup and food stimuli. Microdialysis samples were collected from female rats that were either cycling and postpartum (Experiment 1), or after ovariectomy and treated with empty and hormone-filled capsules (Experiment 2). Relative to nonprimed controls, hormonally primed females had suppressed basal DA concentrations and facilitated pup-evoked DA responses, regardless of stimulus access condition. In contrast, food-evoked DA responses were unchanged by hormonal priming and were greater when females consumed food compared with distal (restricted) exposure to food. During pup and food restriction conditions, the lack of any "appetitive" behavioral differences, even in pup experienced postpartum females, was surprising. In Experiment 3, we confirmed that postpartum dams allocated time equivalently to restricted pup and food stimuli, even after pup deprivation. This was in sharp contrast to the effects of deprivation during the unrestricted access phase. Together, our data demonstrated that, in hormonally primed females, distal pup cues could evoke DA responses without prior stimulus experience, ongoing maternal (behavioral) responses, or clear evidence of robust pup saliency. The results suggest that NAC DA response reflects a state of responsiveness related to basal DA suppression in the hormonally primed female rat.

Low maternal sensitivity at 6 months of age predicts higher BMI in 48 month old girls but not boys.

BACKGROUND: Large population-based studies suggest that systematic measures of maternal sensitivity predict later risk for overweight and obesity. More work is needed to establish the developmental timing and potential moderators of this association. The current study examined the association between maternal sensitivity at 6 months of age and BMI z score measures at 48 months of age, and whether sex moderated this association. DESIGN: Longitudinal Canadian cohort of children from birth (the MAVAN project). METHODS: This analysis was based on a dataset of 223 children (115 boys, 108 girls) who had structured assessments of maternal sensitivity at 6 months of age and 48-month BMI data available. Mother-child interactions were videotaped and systematically scored using the Maternal Behaviour Q-Sort (MBQS)-25 items, a standardized measure of maternal sensitivity. Linear mixed-effects models and logistic regression examined whether MBQS scores at 6 months predicted BMI at 48 months, controlling for other covariates. RESULTS: After controlling for weight-relevant covariates, there was a significant sex by MBQS interaction (P=0.015) in predicting 48 month BMI z. Further analysis revealed a strong negative association between MBQS scores and BMI in girls (P=0.01) but not boys (P=0.72). Logistic regression confirmed that in girls only, low maternal sensitivity was associated with the higher BMI categories as defined by the WHO (i.e. "at risk for overweight" or above). CONCLUSIONS: A significant association between low maternal sensitivity at 6 months of age and high body mass indices was found in girls but not boys at 48 months of age. These data suggest for the first time that the link between low maternal sensitivity and early BMI z may differ between boys and girls.

Executive function and mothering: challenges faced by teenage mothers.

Previous research has established that in comparison to adult mothers teen mothers respond less sensitively to their infants. In adults, components of executive functions relate directly to maternal sensitivity. Since teenagers are known to have a less developed prefrontal cortex and greater difficulties in parenting, this study sought to determine whether the association between executive processes and mothering exists among teenagers. Two groups of mothers, teens (n = 30) and adults (n = 27), who were approximately 4-6 months postpartum, completed tasks assessing spatial working memory and attentional set shifting (cognitive flexibility) using the Cambridge Neuropsychological Test Automated Battery. Mothers were videotaped interacting with their infants and were later coded for various maternal behaviors. As predicted, teenagers performed more poorly than adults on tasks of cognitive flexibility and were less sensitive in their infant interactions. Among both groups there was a negative association between executive function and mothering; however, depending on the age of the mother different executive function tasks were relevant.

The effects of vitamin D3 during pregnancy and lactation on offspring physiology and behavior in sprague-dawley rats.

Recent findings show that developmental vitamin D deficiency leads to altered brain morphology and behavioral development in the rat offspring. We examined the effects of different dietary vitamin D levels in rat dams on behavior and biochemistry of the offspring. Females were divided into five conditions and received diets containing 0, 1,5, 3.3, 6.0, or 10.0 IU/g of vitamin D3 from mating to weaning. Offspring were tested as juveniles and as adults for anxiety, social learning and behavior, and locomotion. Results show that both deficient and excessive levels of vitamin D3 in juveniles lead to altered physiology and behavior. In juveniles but not adults, variations in vitamin D were related to variations in measures of anxiety and marginally, activity levels. For social behaviors, both juveniles and adults were affected by mothers' diets. In general, offspring of animals receiving abnormal concentrations of vitamin D showed the most deficits.