It Takes Two: An antenatal to postnatal RDoC framework for investigating the origins of maternal attachment and mother-infant social communication.

Transformation of the maternal-fetal relationship into the mother-infant relationship remains an enigmatic process. This progression is considered using an RDoC-informed approach centered on domains of Arousal/Regulation, Positive/Negative Valence, and Social Processes. 158 maternal-fetal dyads began participation during pregnancy, maternal-infant dyads were followed at 6-months postpartum. Women exhibited stability in feelings of attachment to the fetus and infant, and in positive/negative appraisal of pregnancy and motherhood. Elicited maternal physiological arousal to emotionally evocative videos generated fetal heart rate variability and motor activity responses. Parasympathetic (i.e., heart rate variability) suppression in the fetus was associated with more positive and regulated infant social communication in the Face-to-face Still Face protocol; suppression of maternal respiratory sinus arrhythmia was related to infant affect but in the opposite direction. Maternal ratings of infant temperament aligned with maternal antenatal affective valence. Attachment trajectories characterized by stability from antenatal to postnatal periods were most associated with maternal affective appraisal of pregnancy; shifts were influenced by infant characteristics and maternal sympathetic responsivity. Results illustrate how variation in arousal and regulatory systems of the pregnant woman and fetus operate within the context of maternal positive and negative valence systems to separately and jointly shape affiliation and temperament in early infancy.

Predicting child temperament and behavior from the fetus.

There remains little debate that the period before birth sets the stage for subsequent development, yet scant evidence exists showing continuity from characteristics of the individual fetus to characteristics of the child. This report examines, in two studies, whether baseline and evoked fetal neurobehavioral functioning are predictive of features of child temperament and behavior as reported by mothers when offspring were between 7 and 14 years old (M = 10.1 years). Study 1 utilizes data generated from 333 maternal-fetal pairs collected during an undisturbed condition during the second half of gestation in relation to the child temperament dimensions of behavioral inhibition and exuberance. Associations at 32 weeks gestation were detected between all features of fetal neurobehavior and behavioral inhibition. In adjusted models, slower fetal heart rate and less fetal movement were associated with significant unique variance in predicting higher levels of childhood behavioral inhibition. No associations were detected for exuberance. Study 2 focuses on the association of evoked fetal reactivity and recovery to induced maternal arousal with subsequent child behavioral difficulties in a subset of the full sample (n = 130). Greater recovery in fetal heart rate following maternal stimulation was predictive of fewer behavioral difficulties and more prosocial behavior in childhood. Results from both studies provide support for gestational origins of core individual differences that portend childhood outcomes with foundational reactivity and regulatory components.

Maternal salivary testosterone in pregnancy and fetal neuromaturation.

Testosterone exposure during pregnancy has been hypothesized as a mechanism for sex differences in brain and behavioral development observed in the postnatal period. The current study documents the natural history of maternal salivary testosterone from 18 weeks gestation of pregnancy to 6 months postpartum, and investigates associations with fetal heart rate, motor activity, and their integration. Findings indicate maternal salivary testosterone increases with advancing gestation though no differences by fetal sex were detected. High intra-individual stability in prenatal testosterone levels extend into the postnatal period, particularly for pregnancies with male fetuses. With respect to fetal development, by 36 weeks gestation higher maternal prenatal salivary testosterone was significantly associated with faster fetal heart rate and less optimal somatic-cardiac integration. Measurement of testosterone in saliva is a useful tool for repeated-measures studies of hormonal concomitants of pregnancy. Moreover, higher maternal testosterone levels are associated with modest interference to fetal neurobehavioral development.

STUDIES IN FETAL BEHAVIOR: REVISITED, RENEWED, AND REIMAGINED.

Among the earliest volumes of this monograph series was a report by Lester Sontag and colleagues, of the esteemed Fels Institute, on the heart rate of the human fetus as an expression of the developing nervous system. Here, some 75 years later, we commemorate this work and provide historical and contemporary context on knowledge regarding fetal development, as well as results from our own research. These are based on synchronized monitoring of maternal and fetal parameters assessed between 24 and 36 weeks gestation on 740 maternal-fetal pairs compiled from eight separate longitudinal studies, which commenced in the early 1990s. Data include maternal heart rate, respiratory sinus arrhythmia, and electrodrmal activity and fetal heartrate, motor activity, and their integration. Hierarchical linear modeling of developmental trajectories reveals that the fetus develops in predictable ways consistent with advancing parasympathetic regulation. Findings also include:within-fetus stability (i.e., preservation of rank ordering over time) for heart rate, motor, and coupling measures; a transitional period of decelerating development near 30 weeks gestation; sex differences in fetal heart rate measures but not in most fetal motor activity measures; modest correspondence in fetal neurodevelopment among siblings as compared to unrelated fetuses; and deviations from normative fetal development in fetuses affected by intrauterine growth restriction and other conditions. Maternal parameters also change during this period of gestation and there is evidence that fetal sex and individual variation in fetal neurobehavior influence maternal physio-logical processes and the local intrauterine context. Results are discussed within the framework of neuromaturation, the emergence of individual differences, and the bidirectional nature of the maternal-fetal relationship.We pose a number of open questions for future research. Although the human fetus remains just out of reach, new technologies portend an era of accelerated discovery of the earliest period of development

Concurrent levels of maternal salivary cortisol are unrelated to self-reported psychological measures in low-risk pregnant women.

Associations between salivary cortisol and maternal psychological distress and well-being were examined prospectively on 112 women with normally progressing, singleton pregnancies between 24 and 38 weeks gestation. At each of 5 visits, conducted in 3-week intervals, women provided a saliva sample and completed questionnaires measuring trait anxiety, depressive symptoms, pregnancy-specific hassles and uplifts, and psychological well-being. Maternal salivary cortisol was unrelated to psychological measures with the exception of minor associations detected with measures of anxiety and depressive symptoms between 30 and 32 weeks only. Findings indicate that self-reported maternal psychological distress and well-being are not associated with significant variation in maternal salivary cortisol levels during the second half of gestation. This suggests that studies that measure psychological factors in pregnancy but do not measure maternal cortisol should exercise caution in assuming activation of the maternal hypothalamic-pituitary-adrenal axis is the mechanism through which maternal psychological factors are transduced to the fetus.

Prenatal antecedents of newborn neurological maturation.

Fetal neurobehavioral development was modeled longitudinally using data collected at weekly intervals from 24 to 38 weeks gestation in a sample of 112 healthy pregnancies. Predictive associations between 3 measures of fetal neurobehavioral functioning and their developmental trajectories to neurological maturation in the first weeks after birth were examined. Prenatal measures included fetal heart rate (FHR) variability, fetal movement, and coupling between fetal motor activity and heart rate patterning; neonatal outcomes include a standard neurologic examination (n = 97) and brainstem auditory evoked potential (BAEP; n = 47). Optimality in newborn motor activity and reflexes was predicted by fetal motor activity, FHR variability, and somatic-cardiac coupling predicted BAEP parameters. Maternal pregnancy-specific psychological stress was associated with accelerated neurologic maturation.

Fetal motor activity and maternal cortisol.

The contemporaneous association between maternal salivary cortisol and fetal motor activity was examined at 32 and 36 weeks gestation. Higher maternal cortisol was positively associated with the amplitude of fetal motor activity at 32 weeks, r(48) = .39, p < .01, and 36 weeks, r(77) = .27, p < .05, and the amount of time fetuses spent moving at 32 weeks during the 50 min observation period, r(48) = 33, p < .05. Observation of periods of unusually intense fetal motor activity were more common in fetuses of women with higher cortisol, Mann-Whitney U = 58.5. There were no sex differences in fetal motor activity, but the associations between maternal cortisol and fetal motor amplitude and overall movement were significantly stronger for male than female fetuses.

Diurnal rhythm of cortisol during late pregnancy: associations with maternal psychological well-being and fetal growth.

Maternal psychological functioning during pregnancy affects both maternal and fetal well-being. The hypothalamic-pituitary-adrenal (HPA) axis provides one mechanism through which maternal psychosocial factors may be transduced to the fetus. However, few studies have examined maternal psychological factors or birth outcomes in relation to the diurnal pattern of cortisol across the day. The current study examined maternal psychological well-being, parity status, and birth weight in relation to the maternal cortisol diurnal rhythm in a group of 98 low-risk pregnant women (51 primiparae). At 36 weeks gestation, participants completed both pregnancy-specific and general self-report measures of psychological functioning and provided saliva samples at 8:00, 12:00, and 16:00 h on 2 consecutive working days for the assay of cortisol. The expected diurnal decline in salivary cortisol was observed. Higher trait anxiety was associated with a flatter afternoon decline for all mothers. For primiparae, steeper morning cortisol declines were associated with lower infant birth weight. The findings suggest that regulation of the HPA axis may differ by parity status with downstream implications for fetal growth and development.

Fetal responses to induced maternal relaxation during pregnancy.

Fetal responses to induced maternal relaxation during the 32nd week of pregnancy were recorded in 100 maternal-fetal pairs using a digitized data collection system. The 18-min guided imagery relaxation manipulation generated significant changes in maternal heart rate, skin conductance, respiration period, and respiratory sinus arrhythmia. Significant alterations in fetal neurobehavior were observed, including decreased fetal heart rate (FHR), increased FHR variability, suppression of fetal motor activity (FM), and increased FM-FHR coupling. Attribution of the two fetal cardiac responses to the guided imagery procedure itself, as opposed to simple rest or recumbency, is tempered by the observed pattern of response. Evaluation of correspondence between changes within individual maternal-fetal pairs revealed significant associations between maternal autonomic measures and fetal cardiac patterns, lower umbilical and uterine artery resistance and increased FHR variability, and declining salivary cortisol and FM activity. Potential mechanisms that may mediate the observed results are discussed.

Prenatal origins of temperamental reactivity in early infancy.

BACKGROUND: Temperament theory has long considered individual differences in reactivity and regulation to be present at birth. Recent evidence suggests that such differences may be present prenatally and moderated by maternal emotionality. AIMS: To determine whether induced maternal emotional activation generates a fetal response and whether observed fetal responsivity is associated with early infant temperament. STUDY DESIGN: Women viewed an emotionally evocative labor and delivery documentary at 32 weeks gestation while physiological indices were evaluated and their infant's temperament was assessed at 6 weeks postnatal age. SUBJECTS: Participants were 137 pregnant women and their infants. OUTCOME MEASURES: Maternal physiological (heart rate and skin conductance) and fetal neurobehavioral (heart rate and motor activity) data were collected during gestation in response to the stimulus. Infant temperament (irritability and consolability) data were based on observational methods after birth. RESULTS: Fetuses reacted to maternal viewing of the video with decreased heart rate variability, fewer motor bouts, and decreased motor activity. There was correspondence between the nature of individual maternal physiological responses to the full video, as well as phasic responses to a graphic birth scene, and fetal responsivity. Fetuses that reacted more intensively to maternal stimulation were significantly more likely to become infants that demonstrated greater irritability during a developmental examination at 6 weeks of age. DISCUSSION: These results support the presumption that early postnatal temperamental characteristics emerge during the prenatal period.

The pregnancy experience scale-brief version.

The role of maternal stress during pregnancy remains a focus of academic and clinical inquiry, yet there are few instruments available that measure pregnancy-specific contributors to maternal psychological state. This report examines the psychometric properties of an abbreviated version of the Pregnancy Experience Scale (PES) designed to evaluate maternal appraisal of positive and negative stressors during pregnancy. The PES-Brief consists of the top 10 items endorsed as pregnancy hassles and 10 pregnancy uplifts from the original scale. The PES-Brief was administered to 112 women with low risk, singleton pregnancies five times between 24 and 38 weeks gestation. Scoring includes frequency and intensity measures for hassles and uplifts, as well as composite measures for the relation between the two. Internal reliability, test-retest reliability and convergent validity were comparable with the original version. The PES-Brief provides an economical source of information on stress appraisal and emotional valence towards pregnancy.

Continuity in self-report measures of maternal anxiety, stress, and depressive symptoms from pregnancy through two years postpartum.

This study examined stability and change in maternal anxiety, stress and depression both during the second half of pregnancy and from pregnancy to six weeks and two years postpartum. Self-report measures included those designed to measure mood and state as well as more persistent attributes. Longitudinal data were collected from 137 women during pregnancy, 120 at six weeks, and 97 at two years. There was significant individual stability in scores on specific measures during pregnancy (range in Pearson rs=0.30-0.86) and from pregnancy through two years postpartum (rs=0.30-0.74). Comparable levels of convergence among measures of different constructs both within pregnancy and over time were also demonstrated, suggesting lack of precision in measurement instruments designed for specific constructs. Despite intra-individual stability, changes in mean levels were also observed over time with somewhat different patters for each variable. However, maternal parity was an important contributor to both level and trajectory. A summary composite score showed an elevated level of psychological distress during pregnancy in multiparous women, followed by a decline through two years postpartum; primiparous women displayed a gradual increase in distress [main effect F (1,87)=3.97, p < 0.05; time interaction F (2,174)= 7.15, p < 0.001] to multiparous levels by two years. Results are discussed in terms of a "motherhood" effect on psychological distress.

Fetal heart rate and motor development in overweight and obese pregnant women.

OBJECTIVE: To determine the relationship between maternal prepregnancy body mass index (BMI) and fetal cardiac and motor activity and integration during the second half of pregnancy. METHODS: Longitudinal data were collected from 610 nonsmoking women with normally progressing pregnancies at three gestational periods (24, 30-32, and 36 weeks) across eight cohorts studied between 1997 and 2013. Fifty minutes of fetal heart rate and motor activity data were collected at each period via actocardiography in a laboratory setting. Data were digitized and analyzed using customized software. Standard BMI categories were computed from maternal prepregnancy weight and height. Participants were stratified into normal weight (n=401, 65.7%), overweight (n=137, 22.5%), or obese (n=72, 11.8%). RESULTS: Fetuses of obese women showed lower heart rate variability and fewer accelerations relative to fetuses of normal weight women. Fetuses of both obese and overweight women exhibited more vigorous motor activity than fetuses of normal weight women. Cardiac-somatic integration was reduced in both obese and overweight groups. Findings differed by gestational age at assessment. CONCLUSIONS: Excess maternal prepregnancy weight in overweight and obese women alters the normal trajectory of fetal cardiac and motor development and their integration, with effects amplified as pregnancy progresses.

Psychosocial influences in dietary patterns during pregnancy.

There is increasing evidence that psychosocial factors may affect dietary intakes and health. The current analysis examined the association of six indices of psychosocial well-being with dietary intake during pregnancy. One hundred thirty-four women with low-risk, normal pregnancies participated in a cross-sectional, observational study that assessed dietary intake at 28 weeks' gestation. Psychosocial characteristics, including anxiety, depressed mood, anger, fatigue, social support, and stress were assessed between 24 and 32 weeks' gestation. Pearson product-moment correlations were calculated to determine the relationships between psychosocial factors and diet. Findings suggest that pregnant women who were more fatigued, stressed, and anxious consumed more foods, as evidenced by their increased macronutrient intakes, while appearing to have decreased intakes of some micronutrients. Psychosocial factors should be considered when counseling women regarding diet during pregnancy.

Maternal psychophysiological change during the second half of gestation.

This study investigated the trajectory of physiological and psychological functioning during the second half of pregnancy and compared responsiveness to a laboratory stressor between pregnant and non-pregnant women. Monitoring of 137 pregnant women at 20, 24, 28, 32, 36, and 38 weeks of pregnancy included measures of heart period (HP), heart period variability (HPV), skin conductance (SCL), respiratory period (RP), respiratory sinus arrhythmia (RSA), and self-report of mood disturbance. HP and RSA declined during this period; SCL and mood disturbance increased. Parity was a significant moderator. HP and SCL responsiveness to the Stroop color-word task was assessed twice in pregnant participants and compared to a sample of 27 non-pregnant women. Physiologic responsiveness was reduced in pregnant women. Pregnant women perceived the Stroop to be more difficult, but performance was unaffected. Despite buffered responsivity to stressful stimuli during pregnancy, advancing gestation is associated with escalating sympathetic tone and declining parasympathetic tone.

The ups and downs of early mothering.

INTRODUCTION: The maternal experience of having a young infant is often viewed through a negative lens focused on psychological distress due, in part, to a historical focus on identifying threats to prenatal, perinatal and postpartum well-being of women and infants. This report examines maternal appraisal of both positive and negative experiences during and after pregnancy and introduces a new scale that assesses both uplifts and hassles that are specific to early motherhood. METHODS: The sample included 136 women who began study participation during pregnancy and completed an existing scale designed to evaluate pregnancy-specific hassles and uplifts. When infants were 6 months old, participants completed the newly developed Maternal Experience Scale (MES) along with questionnaires related to anxiety, depression, attachment, parenting stress and infant temperament characteristics. RESULTS: In general, women with 6-month-old infants rated their maternal experiences far more positively than negatively. MES hassles and uplift scores reflected both convergent and discriminant validity with general measures of psychological well-being and parent-specific measures. Appraisal of the pregnancy experience significantly predicted appraisal of early motherhood for hassles, uplifts and a composite score reflecting emotional valence. Women became relatively more uplifted and less hassled from pregnancy to 6-month postpartum; this was particularly true for multiparous women. DISCUSSION: The maternal perception of motherhood corresponds to her perception of pregnancy. The MES provides a balanced view of motherhood by including maternal appraisal of the uplifting aspects of caring for an infant.

Randomized controlled trial of prenatal zinc supplementation and fetal bone growth.

BACKGROUND: Maternal zinc deficiency is relatively common in developing countries, but its consequences for fetal growth are not established. OBJECTIVE: The goal was to examine whether improvement in maternal gestational zinc status is positively associated with fetal growth as assessed by ultrasonography. DESIGN: We conducted a double-masked, randomized trial among 242 pregnant Peruvian women in an impoverished shantytown in Lima, Peru. At 10-16 wk of gestation, the women were randomly assigned to receive daily supplements containing 60 mg Fe and 250 microg folic acid, with or without 25 mg Zn. We measured fetal head circumference, biparietal diameter, abdominal circumference, and femur diaphysis length at 20, 24, 28, 32, 36, and 38 wk of gestation. Fetal measures were analyzed longitudinally to evaluate differences in trends of fetal growth by supplement type, and within-subject correlations were taken into account. RESULTS: Femur diaphysis length was greater in fetuses whose mothers received zinc supplements (P < 0.05), and the difference tended to increase with gestational age. No significant differences by supplement type were observed for the other anatomical sites measured. CONCLUSIONS: The observed positive effect of prenatal zinc on fetal femur diaphysis length is consistent with the results of experimental studies in animals and in vitro. The supplementation effect represents an upward shift in mean femur diaphysis length at term of about one-quarter of the reference SD. These findings suggest the potential importance of maternal zinc status for fetal bone growth in humans and illustrate the value of ultrasonography for evaluating the effect of prenatal nutritional interventions on components of fetal growth.

Psychosocial influences on weight gain attitudes and behaviors during pregnancy.

OBJECTIVE: To examine pregnant women's weight-related attitudes and behaviors in relation to a constellation of psychosocial characteristics, prepregnancy body habitus, and gestational weight gain. PARTICIPANTS: One hundred-thirty women with low-risk, normal pregnancies. DESIGN: Cross-sectional, observational study assessed attitudes about weight gain at 36 weeks' gestation. Psychosocial characteristics, including anxiety, depression, social support, emotionality, and pregnancy-specific and nonspecific stress appraisal were assessed between 28 and 36 weeks' gestation. STATISTICAL ANALYSIS PERFORMED: Principal components factor analysis, Pearson correlations, t tests, and analysis of variance. RESULT: A range of positive and negative attitudes about weight gain was expressed. Twenty-one percent (n=27) of the sample endorsed at least one weight-restrictive behavior during pregnancy. Women who reported more weight-restrictive behaviors were more anxious (r=.24, P<.01), depressed (r=.29,P<.001), angry (r=.29, P<.001), stressed (r=.23, P<.01), and felt less uplifted (r=-.21, P<.05) about their pregnancies in general. Higher Positive Pregnancy Body Image scores were associated with feeling better about the pregnancy in general (r=.35, P<.001), fewer depressive symptoms, and less anger (both r=.20, both P<.01). Women who were self conscious about their weight gain felt more hassled by their pregnancies (r=.21, P<.05), greater anger (r=.21, P<.05), and more support from partners (r=.22, P<.05). Prepregnancy body mass index was unrelated, but negative attitudes about weight gain existed even among women who gained within recommended ranges. CONCLUSION: Women's attitudes about weight gain in pregnancy are imbedded in their orientation toward pregnancy as well as their general psychological functioning. Effective nutrition counseling for pregnant women should include consideration of weight-restrictive behaviors, the degree to which the pregnancy is perceived as positive and uplifting, and whether weight gain attitudes may be associated with their relationship with a spouse or partner.

Fetal response to induced maternal stress.

BACKGROUND: Despite increased attention to the role of antenatal maternal psychological stress in postnatal development, remarkably little information is available on the nature of the intrauterine fetal response to maternal psychological state. AIMS: To determine whether: (1) the fetus responds to maternal stress; (2) the fetal response changes over gestation; and (3) individual maternal and fetal response patterns are stable over time. STUDY DESIGN: Induced maternal stress at 24 and 36 weeks gestational age using the Stroop color-word task. SUBJECTS: 137 low-risk pregnant women with normally developing fetuses. OUTCOME MEASURES: Maternal (heart rate and skin conductance) and fetal (heart rate, heart rate variability, and motor activity) responses. RESULTS: The manipulation evoked maternal sympathetic activation, which declined in magnitude from 24 to 36 weeks gestation. Fetuses responded to the manipulation with increased variability in heart rate (F(2,256)=7.80, p<0.001) and suppression of motor activity (F(2,216)=15.47, p<0.001). The magnitude of the fetal response increased over gestation. The degree of maternal reactivity to and recovery from the stressor were correlated over time (r's=0.53 and 0.60 for heart rate; r's=0.31 and 0.36 for skin conductance; p's<0.001). There was moderate stability in the magnitude of the fetal motor response (r=0.25, p<0.01). CONCLUSIONS: Demonstration of fetal responses to maternal sympathetic activation evoked by a benign cognitive stressor suggests that fetal neurobehavioral regulation is routinely disrupted by maternal environmental intrusions. There is no evidence of a protective effect of diminished maternal sensitivity to stress on the fetus. Individual stability in the magnitude of the evoked maternal physiologic and psychological responses from 24 to 36 weeks and stability in the fetal motor response implies that characteristic response patterns emerge in utero. We propose that autonomic development is partially entrained through these processes.

Fetal state concordance predicts infant state regulation.

Fetal state organization reflects the development of the central nervous system but may also portend individual differences in postnatal state organization. The goal of the present study was to determine the extent to which fetal state regulation, defined as the percentage of an observation period in which fetal heart rate and movement concordance was displayed, is associated with neonatal state regulation. Neonatal state regulation was evaluated through a standard neurobehavioral assessment at 2 weeks postpartum. Biobehavioral concordance was measured in 52 normally developing fetuses at 24, 30 and 36 weeks gestation using an actocardiograph; the neonatal assessment was administered to 41 of these as infants. Intrafetal stability in biobehavioral concordance did not emerge prior to 36 weeks. Fetuses with higher concordance at 36 weeks were infants that displayed better state regulation during the exam, including more alertness and orientation (r(35)=0.29), less cost of maintaining attention (r=0.36), less irritability (r=-0.41), better regulatory capacity (r=0.47), a greater range of available states (r=0.34), and were significantly more likely to maintain control during the most aversive portions of the exam F(1,31)=4.63, p<0.05). These results support fetal state as a stable individual attribute that is conserved across the prenatal and neonatal periods.