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.

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.

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

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.

Fetal heart rate and motor activity associations with maternal organochlorine levels: results of an exploratory study.

Contemporaneous associations between circulating maternal organochlorines (OCs) and measures of fetal heart rate and motor activity were evaluated. A panel of 47 OCs, including pesticides and polychlorinated biphenyls (PCBs), was analyzed from serum of 50 pregnant women at 36 weeks gestation. Data were empirically reduced into four factors and six individual compounds. All participants had detectable concentrations of at least one-quarter of the assayed OCs and, in general, higher socioeconomic level was associated with higher OC concentrations. Fetal heart rate measures were not consistently associated with maternal OCs. In contrast, one or more indicators of greater fetal motor activity were significantly associated with higher levels of the DDT and low chlorinated OC factors and five of the six individual compounds (heptachlor epoxide, trans nonachlor, oxychlordane, and PCBs 18 and 52). This preliminary demonstration of associations between fetal motor activity and maternal concentrations of persistent and pervasive environmental contaminants suggests that fetal assessment may be useful in ascertaining the potential early effects of these compounds on development.

Physiological reactivity of pregnant women to evoked fetal startle.

OBJECTIVE: The bidirectional nature of mother-child interaction is widely acknowledged during infancy and childhood. Prevailing models during pregnancy focus on unidirectional influences exerted by the pregnant woman on the developing fetus. Prior work has indicated that the fetus also affects the pregnant woman. Our objective was to determine whether a maternal psychophysiological response to stimulation of the fetus could be isolated. METHODS: Using a longitudinal design, an airborne auditory stimulus was used to elicit a fetal heart rate and motor response at 24 (n=47) and 36 weeks (n=45) of gestation. Women were blind to condition (stimulus versus sham). Maternal parameters included cardiac (heart rate) and electrodermal (skin conductance) responses. Multilevel modeling of repeated measures with 5 data points per second was used to examine fetal and maternal responses. RESULTS: As expected, compared to a sham condition, the stimulus generated a fetal motor response at both gestational ages, consistent with a mild fetal startle. Fetal stimulation was associated with significant, transient slowing of maternal heart rate coupled with increased skin conductance within 10s of the stimulus at both gestational ages. Nulliparous women showed greater electrodermal responsiveness. The magnitude of the fetal motor response significantly corresponded to the maternal skin conductance response at 5, 10, 15, and 30s following stimulation. CONCLUSION: Elicited fetal movement exerts an independent influence on the maternal autonomic nervous system. This finding contributes to current models of the dyadic relationship during pregnancy between fetus and pregnant woman.

Near-term fetal response to maternal spoken voice.

Knowledge about prenatal learning has been largely predicated on the observation that newborns appear to recognize the maternal voice. Few studies have examined the process underlying this phenomenon; that is, whether and how the fetus responds to maternal voice in situ. Fetal heart rate and motor activity were recorded at 36 weeks gestation (n = 69) while pregnant women read aloud from a neutral passage. Compared to a baseline period, fetuses responded with a decrease in motor activity in the 10 s following onset of maternal speech and a trend level decelerative heart rate response, consistent with an orienting response. Subsequent analyses revealed that the fetal response was modified by both maternal and fetal factors. Fetuses of women who were previously awake and talking (n = 40) showed an orienting response to onset of maternal reading aloud, while fetuses of mothers who had previously been resting and silent (n = 29) responded with elevated heart rate and increased movement. The magnitude of the fetal response was further dependent on baseline fetal heart rate variability such that largest response was demonstrated by fetuses with low variability of mothers who were previously resting and silent. Results indicate that fetal responsivity is affected by both maternal and fetal state and have implications for understanding fetal learning of the maternal voice under naturalistic conditions.

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.

Physiological blunting during pregnancy extends to induced relaxation.

There is accumulating evidence that pregnancy is accompanied by hyporesponsivity to physical, cognitive, and psychological challenges. This study evaluates whether observed autonomic blunting extends to conditions designed to decrease arousal. Physiological and psychological responsivity to an 18-min guided imagery relaxation protocol in healthy pregnant women during the 32nd week of gestation (n=54) and non-pregnant women (n=28) was measured. Data collection included heart period (HP), respiratory sinus arrhythmia (RSA), tonic and phasic measures of skin conductance (SCL and NS-SCR), respiratory period (RP), and self-reported psychological relaxation. As expected, responses to the manipulation included increased HP, RSA, and RP and decreased SCL and NS-SCR, followed by post-manipulation recovery. However, responsivity was attenuated for all physiological measures except RP in pregnant women, despite no difference in self-reported psychological relaxation. Findings support non-specific blunting of physiological responsivity during pregnancy.

Associations of maternal psychological factors with umbilical and uterine blood flow.

OBJECTIVE: Alteration to blood flow in the maternal-foetal compartment has been proposed as a mechanism underlying maternal psychological effects on pregnancy outcomes. This study characterised the progression of umbilical and uterine blood flow resistance in healthy pregnancies and evaluated concurrent and longitudinal associations with maternal anxiety and other psychological factors. METHODS: The study assessed participants (n=107) at five visits spanning 24-38 weeks gestation. The resistance index (RI) in the uterine and umbilical arteries was measured with Doppler ultrasound. Maternal psychological function was assessed using validated, self-report instruments. RESULTS: Hierarchical linear modelling revealed that uterine and umbilical RI decreased during the second half of gestation, and that uterine RI was lower in nulliparous women. Few concurrent associations emerged between psychological factors and RI. Longitudinal analyses determined that psychological well-being was associated with decreased left uterine artery RI, and psychological distress was associated with lower right artery RI. CONCLUSIONS: Although uterine artery resistance was modestly associated with the maternal psychological milieu during gestation, our findings do not indicate an association between increased maternal distress and decreased RI. Thus, this study fails to affirm a key component of the hypothesised relation of maternal stress to foetal outcomes via vasoconstriction.

Maternal salivary cortisol differs by fetal sex during the second half of pregnancy.

Maternal salivary cortisol was measured at weekly intervals from 24 to 38 weeks gestation. The total sample consisted of 120 women enrolled in staggered intervals in such a way as to generate weekly measures of salivary cortisol during the latter half of pregnancy. Hierarchical linear modeling revealed the expected increase in unbound maternal cortisol during this period, with a slight deceleration in rate of increase at 33 weeks gestation. Women carrying male fetuses had higher levels of salivary cortisol initially as compared to women carrying female fetuses; at 30 weeks gestation there was cross-over such that higher maternal cortisol was observed in women carrying female fetuses beyond this time and through term. Results highlight the importance of considering fetal sex as a moderator of contemporaneous and predictive associations between maternal cortisol and prenatal or postnatal development.

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.

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.

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.

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.

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.

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.