A rapidly accumulating literature indicates that the prenatal period must be taken into account if we are to understand development of the central nervous system (CNS) across the life span. Evidence now suggests that intrauterine signals influence brain structure and affect cognitive function and emotional and physiological stress regulation in the offspring. Furthermore, prenatal hormone exposures are critical for priming the maternal brain for the challenges of motherhood and have implications for the mother's brain structure and function that may last the rest of her lifetime. Just as the reciprocal nature of the parent-child relationship must be understood during the postnatal period, in order to understand the persisting influences of the intrauterine environment on neurodevelopment, the effects of the prenatal environment on both fetus and mother, as well as their reciprocal influences, must be appreciated. This is critical because the same hormones that program fetal development are those that shape the maternal brain and because prenatal bidirectional signaling may provide an adaptive function for both mother and fetus. © Association for Psychological Science 2011.

The fetal phase of life has long been recognized as a sensitive period of development. Here we posit that pregnancy represents a simultaneous sensitive period for the adult female with broad and persisting consequences for her health and development, including risk for psychopathology. In this review, we examine the transition to motherhood through the lens of developmental psychopathology. Specifically, we summarize the typical and atypical changes in brain and behavior that characterize the perinatal period. We highlight how the exceptional neuroplasticity exhibited by women during this life phase may account for increased vulnerability for psychopathology. Further, we discuss several modes of signaling that are available to the fetus to affect maternal phenotypes (hormones, motor activity, and gene transfer) and also illustrate how evolutionary perspectives can help explain how and why fetal functions may contribute to maternal psychopathology. The developmental psychopathology perspective has spurred advances in understanding risk and resilience for mental health in many domains. As such, it is surprising that this major epoch in the female life span has yet to benefit fully from similar applications.

Introduction

The developmental origins of disease or fetal programming model predicts that intrauterine exposures have life long consequences for physical and psychological health. Prenatal programming of the fetal hypothalamic-pituitary-adrenal (HPA) axis is proposed as a primary mechanism by which early experiences are linked to later disease risk. Areas covered: This review describes the development of the fetal HPA axis, which is determined by an intricately timed cascade of endocrine events during gestation and is regulated by an integrated maternal-placental-fetal steroidogenic unit. Mechanisms by which stress-induced elevations in hormones of maternal, fetal, or placental origin influence the structure and function of the emerging fetal HPA axis are discussed. Recent prospective studies documenting persisting associations between prenatal stress exposures and altered postnatal HPA axis function are summarized, with effects observed beginning in infancy into adulthood. Expert commentary: The results of these studies are synthesized, and potential moderating factors are discussed. Promising areas of further research highlighted include epigenetic mechanisms and interactions between pre and postnatal influences.

Mental illnesses originate early in life, governed by environmental and genetic factors. Because parents are a dominant source of signals to the developing child, parental signals - beginning with maternal signals in utero - are primary contributors to children's mental health. Existing literature on maternal signals has focused almost exclusively on their quality and valence (e.g. maternal depression, sensitivity). Here we identify a novel dimension of maternal signals: their patterns and especially their predictability/unpredictability, as an important determinant of children's neurodevelopment. We find that unpredictable maternal mood and behavior presage risk for child and adolescent psychopathology. In experimental models, fragmented/unpredictable maternal care patterns directly induce aberrant synaptic connectivity and disturbed maturation of cognitive and emotional brain circuits, with commensurate memory problems and anhedonia-like behaviors. Together, our findings across species demonstrate that patterns of maternal signals influence brain circuit maturation, promoting resilience or vulnerability to mental illness.

Mental illnesses originate early in life, governed by environmental and genetic factors. Because parents are a dominant source of signals to the developing child, parental signals - beginning with maternal signals in utero - are primary contributors to children's mental health. Existing literature on maternal signals has focused almost exclusively on their quality and valence (e.g. maternal depression, sensitivity). Here we identify a novel dimension of maternal signals: their patterns and especially their predictability/unpredictability, as an important determinant of children's neurodevelopment. We find that unpredictable maternal mood and behavior presage risk for child and adolescent psychopathology. In experimental models, fragmented/unpredictable maternal care patterns directly induce aberrant synaptic connectivity and disturbed maturation of cognitive and emotional brain circuits, with commensurate memory problems and anhedonia-like behaviors. Together, our findings across species demonstrate that patterns of maternal signals influence brain circuit maturation, promoting resilience or vulnerability to mental illness.

Fetal detection of adversity is a conserved trait that allows many species to adapt their early developmental trajectories to ensure survival. According to the fetal-programming model, exposure to stressful or hostile conditions in utero is associated with compromised development and a lifelong risk of adverse health outcomes. In a longitudinal study, we examined the consequences of prenatal and postnatal exposure to adversity for infant development. We found increased motor and mental development during the 1st year of life among infants whose mothers experienced congruent levels of depressive symptoms during and after pregnancy, even when the levels of symptoms were relatively high and the prenatal and postnatal environments were unfavorable. Congruence between prenatal and postnatal environments prepares the fetus for postnatal life and confers an adaptive advantage for critical survival functions during early development.