Elsevier

Regulatory Peptides

Volume 108, Issues 2–3, 15 October 2002, Pages 149-157
Regulatory Peptides

Behavioral perinatology: Biobehavioral processes in human fetal development

https://doi.org/10.1016/S0167-0115(02)00102-7Get rights and content

Abstract

Behavioral perinatology is as an interdisciplinary area of research that involves conceptualization of theoretical models and conduct of empirical studies of the dynamic time-, place-, and context-dependent interplay between biological and behavioral processes in fetal, neonatal, and infant life using an epigenetic framework of development. The biobehavioral processes of particular interest to our research group relate to the effects of maternal pre- and perinatal stress and maternal–placental–fetal stress physiology. We propose that behavioral perinatology research may have important implications for a better understanding of the processes that underlie or contribute to the risk of three sets of outcomes: prematurity, adverse neurodevelopment, and chronic degenerative diseases in adulthood. Based on our understanding of the ontogeny of human fetal development and the physiology of pregnancy and fetal development, we have articulated a neurobiological model of pre- and perinatal stress. Our model proposes that chronic maternal stress may exert a significant influence on fetal developmental outcomes. Maternal stress may act via one or more of three major physiological pathways: neuroendocrine, immune/inflammatory, and vascular. We further suggest that placental corticotropin-releasing hormone (CRH) may play a central role in coordinating the effects of endocrine, immune/inflammatory, and vascular processes on fetal developmental outcomes. Finally, we hypothesize that the effects of maternal stress are modulated by the nature, duration, and timing of occurrence of stress during gestation. In this paper, we elaborate on the conceptual and empirical basis for this model, highlight some relevant issues and questions, and make recommendations for future research in this area.

Introduction

Developmental processes involved in transforming a single-cell human embryo into a fully functioning organism within a mere span of 40 weeks are exceedingly complex and fascinating; indeed, one would be hard pressed to come up with any other example in the physical or biological world that even begins to approximate the sheer elegance of intrauterine development. Biologists over the ages have asked the question: Does the genetic material of the fertilized egg already contain a full set of building specifications for the organism? Over the last decade or so, there has been a major paradigm shift in developmental biology regarding fundamental concepts of how the central nervous system and the rest of the organism develops and functions. The answer to the above question is now believed to be an unequivocal “no”. Genes and environment are no longer considered to exert separate influences, and development is viewed not as a gradual elaboration of an architectural plan preconfigured in the genes, but rather as a dynamic interdependency of genes and environment characterized by a continuous process of interactions in a place- and time-specific dependent manner, and involving short- and long-term information storage, whereby genetic and epigenetic processes,1 at every step of development, become represented in the evolving structural and functional design of the organism [1], [2], [3]. According to this epigenetic view of development, events at one point in time have consequences that are manifested later in the developmental process, and afferent activity has a profound influence on the developmental trajectory [4]. In other words, it appears that within the constraints imposed by the heritable germ line at conception, each developing organism plays an active role in its own construction. This dynamic process is effected by evolving various systems during embryonic and fetal life to acquire information about the nature of the environment, and to use this information to guide development. In the context of this formulation, not only does environment play a necessary role for development to occur, but the nature of the environment may play either an advantageous role for normal or optimal development, or a pernicious role to harm development [5].

Behavioral perinatology is broadly defined as an interdisciplinary area of research that involves conceptualization of theoretical models and conduct of empirical studies of the dynamic time-, place-, and context-dependent interplay between biological and behavioral processes in fetal, neonatal, and infant life using an epigenetic framework of development. The biobehavioral processes of particular interest to our research group relate to the effects of maternal pre- and perinatal stress and maternal–placental–fetal stress physiology. Our choice of stress and stress physiology is guided by the following two major considerations: First, empirical studies in humans and animals support a significant role for pre- and perinatal stress as an independent risk factor for adverse developmental outcomes [6]. Second, stress and stress physiology offer an excellent model system for the study of early developmental processes because it appears that the developing fetus acquires and incorporates information about the nature of its environment via the same systems that in a developed individual are known to mediate adaptation and central and peripheral responses to challenge/stress (i.e. the neuroendocrine, immune, and vascular systems) [7], [8].

We propose that behavioral perinatology research may have important implications for a better understanding of the processes that underlie or contribute to the risk of at least three sets of outcomes: prematurity, adverse neurodevelopment, and chronic degenerative diseases in adulthood. Each of these classes of adverse health outcomes represents major public health issues in the United States and other developed nations, their prevalence is characterized by substantial disparities along factors associated with sociodemographic disadvantage and racial/ethnic minority status (which we and others have argued may, in part, reflect the effects of variations in stress and stress physiology in affected populations), and growing evidence supports a crucial role for early developmental process in their origins [4], [9], [10], [11], [12].

Section snippets

Biobehavioral model of prenatal stress and stress physiology in human fetal development

From a biological perspective, the term “stress” is used to describe any physical or psychological challenge that threatens or is perceived to have the potential to threaten the stability of the internal milieu of the organism (homeostasis). The neuroendocrine, immune, and vascular systems play a major role in adaptation to stress. The principal effectors of these adaptive responses are the corticotropin-releasing hormone (CRH) and locus ceruleus–noradrenaline (LC–NA)/autonomic (sympathetic)

Prenatal stress and fetal developmental outcomes: overview of epidemiological findings

Disruption of reproductive function in mammals is a well-known consequence of stress. Results from experimental approaches in animal models strongly support a causal role for prenatal stress as a developmental teratogen, with large effects of even relatively mild behavioral perturbation in pregnancy on outcomes including, but not limited to, maternal–fetal physiology, length of gestation, and fetal growth [6], [23], [24], [25], [26], [27]. Psychosocial/behavioral stress in human pregnancy has

Prenatal stress and physiological processes in human fetal development: role of placental cotricotropin-releasing hormone

Fetal growth and development involves a complex interplay of factors and signaling molecules within the maternal, placental, and fetal tissues. Pregnancy is associated with major alterations in physiological function, including changes in hormone levels and control mechanisms (feedback loops) that are crucial in providing a favorable environment within the uterus and fetus for cellular growth and maturation and conveying signals when the fetus is ready for extrauterine existence [14]. Fetal

Conclusions, issues, and future directions

Adverse fetal developmental outcomes and their sequela are recognized as significant health problems in the United States. Women reporting high levels of pre- and perinatal stress are, on average, twice as likely to experience an adverse outcome as women reporting low levels of stress. Although the magnitude of this effect of prenatal stress is comparable to that of other “established” obstetric risk factors, the specificity and sensitivity of these measures as predictors of adverse outcome(s)

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