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DiPietro J A, Prenatal Development. In: Encyclopedia of Infant and Early

Childhood Development, ed. by Marshall M. Haith and Janette B. Benson. © 2008, Academic Press, San Diego

See also: AIDS and HIV; Birth Complications andOutcomes; Breastfeeding; Endocrine System; PrenatalDevelopment; Screening, Prenatal; Teratology.

Suggested Readings

Alexander GR and Kotelchuck M (2001) Assessing the role andeffectiveness of prenatal care: History, challenges, and directions forfuture research. Public Health Reports 116: 306–316.

American Academy of Pediatrics and American College ofObstetrics and Gynecology (2000) Guidelines for Perinatal Care, 5thedn. Elk Grove Village, IL: American College of Obstetrics andGynecology.

American College of Obstetricians and Gynecologists (1995) ACOGtechnical bulletin. Preconceptional care. International Journal ofGynaecology and Obstetrics 50: 201–207.

Expert Panel on the Content of Prenatal Care (1989) Caring for OurFuture: The Content of Prenatal Care. Washington, DC: PublicHealth Service.

Harold S (1980) Obstetrics and Gynecology in America: A History,pp. 142–145. Chicago, IL: The American College of Obstetriciansand Gynecologists.

Institute of Medicine (1985) Committee to Study the Prevention of LowBirth Weight. Preventing Low Birth Weight.Washington, DC: NationalAcademy Press.

Institute of Medicine Committee on Nutritional Status During Pregnancyand Lactation, Food and Nutrition Board (1990) Nutrition DuringPregnancy Part I: Weight Gain. Washington, DC: National AcademicsPress.

Johnson K, Posner SF, Biermann J, et al. (2006) CDC/ATSDRPreconception Care Work Group; Select Panel on PreconceptionCare. Recommendations to improve preconception health andhealthcare – United States. A report of the CDC/ATSDRPreconception Care Work Group and the Select Panel onPreconception Care. MMWR Recommendation and Reports.55(RR-6): 1–23.

Lu MC, Kotelchuck M, Culhane JF, Hobel CJ, Klerman LV, andThorp JM, Jr. (2006) Preconception care between pregnancies:The content of internatal care. Maternal and Child Health Journal10(7): 107–122.

Lu MC, Tache V, Alexander G, Kotelchuck M, and Halfon N (2003)Preventing LBW: Is prenatal care the answer? Journal ofMaternal-Fetal Neonatal Medicine 13: 362–380.

Relevant Websites

http://www.aap.org – American Academy of Pediatrics, Dedicated tothe Health of Children.

http://www.acog.org – American College of Obstetricians andGynecologists, Women’s Health Care Physicians.

http://www.marchofdimes.com – March of Dimes, Saving babies,together.

http://www.otispregnancy.org – Organization of Teratology InformationSpecialists.

http://www.cdc.gov – US Department of Health and Human Services.Centers for Disease Control and Prevention, Division of ReproductiveHealth: Home.

http://mchb.hrsa.gov – US Department of Health and Human ServicesHealth Resources and Services Administration, Maternal and ChildHealth Bureau.

604 Prenatal Care

Author's personal copy

Prenatal DevelopmentJ A DiPietro, Johns Hopkins University, Baltimore, MD, USA

ã 2008 Elsevier Inc. All rights reserved.

Glossary

Age of viability – The lowest gestational age at

which survival following delivery is possible, typically

with significant technological support. The most

commonly accepted current gestational age of

viability is 23weeks’ gestation.

Anteflexion and retroflexion – Forward and

backward bending of the body or body part.

Circadian rhythms – A daily cycle of behavioral or

biological patterns.

Gestation – The period of time from fertilization to

birth. In humans, this encompasses 266 days or

approximately 38weeks.

Habituation and dishabituation – Habituation is

response decrement to repeated presentations of an

unchanging stimulus. Dishabituation refers to

resumption of response following presentation of a

Encyclopedia of Infant and Early Childhood

different stimulus than that used to evoke

habituation.

Neurobehavior – Measurable features of

developmental functioning that are maturational in

nature and are presumed to reflect the underlying

neural substrate.

Neuroendocrines – Hormones that mediate

interactions between the nervous system and the

endocrine (hormonal) system Neuroendocrines are

released into the blood in response to nervous

system stimulation.

Ontogeny – The origin and development of an

individual from embryonic period to adulthood.

Post-term birth – Delivery following 42weeks’

gestation.

Pre-term birth – Delivery prior to 37weeks’

gestation.

Development (2008), vol. 2, pp. 604-614

Prenatal Development 605


Introduction

A single, fertilized cell develops into the complex organ-ism that is a human newborn infant in just 266 days. Theexplosive rate of growth and development during thisperiod is unparalleled at any other point in the lifespan.A resurgence of interest in the prenatal period as a stagingperiod for well-being and disease in later life has beenfostered by the enormous attention devoted to the hypo-thesis of ‘fetal programming’ advanced by D. J. Barker andcolleagues. This rapidly emerging field of study focuses onthe role of maternal and fetal factors in adult organfunction, including the brain and nervous system. Thatearlier circumstances, including those during the prenatalperiod, might affect later development is hardly news-worthy to developmentalists. In 1929, the foundationof the Fels Research Institute in Yellow Springs, Ohio,was based on a longitudinal study of child growth anddevelopment that commencedwith intensive investigationof the fetal period. Although investigators had limitedaccess to the fetus due to the primitive research toolsavailable to them, their research questions and orientationwere truly prescient and the results they generated weresurprisingly consistent with more recent findings usingmore sophisticated technologies.

Human gestation encompasses the period of time fromconception to birth. By convention an additional 2 weeksis added to account for the average period of time betweenthe last menstrual period and ovulation so that the aver-age term gestation is 40weeks long or 280 days. However,normal full-term birth spans the gestational period from37 to 41weeks. Pregnancies that end before 37weeks arereferred to as pre-term; those at and beyond 42weeksare post-term. Survival of preterm infants has improveddramatically during the last several decades as a result ofimprovements in neonatal intensive care. However, theage of viability, or the earliest gestational age at whichsome babies can survive with aggressive technologicalsupport, is currently 23weeks’ gestation. Prior to thistime, development of the respiratory and other organsystems is insufficient to sustaining extrauterine life. Atthe other end of the spectrum, pregnancies that last toolong are also hazardous. However, current obstetric prac-tices have drastically reduced post-term gestationsthrough the use of induced or surgical deliveries.

The fertilized ovum enters the uterine cavity shortlyafter conception. Mitotic division generates the blasto-cyst, a hollow ball of cells that becomes implanted in thewall of the uterus within the first 2 weeks. Weeks 2–8comprise the embryonic period, during which time dif-ferentiation of organs and structures proceeds rapidly. Bythe ninth week after conception, approximately 95% ofall structures within the body are developed although theembryo weighs less than 10 g and is only 50 mm long. Thisweek also marks the transition from the embryonic to fetal

Encyclopedia of Infant and Early Childho

period, although there is no clear physical demarcation.The embryo and fetus develop in the intrauterine cavitywithin an amniotic sac, which is filled with amniotic fluid.During the embryonic period, the structures necessaryto support development originate and progress througha series of stages, ultimately resulting in the umbilical cordand placenta. The placenta provides nutrients, exchangesgases, and manufactures hormones vital to maintenance ofthe pregnancy. A mature placenta is intended to functionfor a full-term pregnancy; thus, post-term risks to thefetus are often due to the deterioration of the placenta’sability to optimally support the fetus. The circumstancesthat stimulate labor and delivery are not well understood,although there is significant evidence that signals from thefetus itself serve as impetus.

The fetal period proceeds until birth and is markedby final development of organ morphology and func-tion, including prolonged development of the brain andnervous system. The ‘hardware’ of the brain – neural tubeclosing, neuronal and glial cell proliferation andmigration –commences early in gestation, while the ‘software’ elementsof synapatogenesis, process elimination, and myelinationcontinue through term and after birth. Organs are mostvulnerable to insult when they are developing most inten-sively. Thus, exposure to potentially harmful substancesduring pregnancy has consequences for structural malfor-mations of most organ systems only during the embryonicperiod or shortly thereafter. However, the potential forharmful effects of functional brain development, withimplications for cognitive and behavioral developmentafter birth, persist throughout pregnancy. Figure 1 providesa schematic description of the shifting vulnerabilities duringgestation.

The terms growth and development are often usedinterchangeably but they refer to distinct processes.Growth is typically defined as an increase in cell size ornumber; development implies differentiation of functionor complexity. The remainder of this article focuses onfetal neurobehavioral development, a set of features ofprenatal functional development that are measurable andobservable functional indicators that are presumed toreflect development of the nervous system. The study offetal neurobehavioral development reflects a backward ordownward extension of principles and theories that havebeen applied since the early 1970s to characterize infantbehavior. In fact, developmentalists who study the fetuscommonly assert that ‘‘nothing neurologically interestinghappens at birth.’’ While it is obvious that birth presentstransitional challenges for a number of organ systems,such as the circulatory and respiratory systems, it is notwell recognized that by the end of gestation the fetusdemonstrates virtually the same behavioral repertoire asa newborn infant. Put another way, all behaviors exhibitedby neonates have been observed at some point during thefetal period.

od Development (2008), vol. 2, pp. 604-614

Dividing zygote,implantation, and

gastrulation

Notsusceptible to

teratogens

Common site of action of teratogen

Heart

Heart

CNS

Limbs

Eye Eye Ear Ear

Brain

External genitalia

Teeth

Palate

1 2 3 4 5 6 7 8 9 16 3820-36

Age of embryo (in weeks)

Major morphological abnormalities

Fetal period (in weeks) Full term

Prenatal deathFunctional defects and minormorphological abnormalities

Upper limbs

Heart

Eyes

Teeth

Palate

External genitalia

Ear

CNS

Lower limbs

Figure 1 Schematic representation of growth and development during gestation. Reproduced fromMoore KL and Persaud TV (1993)

The Developing Human: Clinically Oriented Embryology, 5th edn. Philadelphia: W.B. Saunders Company, with permission from Elsevier.CNS, Central Nervous Systems.

606 Prenatal Development


Development during the prenatal period proceeds alonga continuum, with behaviors becoming incrementally morecomplex and varied as gestation proceeds. Like all otherdevelopmental periods, the fetal period is not monolithic;behavior in the early fetal period is largely reflexive andinvolves the entire body while behavior near term is farmore fluid, integrated, and distinct. Although no otherdevelopmental period yields the same potential to revealthe complexities of human ontogeny, no other period ofdevelopmental inquiry is so heavily dependent on technol-ogy to answer even the most basic of questions. Beforeproceeding to detailing current understanding about prena-tal developmental ontogeny, a brief review regarding tech-nologies necessary to viewandmonitor the fetus is provided.

Fetal Monitoring Techniques

Although speculation about the nature of fetal behavior hasexisted since antiquity, the advent of real-time ultrasound inthe early 1970s enabled modern scientific investigation ofprenatal development. Visualization can reveal specificbehaviors (e.g., thumb-sucking), qualitative aspects ofmovement (e.g., fluidity of flexion and extension), structuralfeatures of the fetus (e.g., size), and characteristics of theuterine milieu (e.g., volume of amniotic fluid). In addition,refinement of techniques to monitor fetal heart rate and its


patterning, using Doppler ultrasound, has provided anotherimportant source of information regarding prenatal neuraldevelopment. Doppler has also generated techniques todetect fetal motor activity without ultrasound visualizationand makes it possible to measure the amount of blood flowand resistance in maternal and fetal vessels, includingumbilical, cerebral, and uterine arteries. The most recenttechnological advance is the development of three-dimen-sional (3D) and so-called four-dimensional ultrasound (i.e.,3D image plus addition of a fourth dimension of real timemotion) that allows visualization of details, such as fetalfacial expressions and hand movements, which were notpreviously possible. Figure 2 presents examples of tradi-tional two-dimensional (2D) and 3D images.

Although 3D technology holds great potential forfuture studies, it is yet to be implemented broadly. Almostall knowledge about human prenatal development hasbeen generated by information from a mixture of existingultrasound methods, including 2D ultrasound and fetalheart rate monitoring. Regardless of how sophisticatedultrasound may become in the future, the human fetuswill always remain slightly beyond our actual reach.

Fetal Neurobehavioral Development

Theoretical orientations regarding neurobehavioral devel-opment early in the postnatal period generally focus on


(a) (b)

Figure 2 Sample images (a) traditional two-dimensional ultrasound and (b) recently developed three-dimensional ultrasound.



four domains of functioning: autonomic, motor, state, andresponsive/interactive capacities. These domains are hier-archical in nature such that sufficient maturation of func-tion of each precedes emergence of the next. That is, inorder to sustain interaction with the environment, oneneeds to be able tomaintain a certain degree of state control;in order to maintain state control, one needs to inhibitunnecessary motor activity, and so on. Information aboutprenatal development can also be organized in this manneras their ontogenic origins are rooted firmly in the fetalperiod. In the fetus, the specific aspects of functioningwithin each domain include (1) fetal heart rate and itspatterning, (2) quantitative and qualitative aspects ofmotor activity, (3) the emergence and consolidation ofbehavioral states, and (4) interaction with the intrauterineand external environments.

Fetal Heart Rate

In infants and children, patterns inherent in continuouslymonitored heart rate are frequently used indicators of theautonomic nervous system. In particular, features of varia-bility in heart rate are considered to reflect the develop-ment of parasympathetic processes related to the vagusnerve (i.e., vagal tone) and have been linked to aspects ofinfant and child behavior and development. More infor-mation exists about the development of fetal heart ratethan any other domain. Noninvasive methods to measurefetal heart rate by placing a simple Doppler transducer onthe maternal abdomen have been commonly used inclinical obstetric practice and research for decades and agreat deal is known about development of components ofthe fetal heart rate. A fetal heart beat is detectable nearthe sixth gestational week. As the cardiac system rapidlydevelops, heart rate increases over the next 4 weeks to abaseline rate of approximately 160 beats per min (bpm).Heart rate declines to approximately 135–140 bpm byterm, although normal limits span a wide range.


Patterns in fetal heart rate during the prenatal periodand labor are more revealing about nervous system devel-opment than is heart rate. In fact, the principal meansavailable to determine general fetal well-being or distressrelies on the direction and magnitude of periodic fluctua-tions in heart rate. Fetal heart rate that is characterized byvariability over time and includes transient, acceleratoryexcursions of heart rate well above baseline is interpretedas a reassuring sign of fetal health. In contrast, lack ofvariability and deceleratory episodes (i.e., significantslowing of heart rate well below baseline levels) can beindicative of neural compromise or distress. The heart ratedecline observed during gestation is accompanied by anincrease in the number and size of accelerations, a reduc-tion in deceleratory periods, and an increase in beat to beatand longer-term components of heart rate variability. Bothhave been attributed to changing cardiovascular needs andcardiac functioning in the developing fetus that have bothnon-neural and neural influences.Maturational changes inthe innervation of sympathetic and parasympathetic auto-nomic processes and progressive assumption of higherlevels of central mediation are among the neural compo-nents of these gestational changes.

Fetal Motor Activity

During gestation, fetal movement progresses fromuncoordinated movements that involve the entire bodyto more integrated, narrow, behavior patterns. Spontane-ously generated motor activity is present during theembryonic and early fetal periods. Figure 3 showsthe gestational age at emergence of 15 types of motorbehaviors studied in a sample of 11 fetuses observed onultrasound at weekly intervals early in gestation.

There is progression in the emergence of each behav-ior, from the least to the most differentiated. In addition,there is greater individual discrepancy in the emergenceof more complex patterns, suggesting that these may be


Any movement discernible

Startle reflex

General movements

Hiccups

Isolated arm movements

Isolated leg movements

Head retroflexion

Head rotation

Hand−face contact

Breathing movements

Jaw opening

Stretching

Head anteflexion

Yawn

Sucking, swallowing

Weeks of gestation

7 8 9 10 11 12 13 14 15 16 17 18 19 20

Figure 3 Gestational age of emergence of specific fetal motor behaviors in a sample of 11 fetuses viewed serially with ultrasound.

Adapted from de Vries J, Visser G.H, and Prechtl HF (1982) The emergence of fetal behaviour. I. Qualitative aspects. Early HumanDevelopment 7: 301–322.



more reflective of the development of higher-order brainprocesses. Note that this figure shows only the firstobserved incidence for each; once a behavior is expressed,it continues to persist throughout gestation.

Specific movements are believed to serve preparatoryor functional roles that increase survivability at birth. Forexample, fetal breathing motions begin early in gestationand become more common over time, so that by term thefetus exhibits fetal breathing movements approximately athird of the time. Although air is not a component of theintrauterine environment and these movements serve norole in oxygen regulation, they probably reflect rehearsalof behavior patterns of the diaphragm and other musclesthat are central to respiration. Fetal hiccupping and yawn-ing are commonplace although neither has clear func-tional significance. However, fetal sucking movements ingeneral and thumb-sucking in particular are also commonactivities that may strengthen neural connections neces-sary for the successful transition to postnatal feeding. Italso suggests that non-nutritive sucking (i.e., sucking thatis not associated with nutrition) may serve a self soothingor regulatory role both before and after birth. Otherbehaviors play clear roles in optimizing the intrauterineenvironment. For example, fetal swallowing assists in reg-ulation of the amount of amniotic fluid present. Develop-ment begins with the fetus in a breech, or head upposition; fetal motor behaviors consistent with steppingalong the intrauterine wall have been observed as thefetus makes the transition from a breech to vertex position


(i.e., head down) position midway through gestation. Thishas raised speculation that some fetuses that remainbreech by the time of delivery differ in their motor devel-opment from those who successfully assume the vertexpresentation.

Animal models have provided developmental psycho-biologists with an important source of information tostudy the adaptive significance of specific behaviors priorto birth because they may be studied either with specialpreparation of eggs, for precocial avian species, or withpreparations that make viewing the developing fetus moreaccessible in mammalian species. For example, newbornrat pups display a specific type of locomotion that isnecessary to early survival but disappears soon afterbirth; this coordinated behavior originates during the pre-natal period. Experimental manipulations in animal mod-els have also served to identify basic mechanisms andprogressions of behavioral expression in the developingembryo of fetus as well as the contributions of both inter-sensory experience and the intrauterine environment inshaping ontogeny.

Fetal movements are normally not felt by pregnantwomen until the 16th to 18th week of pregnancy. Afterthis time, women perceive most large amplitude, prolongedmovements but are poor detectors of other spontaneousor evoked fetal movements, detecting as few as 16% ofmovements at term. This makes reliance onmaternal reportan unsuitable source of data in studies of fetal motor activ-ity; instead investigators rely on ultrasound-visualized or




Doppler-detected measurement of fetal motor behavior.Most longitudinal studies report that the fetus becomesless active as gestation advances although movement ampli-tude or intensity increases as the fetus becomes larger.Inhibition of behavior is considered a hallmark of earlychild development in the postnatal period; thus, this patternappears prenatally. In the latter half of gestation, fetusesmove approximately once per minute, and are activebetween 10% and 30% of the time. Such estimates vary,in part, because of differences in how the end of onemovement and beginning of the next are defined. Fetalactivity patterns exhibit rhythmic periodicities during rela-tively short cycles during the day as well as circadianrhythms, with fetal motility peaking late in the evening.Although sex differences in motor activity are commonlyobserved in studies of infants and young children, sexdifferences in fetal motor activity are not apparent.

Fetal Behavioral State

During the second half of gestation, fetal heart rate andmovement patterns become integrated such that fetal heartrate increases and becomes more variable when the fetus ismoving and is lower and less variable when the fetus is still.This coupling develops in a predictable fashion and hasbeen most often attributed to centrally mediated co-activa-tion of cardiac and somatomotor processes; thus, it providesinformation regarding the integration of neural processes.Near 32weeks’ gestation, coupling of these two aspects ofdevelopment is joined by synchronous activity of otherkinds, particularly fetal eye and breathing movements. Inthe late 1970s, investigators determined that periods inwhich there were predictable co-occurrence of specificpatterns in three parameters – heart rate, motor activity,and eye movements – represented behavioral states thatcorrespond to the sleep–wake states observed in the new-born. Four fetal behavioral states were discerned, labeled1F, 2F, 3F, and 4F, in concert with state scoring methodsdeveloped for neonates. These fetal states approximatequiet sleep (1F), rapid eye movement (REM) sleep (2F),quiet waking (3F), and active waking (4F). Investigationsconducted since that time tend to confirm the relativecomparability of these states to those of newborn infants.In the postnatal period, behavioral state provides the con-text for evaluating and interpreting all other behaviors. Asthe fetus matures, state parameters gradually develop link-age between two parameters and ultimate coincidenceaccompanied by predictable state transitions during whichnear-simultaneous changes occur in all parameters. Maturestates do not emerge until near 36weeks; prior to that time,fetuses are most often observed in either indeterminatestates or those that are best characterized simply as generalperiods of quiescence or activity, and the transitionsbetween them are indistinct. Figure 4 presents characteris-tic recordings of 8min each of a fetus in quiescence and


activity. Understanding of the central mechanisms underly-ing maturation of state in the fetus are not yet well eluci-dated although patterning in temporal activation linked tothe reticular formation has been implicated.

Once states coalesce, fetuses spend most of the time ineither quiet or active sleep. Periods that seem consistentwith wakefulness are less common, and in particular,episodes in which the fetus seems to be both quiet andawake are rarely observed, leading some to speculate thatsuch a period either does not exist, or that perhaps inves-tigators do not know how to recognize it. The newborninfant also expresses a fifth behavioral state encompassingfussiness and crying, but such activity is not included inthe traditional definitions of fetal states. However, ifdevelopmentalists are to stand behind their observationthat the newborn behaves in the same way as a near termfetus does, prenatal crying should exist. Because thelarynx must be surrounded by air to produce an audiblecry, but this is not the case in the fetus, other indicators ofcrying would need to be detectable. Anecdotal evidenceof fetal crying has existed for a number of years, andrecently ultrasound has identified inspiratory and expira-tory diaphragmatic patterns that appear to be a fetalanalog to an infant crying in response to a loud sound. Itis important to note, however, that if this fifth state isconfirmed, it, like other states, appears only near theend of gestation.

Fetal Responsivity

Human fetal sensory systems develop in an analogousorder to those of nonprimate species: cutaneous, vestibu-lar, auditory, and lastly, visual. It is fairly well acceptedthat the fetus has the capacity to feel pain and othersensations, but again, this would be expected from aneurological basis only near the end of term. The fetusexhibits behaviors that seem to generate informationabout the intrauterine environment – grasping the umbil-ical cord, licking the placenta, pushing off the uterine wallwith hands and feet. Interest in demonstrating fetalresponsivity to stimuli originating outside the uterusdates to the 1930s Fels Study; preferred stimuli at thattime included door buzzers and warning horns. Womenoften report feeling fetal motor activity in response toloud sounds. More recently, fetal responses ranging fromheart rate surges, abrupt changes to an active behavioralstate, and startles to more subtle responses, includingbladder emptying and reduction in fetal breathing move-ments, have been generated using a variety of vibroacous-tic devices. Vibroacoustic stimulation refers to auditoryand/or vibratory stimuli activated on or near the maternalabdomen, usually above the fetal head. Because fetalhearing matures relatively early, and sound is efficientlyconducted in a dense medium (e.g., amniotic fluid), theuse of loud or intense stimuli has generated a number of


Heart rateBaseline

35

240

(a)

(b)

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60

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25

0

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36 37 38 39 40 41 42 43

35 36Time (min)

Time (min)

Fetal movement

Fetal movement

37 38 39 40 41 42 43

30 31 32 33 34 35 36 37 38

Heart rateBaseline

Figure 4 Doppler-generated segments over a period of 8min of fetal heart rate (upper, horizontal line) and fetal motor activity

(lower, vertical lines) in a fetus at 36weeks’ gestational age (a) reflecting periods of quiescence (1F) and (b) active waking (4F).



concerns about safety and the potential for causing fetaldiscomfort. Nonetheless, it is clear that from at least mid-way through gestation, the fetus can respond to stimulithat originate outside of the uterus.

The question of whether the fetus responds to morenuanced stimuli in a manner indicative of higher cognitiveor information processing is extraordinarily difficult toanswer conclusively. Consider for a moment the chal-lenges of assessing memory in infants. Babies cannotdirectly communicate what they know; they fall asleepunpredictably, have little motor control, and in general


behave in ways that limit our ability to test them. Add tothese challenges the additional feature of not being ableto actually see the subject of testing and you begin toapproach the difficulties of this type of fetal research.Nonetheless, the fetus seems capable of habituation, aprimitive form of sensory learning requiring responsedecrement to repeated presentations of invariant stimuli.Habituation, as measured by successive reductions inmotor and heart rate responses to vibroacoustic stimuli,has been observed late in pregnancy. Such observationssuggest that the mature fetus has rudimentary learning




capacities. However, because fetal research is technicallydifficult to implement and often not conducted with thesame experimental rigor as studies with infants, dishabi-tuation is often not assessed. This makes it difficult todetermine whether studies have shown true habituationin the fetus rather than simple response fatigue.

Given the difficulties in measuring subtle fetalresponses, most studies on fetal learning capabilitiesexpose fetuses to stimuli during gestation but test onrecognition after birth. Virtually all of these focus onfetal ability to learn features of auditory stimuli. Althoughthe intrauterine environment conducts external vibroa-coustic stimuli well, this is not the only source of auditorystimulation. The background noise level within the uterus,based on animal and human models, has been estimated tobe about 30 decibels, roughly consistent with the noiselevel in an average residence without a stereo on. Soundsare generated by maternal physiological processes (e.g.,cardiac, digestive sounds, and placental sounds) and par-tially absorbed exterior noises. External sounds of highfrequency generate greater intrauterine attenuation thanlow-frequency sounds. Prominent above this backgroundis the partially altered, but distinguishable, maternal voice,which is conveyed both through internally conductedvibrations of the vocal chords as well as externally throughthe uterine wall. Fetal responses to auditory stimuli can beelicited as early as 24weeks’ gestation, suggesting that thefetus has a history of exposure to the maternal voice that isat least 4months long.

Seminal work by DeCasper, Fifer, and colleaguesprovides the most convincing evidence for prenatallearning by examining whether newborn infants appearto recognize their own mother’s voice. Although thesestudies are based on relatively small samples, and involvecomplicated methods to assess voice recognition innewborns, such studies indicate that fetuses do learn todiscriminate their own mother’s voice from that ofanother woman and prefer listening to their mother’svoice. In addition, newborns prefer voices that are alteredto reflect the acoustical properties as experienced in uteroand voices that speak in their own language. Newborninfants can detect other maternal features, such as odor,suggesting that multidimensional maternal recognitionthat originates prior to birth may be adaptive for survivalafter birth. There is much less research on explicit effortsto expose fetuses to non-naturally occurring sounds in aneffort to evaluate associative learning. There is evidencethat fetuses can discern rhythmic variations in speechand musical stimuli detected by alterations in fetal behav-ior during stimulus onset. However, research on theability of fetuses to learn specific musical segments asmanifest by neonatal recognition is both preliminaryand inconclusive.

The idea that exposing fetuses to auditory stimuli forthe purpose of enhancing prenatal brain development or


providing direct tuition in, for example, classical music orother patterned stimuli, is absolutely unsubstantiated byexisting research. Although a number of commercial pro-ducts for fetal stimulation are available for purchase, theseare of dubious safety. In terms of efficacy, there is nocredible scientific evidence that providing extra externalstimulation to fetuses is beneficial, and a great deal ofsentiment that it may in fact be harmful. Because fetalhearing is relatively mature, and the basal uterine environ-ment relatively quiet, deliberate exposure to loud soundsmay, at best, interferewith normal sleep–wake cycles and, atworst, may harm fetal hearing. The intrauterine environ-ment is exquisitely tuned tomaximizing development of thefetal brain and nervous system and there is no compellingreason to expect that disturbing normal ontogeny wouldprovide benefit to it. In fact, evidence from animal modelssuggests that providing prenatal sensory stimulation beyondwhat is typically encountered for a species can result ininterference with normal development.

Factors That Influence Fetal Development

Developmental Discontinuity

Although there are progressive linear changes in heartrate, motor activity, state development, and sensory/interactive capacities over the course of gestation, thetrajectory of these changes shifts at a specific gestationalperiod. Such shifts, or periods of discontinuity, are com-mon during infant and child development and connote aperiod in which there is a qualitative shift in one or moredomains. The first commonly recognized discontinuityoccurs in the third month after birth, at which time infantsbecome more interactive and progress beyond newbornbehavior patterns. With respect to the development offetal behaviors, the period between 28 and 32weeks’ gesta-tion has emerged as a transitional period for maturationprior to birth. The discontinuity can be generalized asfollows: prior to 28–32weeks, the fetus displays imma-ture neurobehavioral patterns with a relatively steepdevelopmental slope; after 32weeks, the trajectory of de-velopment becomes significantly less steep. In some ways,a fetus that has passed this transition is more similar toa newborn than to an immature fetus. These observa-tions encompass most fetal parameters that change overgestation, including heart rate patterns, motor activity,fetal movement–heart rate coupling, fetal breathingmotions, and responsivity to stimuli. The onset of thesetrends coincides with a period of rapid increase in neuraldevelopment and myelination. This suggests that prenatalbrain development toward the end of pregnancy is some-what overdetermined and may serve as a protective mech-anism for early birth. Support for this position is providedby the ultimate developmental and cognitive success ofpre-term infants who are born after this gestational




period, despite immaturity in other organ systems. This isnot to imply that development ceases after this period, orthat certain aspects of fetal neurobehavior do not con-tinue to develop in a linear fashion. For example, there is alinear increase in periods of wakefulness for fetuses thatare post-term. However, at the very least, decelerativetrajectories indicate that the rate of fetal maturationpeaks early in the third trimester and begins to taper offwell before term.

Fetal Congenital Anomalies and PregnancyRisk Factors

If fetal neurobehaviors reflect the developing nervoussystem, it would be expected that factors with knownneurotoxicity or that jeopardize normal pregnancieswould also affect expression of fetal neurobehavior.Indeed, fetuses afflicted with a variety of chromosomalanomalies or malformations, including Down syndromeand neural tube defects, show variation in normal fetaldevelopment. This includes fetuses whose physical growthis proceeding below normal limits (i.e., intrauterinegrowth restriction). Exposure to a variety of potentialteratogens (including alcohol, nicotine, methadone, andcocaine) has also been shown to affect various aspects ofnormal behavioral development. Fetuses of women withconditions that threaten pregnancy and change fetalgrowth, such as diabetes, exhibit differences in develop-ment, in this case presumably due to alterations in glucosemetabolism and availability. However, despite the poten-tial for detection of fetal compromise, the field is notsufficiently advanced to be able to predict poor develop-mental outcomes after birth based solely on detection ofatypical patterns of fetal neurobehavior.

The Maternal Context

The psychological bond between mother and child hasbeen extolled throughout history and literature but thereis relatively scant scientific information on the inception ofthis relationship prior to birth. Whereas the knowledgebase concerning neurobehavioral development is quitebroad because it has been a subject of investigation forover 25 years, information on the maternal–fetal interfaceis quite new and much of it requires additional replicationand scientific investigation. There are no direct neuralconnections between the mother and the fetus. Thus, toaffect the fetus, maternal psychological functioning mustbe translated into physiological effects. This translationmay occur through a number of processes, including directtransmission of neuroendocrines to the fetus through theplacenta, alterations in maternal blood flow that affectlevels of oxygen and nutrients available to the fetus, orchanges in the intrauterine milieu that the fetus maydetect through sensory channels.


Fetal behavior exhibits circadian rhythms. For exam-ple, fetal heart rate is lowest in the early morning hoursand fetal motor activity peaks in the evening. However,during daytime hours, there are no consistent peaks orvalleys of fetal activity or inactivity. It is unclear how orwhether maternal diurnal patterns contribute to theobserved fetal variations. Most information on whethermaternal states influence the fetus has been generated bystudies that monitor the fetus during periods of maternalarousal, induced through either physical exertion, includ-ing exercise, or mild psychological stress. Both have beenassociated with subtle alterations in fetal neurobehavioralfunctioning during the period of exposure.

There are a few studies that attempt to correlate mater-nal psychological attributes or experiences, including anxi-ety and stress perception, with fetal neurobehavior andlonger-term outcomes in children. This interest has beensparked by evidence from animal models suggesting thatchronic stress during pregnancy interferes with prenatalbrain development in a manner that generates persistentand deleterious effects on postnatal development. However,to extrapolate these findings to assume that there must besimilar effects on human fetuses may not be wise given thenature of how stress is conceptualized and measured.

In animal models, subjects are exposed to a series ofexperimental procedures that are controlled in terms ofduration, frequency, and intensity. In contrast, humanstudies necessarily rely on measuring the elusive con-struct of psychological stress during pregnancy and thenobserving whether there are associations with child devel-opment years later. Maternal psychological distress beforeand after pregnancy are related, and there are well-knownenvironmental influences of maternal distress on childrearing. Because what is measured in virtually all humanstudies of ‘stress’ during pregnancy is maternal affect andemotional responses to daily circumstances in women’slives, it makes it difficult to know with certainty that thereis a causal association and that other factors, includinggenetic mechanisms, are not involved. Moreover, thehandful of studies that have detected deleterious effectsof maternal pregnancy distress on developmental out-comes have yielded inconsistent and unreplicated results,including evidence of a paradoxical response of ‘acceler-ated’ postnatal development in children whose mothersreported moderately high levels of anxiety and stress.

When child development research was in its infancy,the common perception was that actions of parents ingeneral, and mothers in particular, influenced the child.An influential paper by Bell in the 1960s introduced theconstruct of an opposite direction of effects: that parentalbehavior is directly influenced by characteristics andbehavior of the child. Similarly, prenatal studies ofdevelopment have focused on how pregnant women affectthe fetus. Recent evidence indicates that the maternal–fetal link is also bidirectional. Specifically, fetal motor




activity in the second half of pregnancy stimulates epi-sodic sympathetic surges in the maternal autonomic ner-vous system, even when women are unaware that the fetushas moved. Such maternal sympathetic activation by thefetus may serve as a signal function to the pregnantwoman in preparation for the consuming demands ofearly child rearing. At the same time, pregnancy appearsto result in maternal hyporesponsivity to environmentalchallenges; taken together these phenomena may serve todirect maternal resources away from less relevant envi-ronmental demands. As with postnatal maternal–childinteraction, the best model for maternal–fetal interactionmay be a transactional one, in which each influences theother in a dynamic cycle of reciprocity, but there is muchto be learned in this regard.

Continuities from Fetus to Child

Investigation of normative development during gestationhas been the focus of most of the research to date. Thestudy of individual differences in fetal functioning andimplications for predicting to postnatal development hasbeen largely relegated to clinical applications. The pro-gression from an age-based focus to interest in individualdifferences among fetuses parallels that observed in infantresearch. Do individual differences begin before birth?The presumption is that because there is wide variabilityin neurobehavioral development at birth, this range ofindividuality must begin prior to birth. There is goodevidence that fetal neurobehaviors are relatively stablewithin individuals over time during gestation, therebysatisfying a primary requirement in their establishmentas an individual difference. Unfortunately, there are notenough scientific investigations in which fetal neurobeha-vioral measures are examined in relation to child develop-mental or temperamental outcomes to be utterlyconclusive. It is difficult to design such studies becausethe nature of the measures of specific domains of functionas well as the methods needed to measure them are quitedifferent in fetuses and children. However, those that havebeen undertaken reveal that there are basic continuitiesbetween fetus and child. These studies fall into twocategories: those that attempt to document within-domainconsistency between similar aspects of function, and thosethat investigate cross-domain predictiveness. The lattercategory presupposes that there is conservation of rankordering across individuals from the fetal to infant periodson specific dimensions. Some degree of within-domainindividual consistency spanning from the fetus to youngchild has been found for heart rate and variability, motoractivity, and state control. This means that fetuses withfaster heart rates have faster heart rates in childhood; moreactive fetuses tend to be more active toddlers; and fetuses


that spend more time in quiet sleep tend to spend moretime in this state in infancy. Cross-domain predictions arebased on the consideration that some fetal measures aremarkers for general nervous system development, and assuch, should have predictive validity to later aspects offunctioning that have similar neural underpinnings. Thesestudies have focused on the associations between fetalneurobehavior and either subsequent infant temperamentor developmental proficiency. There is some evidence thatfetuses with greater heart rate variability and couplingbetween movements and heart rate show more maturedevelopmental outcomes in the first few years of life, andthere is a suggestion that fetal heart rate and motor activitypredict infant irritability and attentional performance.The current state of knowledge regarding the genesis andmeasurability of stable individual differences during theprenatal period is based on modest, single study findingsthat await replication and extension. Nonetheless, thereis both strong theoretical support as well as modest empir-ical support that the fetus is indeed the precursor tothe child.

Conclusions

The origins of development begin during the fetal period.Recent technological advancements have opened a win-dow to this period of ontogeny that has resulted in anexpanding field of inquiry. Substantial information existsto support the developmental progression of a range offetal neurobehaviors over the course of gestation. Less isknown about the manner in which individual differencesarise and are conserved after birth, and the ways in whichcharacteristics of the maternal and intrauterine environ-ments affect the fetus, and how the fetus may, in turn,affect these contributors to its own development.However, there is little doubt that the period beforebirth sets the stage for the entirety of human development.

See also: Auditory Development and Hearing Disorders;Birth Complications and Outcomes; Critical Periods;Habituation and Novelty; Newborn Behavior; PhysicalGrowth; Premature Babies; Prenatal Care; Screening,Prenatal; Teratology.

Suggested Readings

Barker DJ (1998) Mothers, Babies, and Health in Later Life. New York,NY: Churchill Livingstone.

de Vries JI, Visser GHA, and Prechtl HFR (1982) The emergence of fetalbehavior. I. Qualitative aspects.Early Human Development 7: 301–322.

DiPietro JA (2004) The role of prenatal maternal stress in childdevelopment. Current Directions in Psychological Science13: 71–74.




DiPietro JA (2005) Neurobehavioral assessment before birth. MentalRetardation and Developmental Disabilities Research Reviews11: 4–13.

Lecanuet JP and Schaal B (1996) Fetal sensory competencies.European Journal of Obstetrics & Gynecology and ReproductiveBiology 68: 1–23.

Lecanuet JP, Fifer WP, Krasnegor NA, and Smotherman WP (eds.)(1995) Fetal Development, a Psychobiological Perspective.New Jersey: Lawrence Erlbaum Associates.

Moon CM and Fifer WP (2000) Evidence of transnatal auditory learning.Journal of Perinatalogy 20: S36–S43.

Preschool and Nursery SchoolH H Raikes, C Edwards and J Jones-Branch, Univers

ã 2008 Elsevier Inc. All rights reserved.

Glossary

Asili nido – ‘Safe nests’, the Italian term for

infant–toddler centers.

Barnehage – ‘Children’s gardens’, care and

education programs for children aged 0–3 years,

in Norway.

Early childhood programs for children of age

3 years and under – Federal and state-supported

center-based programs, private nursery schools,

home visiting programs with a child development

emphasis, out-of home-enrichment programs for

children, and 0–3 programs that originated in

countries other than the US.

Early Head Start – A variation of the federal Head

Start program for children in poverty under the age 3

in over 700 US communities.

Ecole Maternelle Francaise (EMF) – Publicly

supported French nursery schools serving about a

third of French 2-year-olds.

Educare – High-quality 0–3 programs for children in

poverty that blend funding from Head Start and other

federal sources, states, localities and philanthropy,

coordinated by the Bounce Learning Network.

Even Start – Parent–child literacy program.

Home visiting programs – Regular home visitor

services offered in children’s homes to parents and

children for purposes of enhancing children’s

development. Examples of four programs are

provided in this section.

Out-of-home enrichment programs – Educational

programs for children under age 3 years that may

also include instruction for parents. Several

examples are included here.

Encyclopedia of Infant and Early Childhoo

Moore KL and Persaud TV (1993) The Developing Human: ClinicallyOriented Embryology, 5th edn. Philadelphia: W.B. SaundersCompany.

Nijhuis JG, Prechtl HFR, Martin CB, and Bots RS (1982) Are therebehavioural states in the human fetus? Early Human Development6: 47–65.

SmothermanWP and Robinson SR The development of behavior beforebirth. Developmental Psychology 32: 425–434.

Sontag LW and Richards TW (1938) Studies in fetal behavior:I. Fetal heart rate as a behavioral indicator. Monographs of theSociety for Research in Child Development 3(4 (Serial No. 17)): 1–67.

ity of Nebraska–Lincoln, Lincoln, NE, USA

Part C of the Individuals with Disabilities

Education Act – A program that provides services

for children under age 3 years with identified

disabilities.

Introduction

This article provides descriptions of nursery education forchildren under the age of 3 years, including an overviewof quality features for such programs, and descriptions ofcenter-based, home visiting, out-of-home enrichmentprograms, programs for 0–3 year olds that are identifiedwith other countries. It concludes with an overview ofextant research on the effects of early childhood programsfor 0–3 year olds.

Overview of Early Childhood Programs

Early Childhood Education (ECE) programs are highlyprevalent in the US and in European countries, and aregrowing in emphasis in other parts of the world today.Children under age 3 years participate in group or formaleducational experiences for a variety of reasons: (1) socialand cognitive preparedness for preschool or formalschooling or enrichment; (2) remediation or intervention;(3) to learn specific skills deemed important by parents; or(4) for childcare in order for parents to work or pursuetraining. ECE for children age 3 years and under (some-times referred to as nursery, creche, or infant–toddler

d Development (2008), vol. 2, pp. 604-614

this article was originally published in the encyclopedia of infant

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