Fetal and Infant Neurobehavioral Development
OxfordHandbooksOnline
FetalandInfantNeurobehavioralDevelopment:BasicProcessesand
EnvironmentalInfluences
CatherineMonkandAmieAshleyHane
TheOxfordHandbookofPerinatalPsychology(Forthcoming)
EditedbyAmyWenzel
OnlinePublicationDate: Oct
2014
Subject: Psychology,HealthPsychology,ClinicalPsychology
DOI: 10.1093/oxfordhb/9780199778072.013.20
AbstractandKeywords
Thischapterreviewstheliteratureexaminingfetalandinfantneurobehavioraldevelopment.Basicfetal
neurologicaldevelopmentandneurobehavioralfunctioningarereviewed.Majorfetalneurobehavioralmilestones
andtheirassessmentareaddressedandincludefetalbehavioralstates,heartrate,movement,andresponsivityto
stimuli.Theprocessesofneurologicalgrowthfrombirthtoage2arereviewed.Infantneurobehavioraldevelopment
isaddressedandincludesstateregulationandsleep,physicalgrowthandmotordevelopment,andthebasic
processesunderlyingsocial-emotionaldevelopment.Forfetusandinfant,researchexaminingtheassociations
betweenneurobehavioraldevelopmentandmaternaldistressandpovertyisreviewed.Theimplicationsforfuture
directionsinfetal-infantneurobehavioralresearcharediscussed.
Keywords:Prenataldevelopment,fetus,infant,mother-infant,neurologicaldevelopment,physiology
Thischapteronfetalandinfantneurobehavioraldevelopmentcoversbothperiodswithnearlyequalweight,
reflecting,inpart,thegreateraccessibilityofthefetustoresearchand,moresignificantly,theincreasingemphasis
ondevelopmentalrootsforlaterfunctioning,includingthosethattakeholdduringfetaldevelopment.Forboththe
fetusandinfant,wecoverbasicbraindevelopmentandkeyneurobehavioralmilestones,someofwhichoverlap
conceptually(i.e.,stateregulation),aswellasmicro-andmacrolevelcontextualfactorsthatappeartoinfluence
thedevelopmentaltrajectoriesateachtime:maternaldistressandpoverty.Whiletheorganizationcoversfirstthe
fetusonalltopicsandthentheinfant,ouraimistoemphasizethecontinuitiesbetweenfetalandinfant
neurobehavior,aswellastheirsharedorientationandvulnerabilitytotheirexternalworlds.
FetalBrainDevelopment
Fetalbraindevelopmentcanbedividedintothreeprimaryphases:embryonic,whichbeginsatconceptionand
extendsthroughtheeighthgestationalweek1;theearlyfetalperiod,whichextendsapproximatelytomidgestation;
andthelatefetalperiodlastingupuntilbirth.Bytheendoftheembryonicperiod,thebasicstructuresofthebrain
andcentralnervoussystem(CNS)areestablished.Theearlyfetalperiodiscriticalforthedevelopmentofthe
neocortexbecausemostcorticalneuronsaregeneratedduringthisperiod,andmanyhavemigratedtotheir
positionsintheneocortexandbeguntoformessentialconnectionsforfutureneuralcircuits(Stiles&Jernigan,
2010;Tau&Peterson,2010).Thelatefetalperiodseessignificantspecializationofeachneuralregionand
formationofdifferentcorticallayers,aswellasoverallmaturationofthebrain(Encha-Razavi&Sonigo,2003;Tau
&Peterson,2010).Atthemidpointofgestation,20weeks,thebrainweighsapproximately20g(ascomparedwith
350–400gatbirth)andhasallnecessarystructuresformaturefunctioning,buthasasmoothcorticalplate
becausethegyriandsulcihavejustbeguntoform(Encha-Razavi&Sonigo,2003;Fogliarinietal.,2005).These
fissuresbegintoappearbetween18and24weeksanddistinguishthefourlobesofthebrain.Developmentof
secondaryandtertiarysulcicontinuesthroughtheendofgestation.Thecorpuscallosum,whichbeginstodevelop
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Fetal and Infant Neurobehavioral Development
aroundthe12thweekofgestation,isrecognizableby21or22weeksandcontinuestodevelopfortheremaining
prenatalperiod(Encha-Razavi&Sonigo,2003).Throughoutthisdevelopment,changesingrossmorphologyofthe
neuralsystemareunderpinnedbychangesoccurringatthecellularlevel(Stiles&Jernigan,2010).
Duringthefirst2weeksofpostconceptiondevelopment,theembryoisasimple,oval-shaped,two-layered
structurewithtwotypesofmigratingcells,hypoblastsandepiblasts,formingdifferentlayersofthefuturefetus.The
hypoblastisclosesttotheblastocystcavityandmadeofcuboidalcellsthatwillgiverisetoextraembryonic
structures,includingtheliningoftheyolksac.Theepiblastisadjacenttothetrophoblastandgivesrisetoallthree
germlayersoftheembryo:ectoderm,mesoderm,andendoderm.Someoftheblastocystcellsdonotmigrateand
insteadremainintheepidermallayer,wheretheyaretransformedintowhataretermedneurectodermalstem
cells,whichwillgiverisetothebrainandCNS.Thesestemcellsalsoarereferredtoastheneuralprogenitorcells
and,asaregion,theneuralplate.Acomplexcascadeofmolecularsignalingengineersthisandother
differentiationandregionallocationofembryonicstemcells(Stiles&Jernigan,2010).Duringthethirdweekof
gestation,betweenembryonicday20–27,thefirstwell-definedneuralstructure,theneuraltube,isformedfromthe
foldingandfusionoftheneuralplate(Joseph,2000;Tau&Peterson,2010).Theneuralprogenitorcellsarelocated
withinthehollowcavityoftheneuraltube,whicheventuallywillbecometheventriclesystemofthebrain.Assuch,
thisareaiscalledtheventricularzone(VZ),whichwillberelevantforunderstandingfutureneuronalproduction.
Importantly,severallifestylefactors,suchasinadequatefolicacidandvitaminBandtheuseofantiepileptic
medicationssuchasvalproicacid(alsousedtotreatpsychiatricdisorders)cancauseneuraltubedefectsleading
toeitherspinabifidaoranencephaly(Artama,Ritvanen,Gissler,Isojarvi,&Auvinen,2006).Becausetheneural
tubeformsjustamonthpostconceptionandisessentialfornormaldevelopment,seeminglybenignexposurescan
dramaticallyimpactthechild’sfuturebeforeawomanevenknowssheispregnant.
Clicktoviewlarger
Figure1 Embryonicdevelopment.
Reprintedwithopen-accesspermissionfrom:
http://en.wikipedia.org/wiki/File:Development_of_nervous_system.svg.
By4gestationalweeks,therostralportionoftheneuraltubeformsthreeprimaryvesicles,theprosencephalon,
mesencephalon,rhombencephalon,whicharetheembryonicprecursorstotheforebrain,midbrain,andhindbrain,
respectively.By7gestationalweeks,fivesecondaryvesiclesemerge(seeFigure1).Specifically,the
prosencephalondifferentiatesintothetelencephalon(fromwhichwillemergethecerebralcortexandbasalnuclei)
anddiencephalon(thefuturethalamusandhypothalamus),andtherhombencephalondifferentiatesintothe
metencephalon(whichwillgiverisetotheponsandcerebellum)andthemyelencephalon(fromwhichwillemerge
themedulla).Themesencephalondoesnotfurtherdivide(Stiles&Jernigan,2010).Manyofthecranialnervesalso
areformedduringthisperiod.Thetransformationoftheoverallstructureoftheembryoreflectsspecificchangesat
thecellularlevel,specificallyinneuralpatterningthroughoutallregionsofthenervoussystem.Changesinthe
patterningoftheCNSbegininthisperiod,areacceleratedinthelatefetalperiod,andextendformanypostnatal
years(Stiles&Jernigan,2010).Embryonicneuralpatterning—thedifferentiationofdistinctbrainareasbasedon
theircellularorganizationandneuronalconnectivity—affectsallbrainregions;bytheendoftheembryonicperiod,
primitivepatterningofthesensorimotorregionswithintheneocortexisestablished,majorcompartmentswithinthe
diencephalicandmidbrainregionshavedifferentiated,andthesegmentalorganizationofthehindbrainandspinal
columnhavebeenlaiddown(Stiles&Jernigan,2010).
Duringtheearlyandlatefetalperiods(postembryonicdevelopmentendingatgestationalweek8),thegross
morphologyofthedevelopingbrainundergoesdramaticchanges,includingmovingfromasmooth,
“lissencephalic”structuretowardobtainingthecharacteristicmature“texture”ofelevatedridges(gyri)and
depressions(sulci).Duringtheseperiods,braindevelopmentcentersontheprocessesofneuronproduction,
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Fetal and Infant Neurobehavioral Development
migration,connections,anddifferentiation.
Thehumanbraincontainsbillionsofneurons,mostofwhichareproducedbymidgestation(Stiles&Jernigan,
2010).Duringtheembryonicperiod,neuralprogenitorcellsintheVZdividebywhatiscalleda“symmetrical”
modeofdivision,whichproducestwoidenticalneuralprogenitorcells.Bythefetalperiod,themodeofcelldivision
shiftsto“asymmetrical,”whichproducesoneprogenitorcellandoneneuron.Thenewprogenitorcellremainsand
continuestodivide,whereasthepostmitoticneuronleavestheVZtotakesitsplaceinthedevelopingneocortex.
Thismigrationultimatelyresultsintheformationofanorderlysix-layeredstructureknownasthelaminarstructure
ofthecerebralcortex.Migrationoccursalmostexclusivelyinan“inside-out”mannerinwhichdeepercortical
layersareformedbeforemoresuperficialones.Forthepostmitoticneurons,migrationoccursviaradialglialcells
thatserveasguidesonthepathofneuronstotheirfinaldestination.Otherneuronsthatemergefromtheventral
telencephalonwillmigratetangentially,thatis,paralleltothedevelopingcerebralcortexandthalamus,usinga
varietyofguidancemoleculesproducedinlocalregionsalongtheirroutetodirecttheirmovementintothecortex.
Neuronalmigrationpeaksbetweengestationalweeks12and20,islargelycompletebyweeks26–29,andisa
focusofstudywithrespecttoprenatalexposuresalteringfutureneurobehavioraldevelopment(seebelow)(Stiles
&Jernigan,2010;Tau&Peterson,2010),particularlyaspsychopathologynowisconceptualizedasbrain
disordersinvolvingneuralcircuits(Insel&Wang,2010).
Aspartoftheirmigration,neuronsextendaxonsanddendritestoappropriatesynapticpartners.Centraltothis
formationofearlysynapticconnectionsare“scaffoldingcells”(functioningsimilarlytoradialglialcells)and
moleculargradients.Thereiscontinualrefinementandmodificationinherentintheearlyconstructionofsynaptic
connections,andtheyareoftentransientplaceholderstothemorestableconnectionsthatcharacterizemature
circuits.Byweek5ofgestation,theearliestsynapticconnectionsareformed(Tau&Peterson,2010).Thisoccurs
withneuronslocatedinthefirstrecognizablecorticallayer,knownasthepreplate.Theneuronsinthepreplate
serveasinitialsynaptictargetsforneuronalprojectionsfromthedevelopingthalamusandbrainstem.Neurons
withinthepreplateformafunctionallyactiveneuralcircuit,althoughitisquiteprimitive.Withinthepreplateexists
thesubplate;byweeks18–22,itisthickerthanthepreplateandcorticalplate,whichformsoutofthepreplate.The
subplateisrichwithsynapsesandshowsevidenceofthelaminarorganization.Here,inthesubplate,neurons
receivepreliminaryafferentinputsfromthevisualandsomatosensorythalamus,cholinergicafferentsfromthe
basalforebrain,andmonoaminergicafferentsfromthebrainstem.Theseneuronshavethenecessarymolecular
componentsforfunctionalγ-aminobutyricacid(GABA)ergictransmission,whichisexcitatoryduringmuchofearly
development,servingtodepolarizeneuroblastsandcorticalneurons,therebyincreasingtheiractionpotential.
Subplateneuronsarecapableofpropagatingneuralsignalsacrossmonoaminergic,cholinergic,andglutamatergic
synapses.Itisclearthatthearchitectureofthemajorneurotransmittersystemsisinplacebyearlygestation,
althoughmuchremainstobediscoveredabouttheirroleinearlycorticaldevelopment.Moreover,thisemerging
understandingofearlybraincircuitryindicatesthatfetalexposuretofactorsthatinfluencesignaling,metabolism,
orotherelementsofneurotransmitterphysiology—suchasdrugsofabuseorprescriptionmedications—may
impactthedevelopmentofneuralcircuitsandneurotransmittersystems(Tau&Peterson,2010).
Withinthecorticalplate,synapticdensitygrowsbyabout4%perweek,untilthepeaktransferofafferentsynaptic
connectionsfromthepreplatetothecorticalplatebetweenweeks26and28.Dendriticarborizationand
synaptogenesisaccelerateinthelatefetalperiodtoproduceathickeningofthedevelopingcortex.Atweek34,
approximately40,000newsynapsesareformedeverysecond,aprocessthatcontinuesintoearlypostnatallife.
Meanwhile,thesubplatedisappearsbytheendofthefetalperiod(Tau&Peterson,2010).
Thedifferentlayersofcortexcontaindifferenttypesofneurons.Earlyon,neuralprogenitorcellscanproduceany
neurontype,butasdevelopmentproceeds,theylosethiscapacityinaprocesstermed“faterestriction,”whichis
believedtobecontrolledbycellintrinsicsignaling,althoughthisprocessstillispoorlyunderstood(Stiles&
Jernigan,2010).Asitdevelops,thecorticalplateacquirestheorganizationalfeaturesofthematurecortex:
laminationfirstexistsintheprimarysensoryandmotorcorticesbyweek25andafullcomplementofvertical
laminainthedevelopingcortexbyweek32,includingafferentsofallofthemajorneurotransmittersystemsanda
diversityofdifferentiatedgliaandneuronalcelltypes,suchasexcitatoryglutamatergicspinypyramidalneurons
andGABAergicnonpyramidalinterneurons(Tau&Peterson,2010).Dependingonthespecificcorticalregion,
corticallayerIisformedbetweenweeks24and34andlayersIII–IVbetweenweeks32and34.Eachlayercontains
auniquearrayofcelltypes,“themorphologyandlaminarlocationofwhichdictatethepatternoflocalanddistant
projectionsthateachcellmaysendandreceive”(Tau&Peterson,2010;p.150)andthusshapingthemicro-and
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Fetal and Infant Neurobehavioral Development
macrocircuitsthroughoutthebrainthatsubservehumanfunctioning.
Finally,twootherdevelopmentalprocessesplaykeyrolesinfetalbraindevelopment:celldeath(apoptosis)and
myelination.Althoughthenumberofneuronsinthehumanbrainpeaksat28weeks,asmanyashalfofthese
neuronsdieasaresultofnaturallyoccurringcelldeath.Thiscullingofneuronsisaregulatedprocessalthoughthe
reasonsfortheoverproductionofneuronsarenotwellunderstood.Thewell-documentedeffectsoffetalalcohol
exposurehavebeenlinkedtoincreasedneuroapoptosisinthedevelopingbrain(Farber,Creeley,&Olney,2010),
althoughalcoholexposurealsohasbeenshowntoimpairthefunctionofcelladhesionmoleculeL1,whichis
importantinneuronalmigrationanddifferentiation(Tau&Peterson,2010).Myelin,whichenhancesthespeedand
accuracyofthetransmissionofinformationencodedinactionpotentialsthatpropagatealongneurons,isdetected
firstinsubcorticalregionsthenincorticalregionsbetween20and28weeks.Myelinationmaybesensitiveto
perinatalhypoxiaorischemia,aswellastoenvironmentaltoxinssuchasdrugsofabuse,suboptimalnutrition,and
theeffectsofpretermbirth,contributingtoriskforpoorneurodevelopmentaloutcomes(Tau&Peterson,2010).
FetalBehavioralStates
Intrauterinelifeisnotstaticbutcontinuouslyvaryingwithrespecttochangesinfetalmovement,heartrate,
hemodynamics,metabolism,eyemovements,andthestimuliandexposuresthatthefetusencounters(Arduini,
Rizzo,&Romanini,1995).Thedramatictransformationofthefetalbrainfromtheembryonicperiodtobirth
subservesanequallyremarkablebehavioralchangethatconfersorganizationtotheshiftinginuteroworld—the
obtainmentofidentifiableandcoherentfetalbehavioralstates.Forthepurposesoffetalneurobehavioral
assessment,theidentificationoffetalstateshastwofunctionssimilartothoseininfantstateevaluation:(1)
reflectingdevelopmentallyexpectedneuralmaturationthatcansupportdiscrete,organizedstatesandthe
transitionbetweenthem;and(2)providingthecontextfortheevaluationofotheraspectsoffetalneurobehavioral
developmentbyindicatingtheleveloffetalarousalatthetimeofassessment(DiPietro,2005).
Behavioralstatesconsistoftheidentificationofphysiologicalandbehavioralvariablesthatarestableovertime
andrepetitivewithinindividualsubjects,andinsimilarforms,acrossallsubjectsstudied(Arduinietal.,1995).
Followingadevelopmentalneurologyapproachtoinfantstatesdevelopedinthe1970sbyPrechtl(Prechtl,1974),
andaidedbytheabilitytovisualizethefetusviatheintroductionofultrasoundmethods,variousresearchers
begantoidentifybehavioralcyclesinthefetusbasedontheclusteringoffetalmovement,heartrate,andeye
movement(Arduinietal.,1995;Nijhuis,Prechtl,Martin,&Bots,1982).Therearefourdistinctfetalbehavioralstates
thatapproximatenewbornstates(notedinparentheses):1F(quietsleep):quiescence,sometimesinterruptedby
briefgrossbodymovements,eyemovementisabsent,heartrateisstablewithasmalloscillationbandwidth,no
accelerations,exceptincombinationwithastartle;2F(activeREMsleep)identifiedbyfrequentandperiodicgross
bodymovementssuchasstretchesandmovementsoftheextremities,eyemovementispresent,heartratehasa
wideroscillationbandwidthandfrequentaccelerationsthatcoincidewithmovement;3F(quietwaking)grossbody
movementsareabsent,eyemovementispresent,heartratehasawiderbandwidththanin1Fyetno
accelerations;4F(activewaking)notedforitsvigorouscontinualactivity,includingmanytrunkrotations,eye
movementispresent,heartrateisunstablewithlargeandlong-lastingaccelerations,oftenmergingintosustained
tachycardia(Nijhuis,1995).Characteristicsofneuralactivityobservedininfantsleepstateshavebeenseenin
baboonfetusesmonitoredusingelectroencephalogram(EEG)toolssurgicallyimplanted(Grieve,Myers,&Stark,
1994).
Maturefetalstateprofilesdevelopinthelatethirdtrimester,typicallyatapproximately36weeksorbeyond.Once
fullydeveloped,statetransitionscanbeobservedduringwhichnear-simultaneousshiftinginthethreeparameters
occurs.Priortothispointofmaturation,discretestatescanbeobserved,butthecorrespondenceamongthethree
parametersislessfrequent,andtransitionbetweenstatesislesswell–defined.Thereissignificantvariabilityinthe
proportionoftimefetusesspendinspecificstates,althoughsometrendsareevident:atallgestationages,active
sleep,2F,isthemostcommonlyobservedstate,followedbyquietsleep,1F.Activewakefulness,4F,isrelatively
rareandbeginstoemergenearterm.Timespentinquietwakefulness,3F,isveryrare,evennearterm(DiPietro,
2005;Nijhuis,1995).Instudieswiththenear-termfetalbaboon,states2Fand1Falsowerethemostfrequent
(Grieveetal.,1994).Theemergenceofmaturestatesfollowstheestablishmentofdifferentlayersofthefetalbrain
cortex,aswellasthesurgesofneuronalproliferationandsynapticconnections.However,thespecific
mechanismsunderlyingthematurationofthesestatesareonlynowunderstudy,withsomedataindicatingthatthe
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Fetal and Infant Neurobehavioral Development
preopticareasofthehypothalamusandtheforebrainareinvolved(Mohns,Karlsson,&Blumberg,2006).
Infull-termfetuses,prolongedperiodswithoutcoincidenceofphysiologicalandbehavioralfactorsarebelievedto
indicatedisruptionofcentrallymediatedcontrolmechanisms(Groome,Swiber,Atterbury,Bertz,&Holland,1997).
Fetusesofdiabeticwomenwithwell-controlledglucoselevelsshowadelayintheexpectedemergenceof
organizedfetalstates(Visser,Mulder,Bekedam,vanBallegooie,&Prechtl,1986),whereassimilarresultsareseen
inthosewithintrauterinegrowthretardation(IUGR;Arduinietal.,1995).Inaddition,comparedtohealthycontrols,
IUGRfetusesarefoundtohavemoredisorganizedstatetransition,specificallylongerintervalsbetweenshiftsin
behavioralstatesanddiscordantheartrateduringsuchstatetransitions(Arduinietal.,1995).Finally,inastudy
buildingontheindividualvariationinfetalstatedevelopment,DiPietro,Costigan,andPressman(2002)showedthat
indicatorsofproportionatelyhigherbiobehavioralconcordance(fetalheart-rate/movementconcordance)
predictedbetterbiobehavioralregulationinthe2-week-oldneonate.Inanotherstudy,latethird-trimesterfetuses
and2-week-oldnewbornsspentnearlyidenticalproportionsoftimeinquietandactivesleep(Groomeetal.,1997).
Takentogether,thesefindingsindicatethevalidityoffetalstateasanapproachtocharacterizingfetal
neurobehavioraldevelopment,aswellasunderscorethephenomenonthataspectsofneurobehavioral
developmentmeasuredininfantsbegininthefetusandareaccessibletoevaluation(DiPietro,2005).Aspectsof
stateregulationcanindexindividualdifferencesthataremaintainedthroughpostnataldevelopment,aswellas
indicatetypicalversusatypicaldevelopment.
OtherMilestonesinFetalNeurobehavioralDevelopmentandTheirAssessment
Toascertaindevelopmentalmilestonesinthefetus,aswellasindividualdifferencesinthesecapacities,
investigatorshavefocusedononeormoreaspectsoffunctioningwithinthreegeneraldomains:fetalheartrate,
movement,andresponsivitytostimulation(DiPietro,2005).Asindicated,fetalstatealsoisusedtoindex
development,anditissometimescontrolledforinevaluationsusingoneoftheotherdomains.
FetalHeartRate
Forinfants,aswellasforadultsandchildren,measurementofrestingheartrate,and,inparticular,indicesofits
variability,areusedtocharacterizenotonlyphysicalhealth,butalsopsychologicalwell-being(Porges,1997;
Porges,Doussard-Roosevelt,&Maiti,1994;Porges&Furman,2011;Sloanetal.,2001;Smith,Limon,Gallo,&Ngu,
1996).Forexample,inthecontextofpsychologicalchallenge,adultshighonhostilityaswellasthosewith
borderlinepersonalitydisordershowdecreasesinheartratevariabilitycomparedtohealthycontrols(Austin,
Riniolo,&Porges,2007;Sloan,etal.,2001),whilehigherlevelsofrestingheartratevariability,largelycontrolled
byvagalactivation(Berntsonetal.,1997),areassociatedwithmoreoveralladaptiveemotionregulation(Porges,
1997;Porges,etal.,1994;Sloanetal.,1994;Smithetal.,1996).
Overthecourseofgestation,fetalheartratedeclines(DiPietro,Irizarryetal.,2004;Pillai&James,1990)while
variabilityincreases(DiPietro,Caulfield,etal.,2004;DiPietro,Hodgson,Costigan,&Hilton,1996c;VanLeeuwen,
Lange,Bettermann,Gronemeyer,&Hatzmann,1999).Specifically,frommidpregnancytonearterm,average
restingfetalheartratedecreasesbyapproximately6beatsperminute(bpm);inonestudy,thisdecreasewasfrom
146.8bpmto140.9bpm(DiPietro,Hodgson,Costigan,&Hilton,1996c),whereasanotherreportedaveragefetal
heartrateat40weeksat130bpm(Pillai&James,1990).Heartratevariability,frequentlycomputedbasedon
standarddeviation(DiPietro,Hodgson,Costigan,&Hilton,1996c),increasesmoredramatically:inonestudyof31
fetusesobservedmonthlyfor50-minuteultrasoundsessionsfrom20–38weeks,short-termvariabilitybasedon
standarddeviationincreasedatarateof5%perweekuntil32weeks,thenat1.1%thereafter(DiPietro,Hodgson,
Costigan,&Hilton,1996c).Althoughthehumanheartbeginstobeatat3weekspostconception,thedevelopmental
changesinheartrateandvariabilityreflectanincreaseinparasympatheticinnervationoftheheart,aswellas
changesinneuraldevelopment,particularlymyelinationofcorticalandvagalprocesses(Dalton,Dawes,&Patrick,
1983;Dawes,Houghton,Redman,&Visser,1982;Sachis,Armstrong,Becker,&Bryan,1982).Bymidgestation,
fetalheartratecanbereliablycollectedforprolongedperiodsusingDoppler-basedelectronicfetalmonitors
appliedtothematernalabdomen.Atthispoint,thefetalheartissubstantialinsizerelativetootherpotential
sourcesofartifact,andsignallossduetomovementisnotascommonasitisatearliertimepoints(DiPietro,2005).
Intheassessmentoffetalneurobehavior,heartrateaccelerationordecelerationinrelationtostimulioftenisused
asaresponsevariable(Bussetal.,2009;DiPietro,Costigan,Nelson,Gurewitsch,&Laudenslager,2008;
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Kisilevsky,Pang,&Hains,2000;S.Kisilevsky,Hains,Jacquet,Granier-Deferre,&Lecanuet,2004;Lecanuet,
Granier-Deferre,&Busnel,1988;1989;Lecanuet,Graniere-Deferre,Jacquet,&DeCasper,2000;Lecanuet&
Schaal,1996;Monketal.,2004;2010)asisrestingfetalheartratevariability(DiPietro,Hodgson,Costigan,&
Hilton,1996c;DiPietro,K.A.,Hilton,&Pressman,1999).(Seethesection“Exposures”forexamplesofthese
findings.)Importantly,signallossfordetectingfetalheartratecanoccurduringinstancesoffetalmovement,which
isnotrandomlydistributed(DiPietro,2005).Moreactivefetusescangeneratelessreliableheartratedata.Average
heartratesignallosshasbeenobservedtobe6%at20weeksofgestation,andbetween1%and5%at28weeks
andbeyond(DiPietro,Hodgson,Costigan,&Hilton,1996c).
FetalMovement
Inthenewborn,movementcanbeevaluatedbasedontone,posture,reflexes,andoverallactivitylevel(DiPietro,
2005);inthefetus,theprimaryfocusisondifferentquantificationsofspontaneousmovement.Morespecifically,
forpsychologicalanddevelopmentalresearch,fetalmovementhasbeeninvestigatedasaprecursorofindividual
variationinactivity,acommonlystudiedconstructintemperamentresearch(DiPietro,2005;DiPietro,Hodgson,
Costigan,&Johnson,1996a).
Evenintheembryonicandearlyfetalperiods,spontaneousmovementispresent(deVries,Visser,&Prechtl,
1982).Asgestationcontinues,morecomplexmovementpatternsemerge,suchasswallowing,yawning,breathing,
hiccupping,headrotation,andlegmovements,whichareinplacebythefirsttrimester(deVries&Fong,2006;
Roodenburg,Wladimiroff,vanEs,&Prechtl,1991).Eyemovementappearsat14weeks,whereasother
movementsspecifictothefaceareseenlaterterm,suchaseyesopeningat26weeks,and,nearertoterm,
grimacing,non-nutritivesucking,andtongueprotrusion(deVries&Fong,2006).Generalmovements,themost
commonformofmovementandpresentfromthefirsthalfofgestation,alsoincreasetoterm,withchangesinthe
durationofthemovementandinpausesbetweenmovementsincreasing(deVries&Fong,2006).Fetalmovement
showsacircadianrhythm,peakinglateintheevening(Arduinietal.,1987),whereasfetalbreathingpeaks
followingthemother’smealtimes(deVries,Visser,&Prechtl,1988).Fetalmovementdeclinesoverthecourseof
gestation;accordingtoonestudy,after20weeks,fetusesmoveapproximatelyeveryminuteandareactive
between10%and20%ofthetime(DiPietro,2005;DiPietro,Caulfield,etal.,2004).Thereissomecontinuity
betweenlatefetalmovementactivityandnewbornlevelswithinthefirst2–4weeksofpregnancy(Groomeetal.,
1999),althoughsomewhatlessconsistentresultsshowlevelofmovementandassociationswithtemperament
parametersinearlyinfancy(DiPietro,Bornsteinetal.,2002).Forexample,movementlevelat36weekswas
positivelyassociatedwithobservedactivitylevelmorethan1yearlaterforboys,althoughitwasinversely
associatedforgirls;whereasforbothsexes,overallfetalmovementwasnegativelyassociatedwithdistressto
limitationsatthesameage(DiPietro,Bornstein,etal.,2002).
Fetalmovement,andthelag-timebetweenitandaheartrateincursion,alsohasbeenusedtoindexfetal
maturationandgroupdifferencesinneurobehavioraldevelopment(DiPietro,Caulfield,etal.,2004;DiPietro,
Hodgson,Costigan,&Hilton,1996c;DiPietro,Hodgson,Costigan,&Johnson,1996b;DiPietroetal.,2010;TimorTritsch,Dierker,Zador,Hertz,&Rosen,1978).Specifically,from20weeksthroughterm,fetalmotoractivityis
increasinglyassociatedor“coupled”withaccelerationsinfetalheartrate;thestrengthofthis“coupling”
relationshipisanindicatoroffetalwell-being,andreflectsintegrationbetweensomaticandcardiacfunctioning,as
wellasmaturationoftheautonomicnervoussystem(DiPietro,Hodgson,etal.,1996b).Inseveralstudies,DiPietro
etal.havedemonstratedanincreaseincouplingovergestation(DiPietro,Hodgson,Costigan,&Hilton,1996c),as
wellasapositiveassociationbetweenfetalmovementandheartratecouplingandnewbornbrainstemauditory
evokedpotentials(DiPietroetal.,2010).Lowerlevelsofcoupling,andinitsrateofincreaseovergestation,have
beenidentifiedinfetusesoflowersocioeconomicstatus(SES;Pressman,DiPietro,Costigan,Shupe,&Johnson,
1998)andinthoseinLima,Peru,versusBaltimore,Maryland,despitecomparableprenatalcareacrossboth
groups(DiPietro,Caulfield,etal.,2004).Hence,couplingmaybeanimportantpredictorofsubsequentinfant
developmentthatisworthyoffutureresearch.
Pregnantwomendonottypicallyfeelfetalmovementuntilthe16thor18thgestationalweek;withrespectto
assessmentoffetalmovements,womendonotaccuratelyjudgetheirpresenceorabsence(deVries&Fong,
2006;Kisilevsky,Killen,Muir,&Low,1991).Moreover,althoughdoppleractigraphyprovidesreliabledetectionof
fetalmovementdata,divergencesinthequantificationofmovementboutscanmakedifficultdirectcomparisonsof
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Fetal and Infant Neurobehavioral Development
fetalmovementdataacrosslabs(deVries&Fong,2006;DiPietro,2005).Thereisanothercomplicationwith
respecttofetalneurobehavioralassessmentbasedonmovementandcouplingcriteria:incidencesoffetal
movementattheextremeendsoftherangelimitandincreasetheopportunitiesforassociationswithheartrate
incursions,whichcouldaffectthecouplingvalue(DiPietro,personalcommunication).Andfetalmovementcanbe
associatedwithlossoftheheartratesignal,whichcanbiasdatacollectioninveryactivefetuses.
ResponsivitytoStimuli
Fetalresponsetostimulicanbeelicitedandtesteddirectlyandprovidesawindowintofetalneurobehavioral
functioning.Inthesestimulus-elicitingparadigms,thesourceofthestimulivaries(vibroacoustic,musicalnotes,
maternalstatechanges),asdoestheresponsevariable(heartratechange,movement,habituation).By22weeks,
somefetusesshowarousaltoexternalstimuli,andby30weekssuchresponsescanbereliablyelicited(Leader,
1995).Thedemonstrationofanelicitedfetalresponseisintriguingwithrespecttoinvestigationsofthe
developmentofsensorycapacitiesandemergingbraincircuitriessupportinginformationprocessing.However,
thereissomedebateastotheinterpretationoffetalresponses,withonecamparguingcaution(DeCasper,
Granier-Deferre,Fifer,&Moon,2011),onthebeliefthatthefetuses’seeminglycomplexbehaviorsareprimarily
reflectiveofbrainstemreflexesandonlyminimalforebraincontribution(Joseph,2000),andtheothercamp
referringtofetusesasshowingattentionanddiscriminationandevokingtheinvolvementofhigherorderbrain
processes(Kisilevsky&Hains,2011).Inwhatfollows,wediscussfetalresponsestostandardizedvibroacoustic
andauditoryprobes,aswellastoacutechangesinmaternalpsychologicalstate(laboratory-elicitedstressand
inducedrelaxation).Aswillbeconsideredinthenextsection,morethantheothermilestones,thecapacityfor
elicitedresponses(andsubsequentregulation)underscoresthefactthattherootsofindividualdifferencesin
neurobehavioralfunctioning—oftenindependentofmaternalorfetalpathology—emergeandarereadilyassessed
priortobirth.
VibroacousticStimuli:FetalMovement,HeartRate,andHabituation
Avibroacousticstimulus,asopposedtoanairbornesoundstimulus(seebelow),isdeliveredonthematernal
abdomenandincludesbothanairbornesoundandamechanicaltactilevibration.Whenthevibroacousticstimulus
isintense(i.e.,>85decibel[dB]/soundpressurelevel[SPL]),avarietyoffetalresponsesareelicited:startle,heart
rateincrease,abruptstatechanges,decreasedfetalbreathingmovements,andmicturition(Visser&Mulder,1993;
Zimmer&Divon,1993).Relativetointensestimulation,mildervibroacousticsoundstimuligeneratelessrobust
behavioralresponsesandhavebeenusedmoreconsistentlytochartdevelopmentaltimingofthefetalresponse.
Forexample,inastudyof60healthypregnantwomencarryingsingletonfetusesusingavibratorwith64dBSPL
airbornesound,Kisilevsky,Muir,andLow(1992)showedthattheresponsetothiskindofstimulationbeginsat
about26weeksofgestation,withmovementactivitycomingonlinefirst,thenareliableheartrateaccelerationat
about29weeks;overall,theresponsepatternincreasesovera6-weekperiod,becomingfullymatureatabout32
weeks.Thisvibroacoustictest,whichinvolvessensory,motor,and/orheartrateresponses,reflectshigherlevel
CNSactivitythantheobservationofbasalmovementandheartratefunctioning.Anencephalicfetusesmayhave
normalmovementandheartrateactivity,yettheydonotshowaresponsetovibroacousticstimulation(Leader,
Baillie,Martin,&Vermeulen,1982;Ohel,Simon,Linder,&Mor-Yosef,1986).
Vibroacousticstimulationalsohasbeenusedtodemonstratehabituation(learning,orthecessationofabehavioral
responsethatoccurswhenaninitiallynovelstimulusispresentedrepeatedly)inthehumanfetusand
dishabituation(memory,ortherecoveryofaresponsetotheoriginalstimulusfollowingthepresentationofa
secondnovelstimulus).Severalstudiesindicatethatfetuseshabituatetoexternalstimulationbyapproximately25
weeksofgestation(Leaderetal.,1982;Leader&Baillie,1988;Leader,Stevens,&Lumbers,1988;Madison,
Madison,&Adubato,1986).Habituationisassociatedwithotherindicatorsofthelevelofbehavioraldevelopment
independentofgestationalage(Morokumaetal.,2004).FetuseswithDownsyndrometakelongertohabituate,and
differentpatternsofhabituationareassociatedwithdifferentdegreesofDownsyndromeandatypical
neurodevelopment(Hepper&Shahidullah,1992).Onereport,oneofthefewtoincludedishabituationandthus
helpingtodistinguishtruehabituationfromresponsefatigue(DiPietro,2005),showedbychangesinfetalheartrate
thatby32weeksfetuseswerecapableofhabituatingtoa63dBstimulusandthendishabituatingtoitbyshowinga
changeinresponsetoanothernovelstimulusdeliveredat68dB(Sandman,Wadhwa,Hetrick,Porto,&Peeke,
1997).However,themethodologyhasbeensubjecttocriticism,giventherelianceonsmallchangesinfetalheart
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Fetal and Infant Neurobehavioral Development
rate,aswellasontheuseofrepeatedstimulation(i.e.,40timesover45minutes;DiPietro,2005).
MusicandVoiceStimuli:FetalHeartRate
By35weeks,cochlearbiomechanicsandfrequencyselectivityaremature,enablingthefetustoprocessauditory
stimuli(Eldredge&Salamy,1996)anddiscriminateintensity,frequency,andspectraasthefetusnearsterm
(Lecanuetetal.,2000).Inaseriesofcarefullyexecutedstudies,Lecanuetandhiscolleagues(Lecanuet&Schaal,
1996;Lecanuet,Granier-Deferre,Jacquet&Busnel,1992)showedthatfetusesbetween36and40weeksof
gestationdifferentiatedbetweenmaleandfemalevoicesreadingthesametextbasedontheirheartrate
deceleration(anorientingresponse)tothechangeinspeaker(Lecanuetetal.,1992).Otherdataindicatethat
fetusesasyoungas28weeksrespondtomusicwithin30secondsofexposuretoit,asevidencedbyaheartrate
increaseinresponsetoBrahams’s“Lullaby”deliveredthroughaloudspeakerpositionednearthematernal
abdomen.However,bylaterinpregnancy,thefetalheartrateresponseshiftedtoaheartratedecelerationtothe
samestimulus,atleastatlowerdecibelintensities(Kisilevskyetal.,2004).Suchfindingsareintriguing,but,as
DeCasperetal.(2011)recentlypointedout,teasingouttheeffectsofexternalstimulionfetalheartrateis
extremelychallenging,andthuscharacterizingresponsesas“orienting”andimplying“payingattention”should
berenderedcautiously;thescienceoffetalauditoryprocessingisstillinitsinfancy.Ontheotherhand,arecent
studyexploitedthecontinuitybetweenfetalandinfantdevelopmentandtheeaseofnewbornversusfetal
assessmenttodemonstratesupportforfetalauditoryprocessingandmemorydevelopment.Specifically,GranierDeferre,Bassereau,Ribeiro,Jacquet,andDecasper(2011)exposed25fetusestoadescendingpianomelody
twicedailyat35,36,and37weeksofgestation.Sixweekspostpartum,theinfantswereexposedtothesame
musicduringquietsleep,aswere25controlinfantsnaïvetothepianomusic.Bothgroupsofinfantsalsohearda
newstimulus,anascendingpianotune.Althoughallinfantsdisplayedasignificantheartratechange,theinfants
exposedtothemusicasfetusesshowedacardiacdecelerationthatwastwotimeslargerthanthedeceleration
elicitedbythecontrolmusicandthecontrolresponsestoeitherpianomelody(Granier-Deferreetal.,2011).Other
studies,onthebasisofinfantsuckingresponsesinsteadofheartrate,haveshownthatnewbornsprefertheir
mothers’voiceoveranotherwoman’s(DeCasper&Fifer,1980)andthat2-day-oldscandifferentiatethelanguage
theyheardinuterocomparedtoanovelone(Byers-Heinlein,Burns,&Werker,2010).
AcuteChangesinMaternalState:FetalHeartRate,HeartRateVariability,andMovement
Fetalhabituationandresponsestomusicunderscorethepotentialforenvironmentalshapingofneurobehavioral
developmentbeforebirth.Anage-oldquestioniswhethermaternalpsychologicalexperiencessimilarlyreachthe
fetusandifthey,overthecourseofpregnancy,influencechildren’sdevelopmentaltrajectories.Oneapproachto
thisquestionistheacuteinductionofaspecificmaternalpsychological“state,”suchasstressorrelaxation,and
theidentificationofaconcurrentfetalresponse.Forexample,inastudyfrom1967,maternalandfetalheartrate
increaseswereinducedbyashamprotocolinwhichasubjectwas“toldthatshewas…breathingagaswhich
containedonlyhalftheamountofoxygennecessarytosupportfetallife,butthathernormalbodymechanisms
wouldprobablycompensateforthisalteredenvironmentalcondition”(Copher&Huber,1967).Theauthors
concludedfromtheirsignificantresultsbasedsolelyonelicitinganxietyfrompregnantwomenthatthereisa“basis
forconcernregardingtheemotionalstatusofthesubjectwhentestingtheeffectsofmaternal[environmental]
stimuli[i.e.,actualchangesinairoxygenlevels]onthematernal–fetalrelationship”(Copher&Huber,1967).More
recently,afewotherlaboratorieshaveaimedtostudytheacute“transmission”ofmaternalexperiencetothe
fetus.
Twogroupshaveusedacommoncognitivechallengeassessinginterferenceinreactiontime,theStroopcolorwordmatchingtask,inalaboratorysettingtoinduceacutestressinpregnantwomenwhiletheyandtheirfetuses
arephysiologicallymonitored(DiPietro,Costigan,&Gurewitsch,2003;Monketal.,2000;2004;2010).Inresults
fromDiPietroetal.(2003)withfetusesat24and36weeks’gestation,theStrooptaskledtosignificantincreasesin
maternalheartrateandskinconductance(indicativeofsympatheticactivation),aswellastoincreasesinfetal
heartratevariabilityandasuppressionofmotoractivity(butnottochangeinfetalheartrate).Thematernalresults
declinedfrom24to36weeks’gestationwhilethemagnitudeofthefetalresponsesincreasedfromthefirsttothe
secondtestingperiod.Becausetherewasonlyonemodestassociationbetweenamaternalphysiologicalvariable
(skinconductance)andfetalmotoractivity(apositiveassociation),DiPietroetal.hypothesizeda“sensory”
versus“physiological”pathwaybywhichmaternalexperiencemayimpactthefetus.Inthelattermodel,the
primarymechanismwouldbedirectphysiologicalmediation.Changesinmaternalcardiovascularactivitywould
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Fetal and Infant Neurobehavioral Development
contributetochangesinfetalheartrateormovementasaconsequenceofphysiologicalprocessesaimedat
maintaininghomeostasisand/orreactivityindicativeofadisruptioninthetypicalphysiologicalmilieu.Incontrast,in
thesensorymodel,maternalphysiologicalreactivitythefetusrespondstothesensorystimulationofthematernal
stressresponsei.e.,theauditorystimulifrommaternalheartrateandbloodpressurechanges.Datafromother
studiesare,forthemostpart,consistentwithDiPietroetal.’sresultsandlendsupporttothesensoryinterpretation.
InaseriesofstudiesalsousingtheStroopcolor-wordmatchingtaskwithpregnantwomeninthethirdtrimester,
Monkandhercolleagues(Monketal.,2000;2004;2010)foundnochangeinfetalheartrateinresponseto
women’sexposuretothecognitivechallenge(infetusesofpsychiatricallyhealthywomen;seebelow)andonly
minimalassociationsbetweenmaternalphysiologicalreactivityandfetalresponses(intheseresults,amodest
associationbetweenchangesinsystolicbloodpressureandfetalheartrate).Fetalmovementandheartrate
variabilitywerenotassessed.Monketal.(2010)alsoexaminedanadditionaltaskfortheparticipants,
standardizedchangesinbreathingrate,andfoundthatstimulustoproducedramaticincreasesinfetalheartrate.
Therewerenodirectassociationsbetweenmaternalandfetalphysiology,yetrobustchangesinfetalheartrate
occurredwhenwomenwerealternativelybreathinghalfasfastastypicalortwotimesfaster.Moreover,such
changesinbreathing,accompaniedbyabdominalandchestmovement,mayprovideauditoryaswellasvestibular
stimulitothefetus.Takentogether,theseresultsareconsistentwiththehypothesisthatchangesinpregnant
women’scardiorespiratoryactivity(someofwhichmaybeassociatedwithpsychologicalstate)functionasstimuli,
whichthefetusperceivesandtowhichitresponds.Finally,infurthersupportofthesensoryhypothesis,DiPietroet
al.(2008)foundsimilarfetalresponsestoinducedmaternalrelaxationastheydidtoinducedmaternalstress.
Specifically,whenpregnantwomeninthe32ndgestationalweekunderwentan18-minuterelaxationprocedure,
theirheartrateandskinconductancelevelsdecreased(oppositeoftheirresponsestotheStrooptask)but,
paradoxically,theirfetusesshowedsomeofthesameresponsesastheydidtothestressortask:adecreasein
fetalmovementandanincreaseinfetalheartratevariability.Asbefore,therewereonlymodestassociations
betweenchangesinmaternalphysiologyandfetalreactivity.
Sofar,withrespecttotheacutetransmissionofmaternalpsychologicalexperiencetothefetus,thedataare
affirmative:thefetussenseschangesinthemother’smood,butthereisanunexpectedtwist.Mood-based
changesinmaternalphysiologydonot,forthemostpart,directlymediatefetalresponses.Instead,thefetus
sensesandrespondstochangesinmaternalexperienceviaregisteringandreactingtochangesinthemother’s
autonomicnervoussystemactivity.
ContextualInfluencesonFetalDevelopment:MaternalDistressandPoverty
Asindicated,thequestionoftheacutetransmissionofmaternalexperiencetothefetusisinspiredbyand
contributestothemetaquestion:dopregnantwomen’spsychological/psychosocialexperiencesshapethe
neurobiologicaldevelopmentoftheperinate,withimplicationsforchildren’slong-termneurobehavioral
trajectories?Thereisaburgeoningareaofresearchsuggestingthatmaternalanxiety,stress,anddepression
duringpregnancymayhaveanegativeimpactonchildren’spsychosocialfunctioning(Charil,Laplante,
Vaillancourt,&King,2010;Talge,Neal,&Glover,2007;butseeDiPietroforcontrastingfindings:DiPietro,2004;
DiPietro,Novak,Costigan,Atella,&Reusing,2006;DiPietroetal.,2010).Withrespecttopsychosocialexperiences
suchaspoverty,thereareextensivedatadocumentingthenegativeimpactofpovertyonchilddevelopment
(Evans,Gonnella,Marcynyszyn,Gentile,&Salpekar,2005),andsomeofit,beginninginutero,isfocusedlargely
onthequalityofmaternalnutrition(Georgieff,2007;Georgieff&Rao,2001;Nelson,Wewerka,Borscheid,
Deregnier,&Georgieff,2003;Rao,Tkac,Townsend,Gruetter,&Georgieff,2003).However,becausetheprenatal
studiesconcerningmaternaldistressandpovertysuggestamaternalinfluenceduringtheinuteroperiod,recent
studieshaveaimedtoidentifyamaternaleffectatthetimeitishypothesizedtohaveoccurred,thatis,during
pregnancy.Morespecifically,studieshaveaimedtofinddifferencesinfetalneurobehaviorrelatedtomaternal
distressandpoverty.
Instudiesassessingfetalneurobehaviorduringarestingbaselineperiod,several,largelyconsistentresultshave
emerged.Greaterlifestressappraisalwasassociatedwithreducedfetalheartratevariability,indicatingless
optimalphysiologicalregulation(DiPietro,Hodgson,Costigan,&Hilton,1996c),aswasincreasedmovement,
indicatingheightenedarousal(DiPietro,Hilton,Hawkins,Costigan,&Pressman,2002).Inanotherreport,maternal
depression,asassessedbyaself-reportindex,alsowasassociatedwithincreasedmotoractivity(Dieteretal.,
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Fetal and Infant Neurobehavioral Development
2001;Emory&Dieter,2006).Higherlevelsofmaternalcortisol,aprimarystresshormonesometimesfoundtobe
higherinthecontextofpsychologicaldistress,havebeenpositivelyassociatedwithgreateramplitudeinfetal
movement,aswellaswiththeamountoftimefetusesspentmoving(DiPietro,Kivlighan,Costigan,&Laudenslager,
2009).Incontrast,relativetowomenwhoreportedlowerlevelsoftraitanxiety,womenwhoendorsedhighertrait
anxietyhadfetuseswhospentmoretimeinquietsleepandshowedlessgrossbodymovementwhileinactive
sleep(Groome,Swiber,Bentz,Holland,&Atterbury,1995).Althoughdifferencesinfetalassessmentmayaccount
forthisseeminglyconflictingfinding(i.e.,visualizationofthefetusviaultrasound[Groomeetal.,1995]versus
computationofmovementviadigitizeddatafromDoppleractigraphy[DiPietroetal.,2009]),italsolikelyreflects
therelativenewnessofthisscientificdomain.
Otherresearchhasaimedtoidentifyfetaldifferencesrelatedtomaternalpsychologicalfunctioningunder
conditionswhenthemotherfacesachallenge—theStrooptask,asdescribedpreviously—aswellaswhenthe
fetusisdirectlystimulated,thatis,viaavibroacousticprobe.Inthesamestudiesdiscussedearlier,Monkandher
colleaguesfoundthatwhereasfetusesofnonanxiousandpsychiatricallyhealthywomendidnotshowaheartrate
changeduringtheStrooptask,fetusesofanxiousanddepressedwomenhadasignificantheartrateincrease
(Monketal.,2000;2004;2010).Inthemostrecentresults,maternalcortisollevelsweremarginallypositively
associatedwithfetalheartrateactivity(Monketal.,2010).Whenstimulateddirectlywithavibroacousticprobe,
fetusesofwomenwithelevatedlevelsofcorticotropin-releasinghormone(CRH;which,duringpregnancy,is
predominantlyofplacentaloriginandcanbeincreasedbymaternalcortisol)failedtorespondtoanovelstimulus
inahabituation/dishabituationparadigm.Inaddition,higherCRHwaspositivelyrelatedtohigheroverallfetalheart
ratereactivitytothestimulus(Sandmanetal.,1999).Asisclear,embeddedinthisresearchisagainthequestion
ofphysiologicalmechanism:bywhatprocessismaternalpsychologicalexperiencetransmittedtothefetusinsuch
awayastoalterfetalneurobehavior?Morespecifically,thisisasearchforadirectimpactofwomen’smoodbasedbiologyshapingfetalbrain–behaviordevelopment.Thehypothalamic-pituitary-adrenal(HPA)axis,
particularlycortisolanditseffectsonbraindevelopmentaswellasplacentalprotectionagainstit;vasoconstriction
inuterinebloodflow;and,finally,cytokineactivityareallbeingexamined(Glover,Bergman,Sarkar,&O’Connor,
2008;Glover,O’Connor,&O’Donnell,2009;Glover,Teixeira,Gitau,&Fisk,1999;Wadhwa,2005).Ofnote,ina
fewstudies,DiPietroetal.haveshownthatgreaterfetalmovementleadstohigherlevelsofskinconductance
(DiPietro,Caulfield,etal.,2006;DiPietro,Irizarry,Costigan,&Gurewitsch,2004),whichsuggeststhatthedirection
ofthematernal–fetalcommunicationisfarfromfullyunderstood,evenasitrelatestomaternalstatessuchas
stressordepression.Forexample,coulditbethatmoreactivefetusescontributetogreatersympathetic
activation,whichwomeninterpretand“label”asaformofpsychologicaldistress(DiPietro,Costigan,Chen,&
Voegtline,2011)?
Theeffectsofsocialclassonfetalneurobehavioralalsohavebeeninvestigated,althoughthebiologyofthese
findingshasbeenlessconsidered.Povertyisassociatedwithcumulativestressors(e.g.,substandardhousing,
foodinsecurity,familyturmoil,andcommunityviolence),andthesesourcesofstressmitigatetheassociation
betweenlowSESandpoordevelopmentaloutcomes(Evans&English,2002).ThedeleteriouseffectsoflowerSES
extendintotheprenatalperiod.LowSEShasbeenassociatedwithlessfetalheartratevariabilityandlesscoupling
offetalmovementandheartrate(DiPietroetal.,1999;Pressmanetal.,1998).Intriguingly,inastudyofpregnant
womenfromLima,Peru,andBaltimore,Maryland,DiPietro,Caulfield,etal.(2004)showedthatfetusesinLimahad
lowerlevelsofrestingheartratevariabilityandcoupling,aswellasaflattersloperepresentingtheincreasein
couplingacrossgestation.Althoughbothgroupsreceivedprenatalcare,theLimagroupwaslesseducatedand,
onaverage,8yearsolder,andhadlessaffluenceandgreaterdisadvantage.Nonetheless,thisstudyfailedto
identifythematernaldifferencesthatcouldaccountforthefetalresults,leavingtheauthorstounderscoretherole
ofthe“broadercontextoftheantenatalenvironment”inunderstandingmaternalinfluencesthatmayaffectthe
fetusand,ultimately,thedevelopingchild.
Conclusion:FetalNeurobehavioralDevelopment
Althoughinterestinfetaldevelopment,inthechildbeforeheorshecanbeseen,datesbacktobiblicaltimesand
beyond,recentadvancesintechnologyand,inparticular,inknowledgeofbraindevelopmentbeforebirth,have
fosteredadramaticincreaseinstudiesaimedatcharacterizingwhatthefetuscandoandbywhen.Overall,the
findingsonfetalstate,aswellasthematurationalchangesinheartrateandcoupling,underscorethecontinuity
betweenfetalandnewbornbehaviorandtheexaggerateddividethatcanbeattributedtobirth.Takentogether,
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Fetal and Infant Neurobehavioral Development
thesestudiesdemonstratethatbythethirdtrimester,itispossibletoreliably“askthefetusquestions,”touse
standardizedassessmentproceduresandprobestoevaluateneurobehavioralfunctioningthatalsocaninformthe
identificationofsubtleindividualdifferencesinfetaldevelopment.However,astandardizedbatteryforfetal
neurobehavioralassessmentdoesnotyetexist,andmostresearchersfollowDiPietro(2005)incautioningthatthe
productionofsuchastandardizedprotocolispremature.Consistentwitharenewedemphasisonthe
developmentaloriginsofpsychopathology(Baleetal.,2010;Insel&Wang,2010),fetalneurobehavioralresearch
alsoisfocusedonthefactorscontributingtoindividualdifferences,includingvariationinmaternalmood-based
biology.Similartotheresearchperspectiveonthepostpartumbaby,thefetus’developmentisconsideredinthe
contextofhisorherantenatalenvironment.
TheInfant
Here,wepresentresearchfocusingonbrain–behaviorrelationshipsthatofferspromiseforexaminationof
continuityfromthefetalperiodandemphasizesbasicprocessesininfantneurobehavioralgrowth.Thisfocuson
neurobehavioraldevelopmentbeginswithanoverviewofneurologicaldevelopmentandplasticity.Wethenreview
theliteratureoninfantbehavioralregulation,includingstateregulationandsleep.Wereviewtheworkexamining
thedynamicsofphysicalgrowthandmotordevelopment,includingresearchonthemirrorneuronsystemin
infants.Ourreviewofsocial-emotionaldevelopmentininfancyfocusesonbasicprocessesunderlyingkey
constructssuchasattachment(Chapter6,thisvolume)andincludesareviewoftheinfant’semergentcapacityto
relatetoothersvis-à-visattentionregulationandsensitivitytosocialcuesthatextendfrompurelyinterpersonal
exchangestotheeventualinclusionofobjects.Althoughcompartmentalizedtopicallyforthesakeoforganization,
wehavepresentedinfantneurobehavioralgrowthastheproductofdynamicandinterrelatedsystems.Thissection
oninfancyculminatesinadiscussionofmaternaldepressionandpoverty,eachofwhichillustratestheinfant’s
exquisitesensitivitytothebroaderecologyinwhichheisreared—fromthe“micro,”proximallevelofthemother–
infantdyadtothemore“macro”ordistalsocioeconomicenvironment.
InfantBrainDevelopment
Significantneurologicaldevelopmentoccursinthefirst2yearsoflife.Atbirth,thefullydevelopmentneonatalbrain
weighs400g,approximately25%ofitseventualadultsize.Byage2,thebrainhasadvancedfrom25%to75%of
itsadultsize,andthisperiodofrapidgrowthiscommonlyreferredtoasthebraingrowthspurt(Schore,1994).
Duringthistime,thereisamaturationaloverproductionofaxons,dendrites,andsynapsesacrossthecortex
(Singer,1995).Twoprimarymechanismsinvolvedinfunctionalneurologicalgrowtharesynaptogenesis—the
forgingandstrengtheningofsynapsesthatareinuse;andsynapticpruning—thetrimmingofprimitivesynaptic
connectionsthatservenofunctionalpurposeintheextrauterineenvironment(Nelson&Bosquet,2000).Thesetwo
processarethecentralmechanismsofneuralplasticity—theneuralprocessesthatunderliesthedegreetowhich
experienceshapesneuralcircuitry.
Ithasbeensuggestedthattherearetwodistinctmechanismsofplasticity(Greenough&Black,1992).Experienceexpectantdevelopmentoccursonlyafterthebrainhasreceivedacertaincriticalthresholdofinputnecessaryfor
theformationofsynapsesthatwerenotestablishedprenatally.Therearesensitiveperiodsforwhichsuchinput
mustbeachievedinorderforneurologicalchangeanditsassociatedfunctionalitytobecomeinstantiated.The
mostclassicexampleinvolvesthepioneeringworkofWieselandHubel,whodemonstratedthatdeprivationoflight
andforminkittens,viasuturingtheeyes,ledtoblindnessduetoneurologicalchangestothevisualsysteminthe
subcorticalandcorticalregionsresponsibleforprocessingvisualinput.Theseeffectsshowedlittleevidenceof
reversibility(Wiesel&Hubel,1965)andwereconstrainedtoearlylife(Wiesel&Hubel,1963),withnoevidenceof
corticalblindnessoccurringinadultcatsexperiencingvisualdeprivation.Researchexaminingtheeffectsof
cataractsonvisualdevelopmentinthehumaninfanthasshowedthatinfantilecataractsareassociatedwithlongtermvisualacuity(Birch&Stager,1996)andocular-motor(Abadi,Forster,&Lloyd,2006)deficits.Thedeleterious
impactofthecataractdependsonthepathologicalcharacteristicsofthecataracts(extentofvisualdeprivation)
andthetimingofsurgicalintervention—withsignificantlyimprovedvisualacuity(Birch&Stager,1996)andocularmotorfunctioning(Abadietal.,2006)resultingwhensurgicalinterventionoccurswithinthefirst6weeksoflife.
Morerecentresearchhasrevealedthat,followingsurgicalinterventionearlyinlife,earlyvisualdeprivation
associatedwithinfantilecataractsleadstopersistingdeficitsthatarespecifictohumanfaceprocessing(Robbins,
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Fetal and Infant Neurobehavioral Development
Nishimura,Mondloch,Lewis,&Maurer,2010).Hence,earlysensoryandperceptualdevelopmentishighly
dependentonearlyexperienceandguidedbyexperience-expectantprocesses,whichareconstrainedbycritical
periodsduringwhichthebrainmustreceivearequisitelevelofinput.
Thesecondformofplasticityisreferredtoasexperience-dependent(Greenough&Black,1992).Thisformof
plasticityoccurswhenenvironmentalinputservestocreate,strengthen,ormodifysynapticconnections.This
processremainsongoingacrossthelifespanandisnotasdramaticallyconstrainedbycriticalperiods.Alsoin
contrasttoexperience-expectantplasticity,whichisgenerallyspecifictosensoryandperceptualsystems,
experience-dependentprocessesarerelevantforeverydomainofdevelopment—cognitive,behavioral,and
social.Modelsofenvironmentaldeprivationhaverevealedtheimportanceoftheearlyrearingenvironmentfor
corticalactivityaffectingmultipleareasoffunctioning.InRomanianinfantswhoexperienceextremeearly
deprivation(institutionalcare),brainactivityischaracterizedbygreaterEEGpowerinlow-frequencybandwidths
oftheEEG(θ)andreducedEEGpowerinhigh-frequencybandwidths(αandβ),indicatingslowedbraingrowthin
childrenexperiencingearlydeprivation(Marshall&Fox,2004).Recentfollow-upstudiesofinstitutionalizedinfants
haverevealedthatenvironmentalenrichment(fostercareplacement)isassociatedwithincreasesinhighfrequencyEEGpower(Marshall,Reeb,Fox,Nelson,&Zeanah,2008),andthisimprovementisinfluencedby
durationofdeprivation,withchildrenexperiencingenrichmentpriortotheageof24monthsshowingsignificantly
greaterhigh-frequencyEEGpowerthaninfantsplacedintofostercareafterage24months(Vanderwert,Marshall,
Nelson,Zeanah,&Fox,2010).Theneurologicaleffectsofearlydeprivationarefurthersupportedbybehavioral
andcognitiveevidence.Forinstance,deficitsinattentionandvisualprocessinginchildrenwhoexperienced
prolongedinstitutionalizationhavebeenreported(Pollaketal.,2010).McLaughlinetal.(2010)reported
significantlyincreasedsymptomsofattentiondeficitdisorderininstitutionallyrearedchildrenandshowedthatthis
associationwassignificantlymediatedbyreducedhigh-frequencyEEGpowerandelevatedlow-frequencyEEG
power.Theeffectsofenvironmentalenrichmentfollowingdeprivationareconsistentwithanimalmodels.For
instance,rodentmodelshaveshownthatearlyexposuretoenrichedenvironmentsisassociatedwithsignificant
increaseinthenumberofsynapsesperneuronincorticalregionsinvolvedinvision(Turner&Greenough,1985).
Hence,neurologicaldevelopmentininfancyishighlydependentonthequalityofearlyexperiencesbecausesuch
experiencesfacilitatetheformationofsynapticconnectionsthatserveasthefoundationforbehavioraland
cognitivegrowth.
Theorganizationofthecortexcontinuesacrossthefirst3years.Lateralization,orhemisphericspecialization,is
notconsistentlymanifestasastable,dominanthandpreferenceuntilage3years(McManus,Sik,Cole,&Mellon,
1988).However,morerecentstudieshavefoundevidenceforstabilityinhandpreferenceforreachingininfants
betweentheagesof7and13months(Michel,Tyler,Ferre,&Sheu,2006).Thisevidenceisconsistentwith
researchusingelectrophysiologicalmethodologies,whichhasprovidedevidenceforemergentspecializationof
thelefthemisphereforspeechprocessingearlyininfancy(Dehaene-Lambertz&Baillet,1998).Recent
neuroimagingstudieshaverevealedbothstructuralandfunctionalasymmetriesinyounginfants.Forinstance,
Glasel,Leroy,Dubois,Hertz-Pannier,Mangin,andDehaene-Lambertz(2011)showedastructuralasymmetryinthe
rightsuperiortemporalsulcusoftypicallydevelopingpreverbalinfants.Usingfunctionalneuroimaging,DehaeneLambertzetal.(2010)foundthatmaternalandnovelspeechsamplesactivatedthelefttemporallobeinhealthy2month-olds.
Researchexaminingchangesinhandpreferencehasofferedevidencethatthedevelopmentoflateralizationis
dynamicacrossthefirst2yearsandinfluencedbyexperience(Dehaene-Lambertzetal.,2010).Forinstance,
languagemilestonesareassociatedwithlateralization.Cochet,Jover,andVauclair(2011)foundthattoddlers’use
ofaconsistentdominanthandfordeclarativepointingincreasedfollowingthelanguagegrowthspurt.Changesin
handednessarealsoassociatedwithmotormilestones:precrawlinginfantsshoweddecreasedhandpreference
followingtheonsetofhands-and-kneescrawling(Corbetta&Thelen,1999)andincreaseduseofbothhands,or
coupling,inreachingfollowingtheonsetofwalking(Corbetta&Bojczyk,2002).Takentogether,thisresearch
indicatesthatthereisevidenceoflateralizationpresentininfancybutthatthisprocessisdynamicacrossthefirst
3yearsandinfluencedbylinguisticandsensory-motorexperiences.
Theremaybesignificantcognitiveimplicationsfortheearlydevelopmentoflateralizationacrossdevelopment.
Consistencyandtypeofhandpreferenceinchildhoodhasbeenofconsiderableinterestintheontogenyof
dyslexia(Annett,2011),andrecentlongitudinalevidenceshowsthat,relativetochildrenwhodidnotshowa
consistenthandpreference,girls,butnotboys,showingaconsistenthandpreferencefromlateinfancytoearly
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Fetal and Infant Neurobehavioral Development
childhoodscoredhigherontestsofverbalintelligenceandreadingachievementinchildhoodandadolescence
(Wilbourn,Gottfried,&Kee,2011).
InfantBehavioralStates
InfantStateRegulation
Therapidlyevolvingorganizationalstructureofearlybraingrowthisevidentinthebehavioralorganizationofthe
neonate.Atbirth,theneonate’ssleep–wakecycleshiftsmorerapidlythanthatofachildoranadult.Theneonate
engagesinpatternsofmotoractivitythataresimilartothoseobservedduringthelatephaseofthefetalperiod
(Groomeetal.,1999).Theneonate’ssleep–wakecyclestendtoshowamodestdegreeofbehavioralorganization,
andthesecyclesevolverapidlyacrossthefirstmonths.Newbornsevidence10distinctbehavioralstates(Thoman
&Whitney,1990),asoutlinedinTable1.Thepaceofcyclingthroughthesestatesslowsastheinfant’sbehavioral
organizationbecomesmorepredictable,withagradualincreaseintheamountoftimespentinwakingstatesand
sleepingschedulesbecomingmorepredictablebytheageof3months(Henderson,France,Owens,&Blampied,
2010).
Table1TaxonomyofInfantBehavioralStates
State
Description
Alert
Eyesopen,attentiveorscanning,gross-motoractivity
Nonalert
waking
Eyesopen,attentionunfocused,activitylevelvariable
Fuss
Vocaldistresssoundsatlowintensity,continuousorintermittent
Cry
Intensevocaldistress,continuousorintermittent
Drowse
Eyesopeningandclosingoropennarrowly,lowactivitylevel
Daze
Eyesopenandglassy,noactivity
Sleep–
wake
transition
Eyesmaybeopenorclosed,orvacillatebetweenopenandclosedrapidly,generalizedmotor
activity
Active
sleep
Eyesclosed,withREMsoccurringintermittently,sporadicmotoractivitymayoccur;lowered
muscletone;emotionexpression(smiling,crying)orothervocalizationsmayoccurintermittently
Quiet
sleep
Eyesclosed,respirationslowandregular,motoractivitylimitedandmayincluderhythmic
mouthing
AdaptedfromThoman&Whitney(1990).
Stateregulationservesasanimportantmarkerofself-regulation,asinfantsuseshiftsinstatetoadapttothe
demandsoftheirenvironment(Thoman,1990).Stateregulationisanimportantmarkerofneurologicalandoverall
physiologicalfunctioning—shiftsinstateareassociatedwithchangesincerebralmetabolismandbloodflow,
endocrinefunction,andchangesincardiovascularandrespiratoryfunction(Orem&Barnes,1980).
Theemergenceofprolongedperiodsofwakingduringthedayallowforoptimallevelsofenvironmentalstimulation,
thusmaximizingtheopportunityforestablishmentofsynapticconnectionsforemergingsensory-motorcircuitry.
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Fetal and Infant Neurobehavioral Development
Theincreaseinactivealertnesssetsthestageforsocialexperience.Cecchini,Baroni,Vito,andLai(2011)showed
thatinfantsmilingvariedduringsleepandwakeperiods,withwakefulsmilesshowingclearlinkstosocial
experience.Theprolongedperiodsofactivealertstatesprovideopportunitiesforsocialcommunication,allowing
caregiverstoengagetheinfantinface-to-faceplay.Infantcryingisalsoofsocialsignificancebecausevocalizing
distressservesmultiplefunctions,includingcommunicationandphysiologicalregulation(Acebo&Thoman,1995).
Cryinginresponsetohunger,fatigue,anddiscomfortoffersanimportantmodeofcommunicationtocaregivers
wholearntodifferentiatethesecriesandrespondcontingently(Gustafson&Deconti,1990).Styleofmaternal
respondingisrelatedtoinfantcrying—forinstance,relativetolowerfrequenciesofcrying,higherfrequenciesof
cryingduringmaternalholdingareassociatedwithlessinteractionalstabilityinthemother–infantdyad(Thoman,
1990).
Infantbehavioraldysregulationisassociatedwithearlyriskformothers,infants,anddyadicfunctioning.Excessive
cryingininfancyisassociatedwithmaternalpostpartumdepression(Viketal.,2009),loweredmaternal
perceptionsofself-efficacy(Stifter&Bono,1998),maternalreportofphysicalandemotionalsymptomsandmarital
dissatisfaction(Levitzky&Cooper,2000),andchildabuse(Brewsteretal.,1998).Moregeneralizedbehavioral
dysregulationisassociatedwithothermarkersofearlyrisk,includingprenatalnutritionaldeprivation(HernándezMartínezetal.,2011),maternalantenataldepression(Goodman,Rouse,Long,Ji,&Brand,2011),prenataldrug
andenvironmentaltoxinexposure(Myersetal.,2003;Stewart,Reihman,Lonky,Darvill,&Pagano,2000),and
prematurebirth(Stephensetal.,2010).Inalargesampleof1,248high-risk,prenatallydrug-exposedinfants,Liuet
al.(2010)foundthat5.8%ofthesampleshowedextremebehavioraldysregulationintheneonatalperiod(i.e.,
highlyaroused,hypertonic,low-qualitymovement,poorattention,andlowself-regulation).Theseinfants
manifestedpersistentdeficitsontestsofmentaldevelopmentininfancyandcognitiveandbehavioralfunctioningin
earlychildhood.Theseeffectswereindependentofprematurebirth(gestationalage)andlowSES.Infantsshowing
extremebehavioraldysregulationasneonatesappearedtobethemostsensitivetoprenataldrugexposureand
prematurity(Liuetal.,2010).Thebehavioralorganizationoftheprematureinfantisalsopredictiveoflaterhealth
andbehavioraldifficulties(Ohgietal.,2003;Stephensetal.,2010).Intheirsampleofprematureinfants,Stephens
etal.foundthatprematurebirthandaprofileofunderarousalontheNeonatalIntensiveCareUnitNetwork
NeurobehavioralScales(NNNS;Lester&Tronick,2004)predicted26%ofthevarianceinlowmotorperformance
ontheBayleyScalesofInfantDevelopmentat24months.Oghietal.(2003)foundthatlowerNeonatalBehavioral
AssessmentScale(NBAS;Brazelton&Nugent,1995)scoresformotorandstatecontrolinvery-low-birthweight
(VLBW)neonatescouldbeusedtocorrectlyclassify50–75%ofchildrenshowinghighlevelsofbehaviorproblems
inmiddlechildhood(ages7–8years).
InfantSleep
Sleeppatternsininfancychangedramaticallyacrossthefirstyearandareanimportantmarkerofbehavioral
regulation.Hormonalevidenceoftheemergenceofcircadianrhythmshasbeendocumentedin3-month-old
infants(Rivkees,2003).Behaviorally,consolidationofdiurnalfunctioningoccursbetweenmonths4and6,when
wakingbecomesconsolidatedtothedayandsleepconsolidatedtonight(Cornwell&Feigenbaum,2006).These
behavioraldataarecomplementedbypolygraphicdata,whichshowhighlevelsofvariabilityinsleepstates,
includingmorefrequentepisodesofactivesleep,priortoage3months(Hoppenbrouwers,Hodgman,Arakawa,&
Geidel,1988).
Likewakingbehavior,sleeppatternsalsobecomemoreorganizedacrosstheearlymonthsofinfancy.Using
retrospectivereportmethodology,MooreandUcko(1957)reportedthat70%of3-month-oldinfantsslept
continuouslyfor5consecutivehours(12a.m.to5p.m.)byage3months.Amorerecentprospectivelongitudinal
studyexaminingparentalsleepdiariesof75typicallydevelopinginfantsbetweentheages6daysand12months
affirmstheearlyconsolidationofself-regulatedsleep(Hendersonetal.,2010).Hendersonetal.notedthatthe
mostdramaticshiftinincreaseinlengthofinfantssleepoccurredbetweentheagesof1and4months,withthe
majorityofinfantssleepingfor8consecutivehoursbyage3monthsandmorethanhalfthesamplesleepingin
accordancewithfamilyconventions(from10p.m.to6a.m.)byage5months.
Longer,morepredictablewindowsofnocturnalsleeparealsoofconsiderableimportance.Differentsleepstates
appeartoservedistinctneurobiologicalfunctions.Forinstance,inadults,non-rapideyemovement(NREM)sleepis
associatedwithactivationofpreopticandbasalforebrainregions,andslowedrespirationandactivitysupports
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Fetal and Infant Neurobehavioral Development
energyconservation.Incontrast,active(REM)sleepinvolvesactivationoftheisolatedbrainstemandis
characterizedbyalossofmuscletoneduetothesimultaneoustriggeringofwithdrawalandexcitationmotor
neuronsinvolvedinmemoryconsolidationandneuronaldevelopment.NeurologicalactivityishighduringREM
sleep,andtheproportionofREMsleepishighestinaltricialspecies(whereoffspringarebornimmobileandheavily
dependentonmaternalcareforsurvival),suggestingperhapsthatactivationofsensorimotorregionsofthebrain
occurringduringthistimeprovidescriticalinputnecessarytosupportsensorimotordevelopment(Siegel,2005).
Additionalevidencerevealsthatinfantsarecapableoflearningduringsleep.Fiferetal.(2010)usedaneye
conditioningparadigmtoexamineinfantcontingencylearningandassociatedneurologicalsubstratesinsleeping
1-and2-day-oldinfants.Relativetoinfantswhoexperiencedrandomtone-airpuffstimuli(controlgroup),infants
whoexperiencedaconsistentPavlovianpairingoftonefollowedbyairpuff(experimentalgroup)showed
significantlymoreeyemovement,specificallyafourfoldincreaseinthelikelihoodofconditionedeyemovements,
inresponsetothepresentationofatonebytheendoftraining.Event-relatedpotential(ERP)datacollectedwithin
theexperimentalgroupshowedamorepositive-goingslowwaveinthefrontalregions,providingevidenceof
learningacrosstrialsinsleepingnewborns.Anotherstudyappliedsimilareye-blinkconditioningmethodologyin
sleeping1-month-oldsassessedinthelaboratory(Reeb-Sutherlandetal.,2011).Thisstudyalsoexamined
differentiallearningduringsleepbasedontypeofunconditionedstimulus(social[femalevoice]ornonsocial[tone
vs.backwardvoice])andshowedthatlearningacrosstrialsincreasedmorerapidlyforthesocialstimulusversus
thetwononsocialconditions.Giventhelargeproportionoftimenewbornsspendinsleepstatesandthedramatic
behavioralandcognitivegainsofthefirstmonthsoflife,theneedandcapacitytolearnlikelyextendstosleep
(Fiferetal.,2010).Furthermore,socialstimuliappeartoholdaprivilegedpositioninearlylearningduringsleepin
thefirstmonthofinfancy(Reeb-Sutherland,etal.,2011).
Theevidenceforinfantlearningduringsleepstatesiscomplementedbyresearchexaminingassociationsbetween
sleepqualityanddevelopmentalhealth.Itiswell-documentedthatpersistentsleepdisturbancesinchildhoodare
associatedwithpoorerhealth,behavioral,language,andlearningoutcomes(Owens&Witmans,2004;Quach,
Hiscock,Canterford,&Wake,2009).Evidencedrawnfromsamplesofchildren(Bourkeetal.,2011)and
preschoolers(Karpinski,Scullin,&Montgomery-Downs,2008)hasrevealedthatmildtoseverelevelsofsleepdisturbedbreathingareassociatedwithpoorerperformanceontasksofexecutivefunctioning(Quachetal.,2009).
Lessisknownaboutthelong-termcognitiveimpactofdisorderedsleepininfancy.However,onestudyshowed
thatahigherproportionofREMsleep(relativetototalsleeptime)isassociatedwithlowerdevelopmentalquotients
inasampleofdevelopmentallydelayedinfants(Shibagaki,Sawata,&Tachibana,2004).
Thequalityoftheearlycareenvironmentaffectsinfantsleep.Higherlevelsofmaternalemotionalavailability
(sensitiveresponsivenesstemperedwithappreciationforinfants’needforsleep[vs.stimulation]andtheabsence
ofhostility)duringthebedtimeroutinewasassociatedwithlessdisruptedsleepinasampleofinfantsaged1–24
months(Teti,Kim,Mayer,&Countermine,2010).MorrellandSteele(2003)demonstratedcontinuityinsleep
disturbancesbetweenthefirstandsecondyearoflife.Infantswhoshowedacontinuousprofileofsleepproblems
weremorelikelythaninfantswithnosuchstableprofileofsleepdifficultiestoberatedastemperamentallydifficult
bytheirmothersandtohavemotherswhomanifestedproblematicideasaboutlimit-settingandwhoreliedon
physicalcomfortingatbedtime(cuddlingorfeedingtosleep;Morrell&Steele,2003).Thelargerecologyofthe
familyisanimportantcontributortoqualityofinfantsleep.Inalargesampleofadoptedchildren,Manneringetal.
(2011)foundthatmaritalinstabilityatinfantage9monthspredictedinfantsleepproblemsat18months.Another
studyof35infantsfoundthattypicallydevelopinginfantswithfatherswhoprovidednighttimecarewokefewer
timesduringthenightthandidinfantsoflessnocturnallyinvolvedfathers(Tikotzky,Sadeh,&Glickman-Gavrieli,
2011).Althoughthesefindingsarecorrelationalinnature,Tikotzkyetal.suggestedthatmoreconsolidatedsleep
forinfantsreceivinghighpaternalcaremaybeafunctionofmorepositiveglobalco-parentingpractices,whichare
associatedwithlessparentalstressandanenhancedfamilialatmosphere.
OtherMilestonesinInfantNeurobehavioralDevelopment
MotorDevelopment
Theneonateisbornwithasetofmotorreflexesthataremarkersofneurologicalhealth.Severalofthesereflexes
haveclearadaptivevalueandareknownassurvivalreflexes.Theseincludesucking,swallowing,androoting,and
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Fetal and Infant Neurobehavioral Development
collectivelytheyreflectasetofhardwiredmotormilestonesthatservetosupportsurvival(Wolff&Ferber,1979).
Oflessobviousadaptivevaluearetheprimitivereflexes,whichincludetheBabinski,Moro(startle),palmargrasp,
stepping,andswimmingreflexes.Ithasbeensuggestedthatthesereflexesarelingeringbyproductsofour
evolutionaryhistory.Importantly,thesereflexesareexpectedtobepresentatbirthbutdisappearshortly
thereafter(within4–8monthspostpartum).Indeed,thepresenceandexpecteddepartureofthesereflexesare
importantmarkersofneurologicalhealth(MacNeela,1984).
Motordevelopmentisdramaticacrossthefirst2yearsasthesporadicundifferentiatedmovementofthenewborn
evolvesintotheimpressivemotorrepertoireofthetoddler.Likestateregulation,thereisevidencethatgeneralized
levelofmotoractivityisstablefromthefetalperiodtothefirstmonthofneonatallife(Groomeetal.,1999).Action
ininfancyevolvesrapidlyanddynamicallyandistheproductofthecomplextransactionsbetweenneurological
growth,currentlevelofmotorfunctioning,physicalandphysiologicalfunctioning,andenvironment—thedemands
ofthetaskathandandthecontextualforces(e.g.,gravity)thatimpactperformance(Thelen,2005).Apowerful
exampleofthiscomplexinterplayisthedemonstrationthatthe“primitive”infantsteppingreflexthatdisappears
within3monthsfollowingbirthisreadilyapparentwhenthedemandsoftheenvironmentsupportinfantsteppingas
the3-to8-month-oldinfantishelduprightonatreadmill(Thelen,1986).Suchevidencewasthefirstto
demonstratethatmotoricadvancesininfantsareexquisitelycateredtothedemandsoftheenvironmentbut
constrainedbytheconcurrentdevelopmentalorphysicalstateoftheinfant.
Supportforthedynamicsystemsnatureofmotordevelopmenthasbeenfoundinmicrogeneticstudiesexamining
changeinbehaviorbeforeandaftertheonsetofamajormotormilestone(seeTable2foranoverviewofmajor
motormilestones).Forinstance,infantswhopreviouslyshowedaone-handedpreferenceingraspingwill
temporarilyresorttobimodalgraspingfollowingtheonsetofsitting(Corbetta&Bojczyk,2002),crawling(Corbetta
&Thelen,1999),andwalking(Berger,Friedman,&Polis,2011;Corbetta&Bojczyk,2002).Theonsetofeachnew
motormilestonerequirestheinfanttolearnnewaffordancesforthenewposture(Adolph,2000).Forinstance,
infantswhohavemasteredsittinguprightindependentlywillnotreachovera“risky”gapinsurfacetoretrievean
objectinasittingpositionbutwilldosoupontheonsetofcrawlingwhenplacedinthecrawlingposition(Adolph,
2000).Althoughexperiencedcrawlerswilleffectivelyjudgeandnavigatea“risky”slope,thisprudenceis
temporarilylostwiththeonsetofwalking,wherethenovicewalkerwillproceedwithoutcaution(Adolph,1997).The
samemaynotbetrueforavoidanceofdrasticdrop-offs.Forexample,newwalkersshowedmorerefusalwhen
invitedtocrosstothedeependofavisualcliffthandidexperiencedcrawlers,evenwhenplacedinthemore
noveluprightwalkingposition(Witherington,Campos,Anderson,Lejeune,&Seah,2005).
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Fetal and Infant Neurobehavioral Development
Table2MajorGrossMotorMilestonesfromBirthThroughAge12Months
MotorMilestone
MeanAge(when50%ofinfantshaveachievedmilestone)
Liftshead90degreeswhileonstomach
2.2months
Rollsover
2.8months
Sitswithsupport
2.9months
Sitswithoutsupport
5.5months
Standswithsupport
5.8months
Crawling
7.0months
Walkswithsupport/cruising
9.2months
Standsindependently
11.5months
Walksindependently
12.1months
Walksupsteps
17.0months
Kicksballforward
20.0months
AdaptedfromBayley(1993).
Advancementsinmotordevelopmentinfluenceotherdomainsofdevelopment.Sittingindependentlyallowsfor
moreeffectiveobjectexploration(Soska,Adolph,&Johnson,2010).Theonsetofwalkingisassociatedwith
increaseduseofdistalobjectsanduseofobjectstoinitiatesocialinteractionswithcaregivers(Karasik,TamisLeMonda,&Adolph,2011).Theonsetofself-propelledmovementisassociatedwiththeemergenceofvisual
proprioception,orthevisualawarenessofone’sownmovement,evenwhenself-propelledmovementisachieved
artificiallyviatrainingonapoweredmobilitydevice(Uchiyamaetal.,2008).Theonsetoflocomotionisassociated
withsocial-emotionalchangesininfants,includingmorepositiveaffectandincreasedparentalperceptionsofboth
positiveandnegativeaffect(Whitney&Green,2011).
Theenvironmentalsoinfluencesinfantmotordevelopment.Mothersusearichcommunicativerepertoiretoassist
infantsinnavigatingtheirphysicalworld(Karasik,Tamis-LeMonda,Adolph,&Dimitropoulou,2008;Karasik,etal.,
2011).Infantsthenusethissocialinformationtoguidetheirlocomotion(Adolph,Karasik,&Tamis-LeMonda,2010),
althoughthisistemperedwiththeirownperceptualjudgmentsandincreasingautonomy(Adolphetal.,2010).Use
ofinfantwalkers,whichpreventtheinfant’snaturaluseofenvironmentalinput,isassociatedwithslowedmotor
development(Garrett,McElroy,&Staines,2002).Infantswhoexperiencelesspurposeful“tummy-time”orlower
exposuretotheprone(vs.supine)lyingposition(Majnemer&Barr,2005)andoverweightinfants(Slining,Adair,
Goldman,Borja,&Bentley,2010)maybeatsignificantriskfordelayedmotordevelopment,suggestingthat
nutritionandexperiencehaveimportantimplicationsformotordevelopment.
Thedevelopmentofcomplexactionpatternsininfancyisrelatedtosocialexperience.Observationallearningis
evidentintheneonate’sabilitytoimitatesimplefacialgesturessuchastongueprotrusionandopen-mouthfacial
gestures(Meltzoff&Moore,1977;1983).Neonatalimitationisalsoevidentinnonhumanprimates(Ferrarietal.,
2009).Nine-month-oldhumaninfantshavebeenshowntoemulatenovel,complexmotortasksviasimple
observationandcanevidencedeferredrecallforcomplexnovelactions,evengeneralizingthoseactionsto
manipulationswithsuperficiallydifferentbutfunctionallysimilarstimuli(Learmonth,Lamberth,&Rovee-Collier,
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Fetal and Infant Neurobehavioral Development
2004;Lukowski,Wiebe,&Bauer,2009).Acrossinfancy,observationofmotortasksisassociatedwithmental
representationofexpectanciesaboutthephysicalworld.Forinstance,infantsmakepredictionsabouttheaction
intentofothers,andtheseimplicitrepresentationsgrowincreasinglymoresophisticatedacrossthefirstyear,born
fromobservationofothersandtheirownaccomplishmentofmotormilestones(Sommerville&Woodward,2010).
Forexample,infantslooklongerwhentheactionofanotherendsinamannerthatisincongruentwithapreviously
demonstratedgoal,suchaswhenanadultexperimenterwhopreviouslyreachedforoneobjectswitcheshergoal
andgraspsforadifferentobject(Woodward,1998).Thisassociationbetweenactionandrepresentationisevident
inactualimitationofactionaswell;7-month-oldinfantsselectivelyreproducethegoal-directedactionsofothers
(Hamlin,Hallinan,&Woodward,2008),andthisappearstobespecifictotheactionsofanimateversusinanimate
objects(Mahajan&Woodward,2009).
Anemergentbodyofevidenceisrevealingtheneuralsubstratesbehindobservationalmotorlearning,elucidating
thesophisticatedimplicitprocessesthatunderlierepresentationsofcomplexmotortasks.Workwithchildren
(Lepage&Théret,2007)hasrevealedthatthefrontal-parietalmotorregionsofthebrainthatactivatewhile
performingagoal-directedactionalsobecomeactivatedwhenobservinganotherperformthesameaction,a
phenomenonreferredtoasmotorresonancethathasledtothesuggestionofamirrorneuronsystemthat
underliesobservationallearning.Recentworkwithinfantshasrevealedthatsuchamirrorneuronsystemisin
placeearlyinlifeandlikelyplaysaroleinobservationallearningofcomplexgoal-directedactions.Recent
researchusingevent-relatedEEGdesynchronizationhasshowedactivationofthemotorregionswhen9-montholdinfantsexecutedorobservedreachingandgrasping(Southgate,Johnson,ElKaroui,&Csibra,2010).Marshall,
Young,andMeltzoff(2011)foundthat14-month-oldsshowedactivationofmotorpathwayswhileexecutingand
observingabutton-presstask.Thisemergingbodyofresearchwithinfantsprovidesnewevidencetoaffirmthe
representationalfunctionofmotortasks,withthemirrorneuronsystemsunderlyingtheprocessbywhichsocial
inputistranslatedintoaction.
SocialDevelopment
Neonatalimitationandobservationallearningofmotortasksininfancyarecleardemonstrationsofthenewborn’s
exquisitesensitivitytothesocialworld.Newbornsshowanimmediateattunementtothesocialworld.Highamplitudesuckingmethodologyhasrevealedthatinfantspreferhumanspeechversusnonspeechsounds,and
thisisevidentinthefirst1–4daysafterbirth(Vouloumanos&Werker,2007).Additionalresearchhasshownthat
neonateslooklongeratfaceversusnonfacestimuliinthefirsthouroflife(Johnson,Dziurawiec,Ellis,&Morton,
1991).By10–16weeks,infantsmanifestapreferenceforviewingfilmedsocialbehaviorthatissynchronous(lipvoicesynchrony)versusthatwhichistemporallyalteredorasynchronous(Dodd,1979).
Infantsbecomeincreasinglymoreactiveparticipantsinsocialexchangeswiththeircaregiversacrossthefirst4
months.Daysafterbirth,infantsmanifestavisualpreferencefortheirmother’sfaceoverthatofafemalestranger
(Pascalis,deSchonen,Morton,&Deruelle,1995).Byage6weeks,infantscoordinatetheirgazebehaviorwith
maternalvocalbehaviorduringface-to-faceinteractions(Crown,Feldstein,Jasnow,Beebe,&Jaffe,2002).
Examinationofinfantsaccadicreactiontimeshasrevealedthat,acrossthefirst3months,infantgazebehavior
becomesincreasinglymoresophisticated,encompassinglessfixatedstaringbehavior(Hopkins&VanWulfften
Palthe,1985)andmoredeliberatescanningoftargets(Hunnius&Geuze,2004).Moregazecontrolopensthedoor
formorecomplexsocialcoordinationbetweeninfantsandcaregivers.Microanalyticcodingofmother–infant
interactionhasrevealedthat3-month-oldinfantscoordinatetheirgaze(Harel,Gordon,Geva,&Feldman,2011)
andaffect(Lester,Hoffman,&Brazelton,1985;Tronick,1989)tothatoftheirmother.By4months,social
coordinationisevidentinthevocalrhythmsofthemother–infantdyad,andearlypatternsofinfantvocal
coordinationwithmotherandstrangerforetellsocialandcognitiveoutcomesatage12months(Jaffe,Beatrice,
Stanley,Crown,&Jasnow,2001).Asynchronousbehavioralcoordinationwithmotheracrossmultiplemodalities,
particularlyfacial-visualengagementandtouch,atinfantage4monthsispredictiveofsecureversusinsecure
attachmentclassificationintoddlerhood(Beebeetal.,2010).
Afterthefirstquarterofthefirstyear,theinfant’ssocialexchangeswithcaregiversinvolveincreasedinterestin
theirphysicalworld.Inthefirst3–4months,infantsdemonstratetheabilitytofollowthegazeofanadulttowarda
specificproximaltargetwithintheirvisualfield(D’Entremont,Hains,&Muir,1997)anddisengagefromthetargetto
refocustheirgazeontheircaregiver(Perra&Gattis,2010).By6months,infantsfollowmoredistalgazesofadults
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Fetal and Infant Neurobehavioral Development
butarelikelytobecomefixatedondistractersthatentertheirvisualfieldbeforethedistaltargetisidentified
visually(Butterworth&Jarrett,1991).Thevisualprecisionofgazefollowingcontinuestoevolveacrossthefirst
year,suchthatbetween12and18monthsinfantsareabletofollowanadultgazetoatargetwelloutsideoftheir
directvisualfield(Butterworth&Jarrett,1991).Between6and9months,thisattentionfollowingisevidentbyinfant
engagementinperiodsofjointattention,astheinfantjointlysharesattentiontoobjectsorotherreferentswith
others(Scaife&Bruner,1975).Infantsfirstmanifesttheabilitytorespondtobidsforjointattention(Bakeman&
Adamson,1984)andeventuallyadvancetoinitiatingboutsofjointattention(e.g.,viapointingatobjects)bythe
ageof12-months(Tomasello,Carpenter,&Liszkowski,2007).Jointattentioncontinuestoevolveacrossthe
secondyearascaregiver–infantinteractionswithobjectsgraduallyshiftfrommaternal-driventoinfant-ledplay
withobjects,intandemwithashiftfromtheinfant’srelianceongestureandphysicalplaytotheuseoflanguage
(Aureli&Presaghi,2010).Thisdevelopmentalshiftfromrespondingtobidsforjointattentionat6monthstomore
initiationofjointattentionby12monthsmaybeduetoevolutioninneurologicaladvancementinneuralcircuitry
involvedinregulationofattention.Mundy,Card,andFox(2000)acquiredbaselineEEGfrominfantsatage14
monthsandfoundaprofileofparietallobeactivation(associatedwithposteriorimplicitattentionregulation)was
associatedwiththedevelopmentofrespondingtojointattentionbidsbetweentheagesof14and18months.
Furthermore,developmentofinitiationofjointattentionbetween14and18monthswasassociatedwithaprofileof
activationintheprefrontalandcentralpathways(involvedinhigherlevel,voluntarycontrolofattention;Mundyet
al.,2000).
Theoccurrenceofjointattentionbetweeninfantsandtheircaregiversisassociatedwithlanguagelearning
becausethesharedattentiontoacommonreferentorobjectinvitestheopportunitytoidentifylabelsforreferents
(Bruner,1975;Tomasello,1992).Relativetomother–infantdyadswhoengageinlowerfrequenciesofjoint
attention,dyadswhoengageinhigherfrequenciesarecharacterizedbymoregeneralizedlevelsofmaternal
verbalinputduringmother–infantinteractions(Stevens,Blake,Vitale,&Macdonald,1998).Infantswhoco-engaged
inmorefrequentinstancesofjointattentionwithmothersatage6monthshadhighervocabularyscoresin
toddlerhoodrelativetoinfantswhoco-engagedinlessfrequentinstancesofjointattention(Saxon,1997).
Likealldyadicprocesses,infantsmaketheirownimportantcontributionstothesocialexperienceofshared
attention.Thereareimportantindividualdifferencesinthedegreetowhichinfantscanengageinjointattentionor
manifestjointattentionskill(Mundy&Gomes,1998).Thereisapositiveassociationbetweeninfantskillin
respondingtobidsforjointattention(gaze,pointing)andthefrequencyofjointattentionepisodesobservedduring
mother–infantplay(Markus,Mundy,Morales,Delgado,&Yale,2000).Six-month-oldinfants(Morales,Mundy,&
Rojas,1998)and12-month-olds(Markusetal.,2000)whomoreskillfullyrespondedtojointattentionbidsthan
thosewhomanifestedlessskillwerereportedtohavehighervocabulariesastoddlers.Individualdifferencesin
infantrespondingtojointattentionat12monthsandinitiatingjointattentionat18monthswereeachpositively
associatedwithlanguageatage24months(Mundyetal.,2007).Infantswhorespondtojointattentionperformed
betteronlanguageat18monthsthaninfantswhodidnotrespondtojointattention(Brooks&Meltzoff,2005).
Ithasbeensuggestedthattheexperienceofsharedattentionwithanotherrepresentsanimportantmilestonein
socialcognitionbecauseengagementinjointattentionrepresentstheexpressionoftheinfant’sunderstandingof
intentionalityortherepresentationofotherpersonsasintentionalagents(Tomasello,1995).BrooksandMeltzoff
(2005)showedthat10-and11-month-oldinfantsweresignificantlymorelikelytofollowthegazeofanadultwhen
theadult’seyeswereopenversusclosed.Thesamewasnottruefor9-month-olds,whofollowedgazeregardless
ofwhethertheeyeswereopenorshut.Hence,althoughgaze-followingisclearlyevidentin6-month-oldinfants
(Bakeman&Adamson,1984;Butterworth&Jarrett,1991;Scaife&Bruner,1975),therepresentationofintentionis
onlymanifestmonthsaftertheinfanthasengagedinattentionregulation,suggestingthatexperienceinattention
regulationisacriticalprecursortosocialcognition(Mundy&Newell,2007).Clearlinksbetweenjointattentionin
infancyandperformanceonsubsequentmeasuresofsocialcognitionhavebeenfound.Forexample,joint
attentionskillininfancyispositivelyassociatedwithtoddler’suseofmentalstatelanguage(e.g.,expressions
abouttheirowncognitions,emotions,desires,perceptions,andphysiologicalstate;Kristen,Sodian,Thoermer,&
Perst,2011),performanceontheoryofmindtasks(i.e.,visualperspective-taking,“seeing-leads-to-knowing,”and
asituationanddesire-basedemotiontasks;Charmanetal.,2000),andparentreportofglobalsocialcompetence
inearlychildhood(VanHeckeetal.,2007).
EmotionalDevelopment
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Fetal and Infant Neurobehavioral Development
Emergentsocialinformationprocessingininfancydevelopsintandemwiththecapacitytorecognizeemotionsin
others.Newborninfantslooklongeratastimulusdepictingahappyfaceversusafearfulone(Farroni,Menon,
Rigato,&Johnson,2007).Habituationstudieshaverevealedthat,byage3months,infantsdiscriminatebetween
facesdepictinghappinessversussadness(Barrera&Maurer,1981;Kuchuk,Vibbert,&Bornstein,1986).In
addition,a3-month-old’sfacerecognitionisbetterforaffectivelypositiveversusneutralfaces(Turati,Montirosso,
Brenna,Ferrara,&Borgatti,2011).Discriminationoffearfulfacescomesonlineshortlythereafter.Byage5months,
infantsdiscriminatebetweenhappyandfearfulfaces(Bornstein&Arterberry,2003),andthereisrobustevidence
thatinfantsasyoungas5monthsrespondwithnegativeaffecttotheshiftinmaternalaffectfromnormalface-tofaceplaytoa“still-face”(Cohn&Tronick,1983).Byages4–7months,infantsshowavoidancewhenpresented
withthreateningversusnonthreateningfaces(Hunnius,deWit,Vrins,&vonHofsten,2011).Acorresponding
neurologicalresponseindicatingattentionalarousalhasbeenrevealedinERPstudiesof7-month-oldsviewing
photographicimagesoffearfulandangryfaces(Hoehl&Striano,2008).Infantsareslowertohabituatetofearful
versushappyfacialstimuli,suggestingthatinfantsshowanattentionalbiastothreatatasyoungas7months
(Nelson,Morse,&Leavitt,1979).Additionaleyetrackingworkwith7-month-oldshasrevealedthatthepreference
toattendtofearfulfacesoccursintandemwithheartratedecelerationoracardiacorientingresponse(Peltola,
Leppänen,&Hietanen,2011).
Towardtheendofthefirstyear,infantsengageinsocialreferencing,lookingtotheemotionalexpressionsof
otherstodeterminehowtoapproachnovelpeople,objects,andsituations(Campos,1980).Researchusingsocial
referencingparadigmshasrevealedthat10-to12-month-oldinfantsshowwarinessofatargetthathasbeen
presentedinthecontextofnegativeaffectiveexpressionsinadults,evenifthosequeuesaredepictedonavideo
monitor(Mumme&Fernald,2003;Mumme,Fernald,&Herrera,1996).Thisiscomplementedbyemergentevidence
usingERPsinyoungerinfants;forinstance,6-month-oldsshowheightenedattentionalarousalwhenviewinga
fearful(vs.neutral)facegazingdirectlyatanobject(Hoehl&Striano,2010).
Thereisevidencethatinfantemotionprocessingisassociatedwithsocialexperience.Three-and-a-half-month-old
infantsdiscriminatebetweensadandhappyfacialexpressionsonlywhentheyarefirsthabituatedtothese
changesinaffect(fromsadtohappy)asdisplayedbytheirparents(vs.anoveladult;Walker-Andrews,KroghJespersen,Mayhew,&Coffield,2011).Additionalresearchhasshownthatsocialsensitivitytoaffectivelypositive
facesatage3monthsisassociatedwiththeircaregivinghistory;infantswhoweremostsensitive(lookedlonger)
toincreasesintheintensityofpositiveaffectinstillimageshadmotherswhowereobservedduringhome-based
interactionstofocustheinfant’sattentiononthem(mother)morefrequently(Kuchuketal.,1986).
ContextualInfluencesonInfantDevelopment:MaternalDistressandPoverty
MaternalDistress
Healthyinfantdevelopmentdependsonthequalityofthepostpartumenvironment.Researchwithinstitutionalized
childrenhasdemonstratedthatextremeneglectisassociatedwithcompromisedphysical,cognitive,andsocialemotionaldevelopment(Gheraetal.,2009;Marshalletal.,2008;Nelsonetal.,2007).Lessextremeperturbations
inthequalityoftheearlyrearingenvironmentarealsoofconsiderableimportancetohealthydevelopment.For
instance,low-quality,insensitivematernalbehaviorduringroutinecare-focusedtasksininfancyisassociatedwith
aneurobehavioralprofileofstressreactivityandbehavioraldefensiveness(e.g.,rightfrontalEEGasymmetryat
baseline,inhibitedbehaviorinthepresenceofanadultstranger,aggressionduringplaywithanovelpeer,and
maternalreportofpronenesstoanger)thatpersistsintoearlychildhood(Hane&Fox,2006;Hane,Henderson,
Reeb-Sutherland,&Fox,2010).Additionalresearchshowsthathigh-qualitymaternalbehaviorininfancyis
associatedwithslowerincreasesinfearreactivityfrom4to16months(Braungart-Rieker,Hill-Soderlund,&
Karrass,2010)andmaternalreportoffewerbehaviorproblemsandhighersocialcompetenceinearlychildhood
(Leerkes,Blankson,&O’Brien,2009).
Sensitivematernalbehavioralsobuffersagainstthedeleteriouseffectsofantenatalanxiety(Grant,McMahon,
Reilly,&Austin,2010;Kaplan,Evans,&Monk,2008).Forexample,infantsofmothersmeetingcriteriafordiagnosis
ofanxietyordepressioninthesecondtrimesterofpregnancyshowedsignificantlyhigherbasalcortisol(a
neuroendocrinemarkerofheightenedstress)thandidinfantsofhealthywomenonlywhenthequalityofpostnatal
careatage4monthswaslow(Kaplanetal.,2008).Womenwhosufferfromantenataldepressionandanxietyare
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Fetal and Infant Neurobehavioral Development
atsignificantriskforcontinuedillnessfollowingthebirthoftheirinfant(Field,2011;Josefsson,Berg,Nordin,&
Sydsjo,2001).Depressedmothersprovidelessstimulatinghomeenvironmentsbeginningearlyinthepostnatal
period(Conroy,Marks,Schacht,Davies,&Moran,2010).Agreatdealofresearchhasdemonstratedthatthe
qualityofmother–infantinteractionissignificantlycompromisedindepressedmothers,whichmaytaketheformof
withdrawnorintrusiveinteractivebehavior(Tronick&Reck,2009).Forinstance,motherssufferingfrom
postpartumdepressionsubsequentlyengagedtheirinfants(atage4months)withlessoptimallevelsofstimulation,
includingdiscordantattentionco-regulationandattenuatedgazecoordination,butheightenedaffectcoordination
(Beebeetal.,2008).Thispatternofasynchronoussocialengagementbetweendepressedmothersandtheir
infantspersistsacrossthefirstyearofinfancy(Feldmanetal.,2009).Intoddlerhood,maternaldepressionis
associatedwithlessco-engagementinjointattentiontoobjects(Goldsmith&Rogoff,1997;Jameson,Gelfand,
Kulcsar,&Teti,1997).
Theexperienceofbeingcaredforbyadepressedcaregivermarkssignificantupheavalfortheinfant.Maternal
depressiondistortsemotionalcommunicationinthemother–infantdyadandsignificantlyalterstheinfant’ssocialemotionaldevelopment(Tronick&Reck,2009).Theexperienceofmaternalapathyandwithdrawalisstressfulfor
infants.Earlyininfancy,typicallydevelopinginfantsrespondtoalaboratory-inducedexperienceofmaternal
depression(vis-a-visthematernal“still-face”paradigm)withprotest,gazeavoidance,andnegativeaffectthat
carriesoveronceanormativepatternofface-to-faceplayisresumed(Cohn&Tronick,1983),suggestingthat
infantsaresensitivetotheexpressionofdepressedbehaviorintheircaregivers.Theimpactofdepressed
caregivingisevidentinthebehaviorofinfantsofdepressedmothers,whoshowageneralizedprofileofaffective
dysregulation,includingmorewithdrawn,lessactive,andlessaffectivelypositivesocialbehaviorthandoinfantsof
nondepressedmothers;seeTronick&Reck(2009)andField(2010)forreviews.This“depressed”patternof
interactingininfantsofdepressedmotherscarriesovertointeractionswithotheradultsininfantsasyoungas3
months(Field,Healy,Goldstein,&Perry,1988).Relativetoinfantsofnondepressedmothers,infantsofdepressed
mothersevokelesspositivebehaviorfromunfamiliaradults(Tronick&Reck,2009).Whenpresented
experimentallywiththechallengeofamaternalstill-faceinthelaboratory,infantsofdepressedmothers(vs.infants
ofnondepressedmothers)showmorereactive/activeformsoftouchbehavior(Moszkowskietal.,2009).Relative
toinfantsofhealthywomen,infantsofdepressedmothersshowlowerlevelsofsocialengagement,lessselfregulation,andmorenegativeaffect(Feldman,etal.,2009).Infantsofdepressedmothersalsoshowphysiological
differencesconsistentwithstressreactivityandnegativeaffect,includingaprofileofrightfrontalEEGasymmetry
(forareview,seeField&Diego,2008)andbasalautonomicandneuroendocrinearousal(Diegoetal.,2004).
Infantsofdepressedmotherscontinuetoshowaprofileofriskacrossdevelopment.Postpartumdepressionis
associatedwithinsecureattachment(Campbelletal.,2004),attenuatedsocialcompetence(Wu,Selig,Roberts,&
Steele,2011),compromisedlanguagedevelopmentinearlychildhood(Brennanetal.,2000;Chapin&Altenhofen,
2010),andincreasedinternalizingbehaviorproblemsinmiddlechildhood(Anhalt,Telzrow,&Brown,2007).
Relativetochildrenofnondepressedmothers,childrenwhoarerearedbymotherswhoshowastableprofileof
depressionacrosstheirchildhoodaresignificantlymorelikelytoshowbehaviorproblemsandengageinmorerisktakingbehaviorinadolescence(Campbell,Morgan-Lopez,Cox,&McLoyd,2009).
Poverty
Accordingtorecentstatistics,morethan1in5childrenundertheageof5liveinpoverty(ChildTrends,2012).
Familieswithinfantsandyoungchildrenarethemostlikelytodwellinpoverty.Forinstance,in2011,25%of
children0–5yearslivedinpoverty,and20%ofchildrenaged5–17livedinpoorhouseholds(ChildTrends,2012).
Alargebodyofresearchhasdocumentedthemultifacetedriskassociatedwithpovertyforinfantsandyoung
children,includingpoorercognitive,linguistic,social,andemotionalfunctioning(seeMcLoyd,1998,forareview).
Lessisknownaboutthebasicprocessesthatunderlietheassociationbetweenpovertyandpoordevelopmental
outcome—andthisisinnosmallpartduetothecomorbidityofriskfactorsassociatedwithpoverty,includingpoor
prenatalhealthcare(Laditka,Laditka,&Probst,2006),increasedexposuretodrugsinutero(Lester&Tronick,
1994;Liuetal.,2010),increasedratesofmaternaldepression(Tandon,Perry,Mendelson,Kemp,&Leis,2011;
Rafferty,Griffin,&Robokos,2010),lowlevelsofpaternalinvolvement(Fagan,Palkovitz,Roy,&Farrie,2009),and
higherexposuretoparentalconflict(Forehand&Jones,2003;Jones,Forehand,Dorsey,Foster,&Brody,2005)
andcommunityviolence(Forehand&Jones,2003).
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Fetal and Infant Neurobehavioral Development
Povertymaydirectlyinfluenceearlyneurobehavioraldevelopmentvis-à-visdeprivationofmicronutrients.In
familieswithinfantsandyoungchildren,limitedconsistentaccesstofood,orfoodinsecurity,isassociatedwith
lowerlevelsofallvarietiesoffoods,particularlyfruitsandvegetables(Kaiseretal.,2003).Infantsandtoddlerswho
experiencefoodinsecurityareatelevatedriskforiron-deficiencyanemia(Skalickyetal.,2006).Iron-deficiencyin
infancyisassociatedwithdysregulatedsleep–wakecyclesininfancy(Peiranoetal.,2010)andsloweractivation
ofvisualneuralpathwaysininfantsaged6–24months(Monga,Walia,Gandhi,Chandra,&Sharma,2010).
Environmentalleadexposureassociatedwithunhealthyhousingconditionsmayalsoplaceimpoverishedinfantsat
adisproportionateriskforpoorerneurobehavioraloutcomes(Gumpetal.,2007;2009).Ininfants,exposuretolead
isassociatedwithincreasedcardiacandneuroendocrinereactivitytostress(Gumpetal.,2007;2009).The
negativeandcumulativeimpactofleadexposureisevidentbyearlychildhood.Forinstance,higherbloodlead
levelsareassociatedwithattentiondeficitsinpreschoolchildren(Chiodoetal.,2007)andwithdisorderedconduct
(Markusetal.,2000)andlowerintelligence(Chiodoetal.,2007)inchildhood.
Anemergentbodyofresearchisbeginningtoexamineneurologicaldifferencesinyoungchildrenbasedonsocial
class.Inasampleof5-year-olds,Farahandhercolleaguesexaminedneurocognitiveprofilesoflow-versus
middle-classchildrenandfoundspecificdeficitsforlow-incomechildrenontaskstappingthe
left/perisylvian/languagesystemsandtheprefrontal/executivesystem(Noble,Norman,&Farah,2005).The
evidenceforlanguagedeficitsinchildrenoflowSESisconsistentwithfunctionalimagingresearchshowinga
positiveassociationbetweenSESandactivationintheleftinferiorfrontalgyrusin5-year-oldchildrenduring
completionofalanguagetask.Animalmodelsareconsistentwiththesedataandhighlightthemechanistic
importanceoftheearlyrearingenvironmentintermsofqualityofpostnatalmaternalcare(Caldjietal.,1998;Caldji,
Diorio,&Meaney,2000;Liuetal.,1997)andthelevelofenrichmentofthehomeenvironment(vanPraag,
Kempermann,&Gage,2000)ontheseeffects(seeHackman,Farah,&Meaney,2010,forareview).Themitigating
roleofearlycareenvironmentsissupportedinthehumanliterature.Forinstance,maternalengagementininfancy
andnotincome-to-needsratiopredictedsubsequentneuroendocrinedysregulationinalow-incomesampleof
infants(Blairetal.,2008).
Conclusion:InfantNeurobehavioralDevelopment
Theimpressiveneurobehavioralgrowthrealizedacrossthefirst2yearsnecessitatesapreparedbrain,anactive
infant,andasupportiveenvironment—allofwhichactinconcerttoadvancedevelopment.Earlyexperiencewith
selfandothersfuelsneurobehavioraladvancementsinbehavioral,motoric,andsocialandemotional
development.Acrossinfancy,thereiscomplexinterdependencyacrossthesesystems.Forinstance,thecapacity
toimitateothersisevidentatbirth(Meltzoff&Moore,1977;1983)andinmirrorneuronactivity(Marshalletal.,
2011;Southgateetal.,2010).Moreover,theinfant’scarefulobservationofthesocialworldplaysacentralrolein
thedevelopmentofaction(Learmonthetal.,2004;Lukowskietal.,2009),representation(Hamlinetal.,2008;
Mahajan&Woodward,2009;Sommerville&Woodward,2010;Woodward,1998),andsocialinformation
processing,includingemotionprocessing(Walker-Andrewsetal.,2011),socialreferencing(Campos,1980;
Mummeetal.,1996),andintentionality(Brooks&Meltzoff,2005).Experiencewithmovementisaffordedby
caregiverbehavior(Garrettetal.,2002;Majnemer&Barr,2005),andinfantactionitselfinformsperception
(Adolph,1997;2000;Camposetal.,2000)and,intandemwithactivationofhigherlevelattentionalmechanisms
(Lepage&Théret,2007),pavesthewayfortheinfanttobegininitiatingjointattentionviauseofgesture(Mundyet
al.,2000).Givensuchinterdependency,compromisedenvironmentalinputthatdampensanyoneofthese
systemswilllikelyresultincoststoothersystems.Thisisevidentinthecaseofbothmaternaldepressionand
poverty,eachofwhichisassociatedwithpervasiveandpersistentnegativeoutcomes.Maternaldepression
affectsinfants’basiccapacitytoreadsocialcues(Tronick&Reck,2009),andthisisevidentinthewithdrawn
behavioroftheinfant(Diegoetal.,2004;Tronick&Reck,2009)andsubsequentlowlevelsofsocialcompetence
(Wuetal.,2011)anddelayedlanguagegrowth(Brennanetal.,2000;Chapin&Altenhofen,2010)ofinfantsof
depressedmothers.Impoverishedcaregivingenvironmentsareassociatedwithahostofpooroutcomesacrossall
domainsofdevelopment(McLoyd,1998)andneurologicaldifferencesthatareevidentinchildhood(Hackmanet
al.,2010)andthatarelikelymediatedbythequalityofearlycareenvironments(Blairetal.,2008;Hackmanetal.,
2010).Insum,healthyneurobehavioraldevelopmentdependsonahealthy,expectantpostnatalbrain;the
continualbehavioralinputoftheinfant;andtheenvironmentalaffordancesnecessarytoaccomplisheach
interdependentmilestone.
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Fetal and Infant Neurobehavioral Development
FromFetustoInfant:FutureDirections
Inthischapter,wehavereviewedtheresearchonfetalandinfantneurobehavioraldevelopment.Althoughtothe
extentpossiblewehavereviewedresearchshowingparalleldomainsofdevelopment,thereiscurrentlyadearth
ofresearchthatdemonstratescontinuityfromthepre-topostnatalperiods.Expandingtechnologynowallows
researchersto“askthefetusquestions,”andthisworkclearlydemonstratesfetalcompetenciesandfetal
sensitivitytocontext(i.e.,theuterineenvironment).Inthefuture,longitudinalresearchthatmakesuseofparallel
methodsforassessmentduringpre-andpostnatalperiodswillbecritical.Longitudinalresearchthatuses
consistentmethodologiesmovingfromfetustoinfantwillelucidatetrajectoriestokeyoutcomesthatappropriately
highlightongoingperson-by-environmenttransactions,whichmayormaynotbeinterruptedbytheeventofbirth
itself.
Forfetusandinfantalike,developmentisshapedbytheenvironment.Researchonmaternaldepressionand
povertycitedhereinconvergetodemonstratethis.Movingforward,researchthatextendsthefocusonmothersto
thebroaderrearingecologyofthefamilysystemiswarranted.Althoughhistoricallyunderstudied,recentresearch
isamplyhighlightingtheimportanceoffathersas“partners”intheprenatalperiodandasparentsofinfants.For
instance,paternaldepressionintheprenatalperiodisdirectlyassociatedwithinfantirritability(vandenBergetal.,
2009).Furthermore,lackofpaternalinvolvementinthepostpartumperiodisassociatedwithincreasedseverityin
maternalpostpartumdepression(Séjourné,Vaslot,Beaume,Goutaudier,&Chabrol,2012).Qualityoffather–infant
interactionsdirectlypredictssubsequentbehavioraldevelopment,withhigherqualityinteractionsforetellingfewer
externalizingbehaviorproblems(Ramchandani,Domoney,Sethna,Psychogiou,Vlachos,&Murray,2013)and
bettersocialcompetencewithstrangers(Ferber,2010)intoddlerhood.Despitethisevidence,weknowlittleabout
themechanismsunderlyingpaternalcontributionstoearlydevelopment—forexample,nostudytodatehas
examinedthedirectroleoffathersinregulatingneurologicalorphysiologicalrespondingininfants.Fathersmay
alsotakeamore“active”or“direct”roleinshapingprenataldevelopmentbecauseepigeneticevidencedrawn
fromanimalsshowsanassociationbetweenpaternalstressexposurebeforethetimeofconceptionandblunted
HPA-axisrespondingtostressinductioninoffspring(Rodgers,Morgan,Bronson,Revello,&Bale,2013).Thiseffect
maybemediatedbyepigeneticalterationstogametes,asmalemiceexposedtochronicstresspriortomating(vs.
nonstressedexperimentalcontrols)showeddifferencesinthemicroRNAsoftheirsperm(Rodgersetal.,2013).
Hence,theroleoffathersmaynotbelimitedtoprenatal“support”systems,butinsteadincludedirecteffectson
antenataldevelopmentthroughepigeneticmechanisms.Futureresearchmustexpandonthepaternityliterature,
examiningboththedirectandindirecteffectsofpaternallifehistory,mentalhealth,andparentingpracticeson
bothfetalandinfantneurobehavioraldevelopment.
Inthischapter,wehaveprovidedanoverviewofthebasicprocessesunderlyingearlyneurobehavioral
development,whileemphasizingthecriticalroleofexperiencetherein.Perhapsthemostimportantextensionsof
thisbasicliteraturewillbeworkthattranslatesthisinformationintoappliedprogramming.Fromconceptionon,early
humandevelopmentismarkedbyanemerging,expectingbrainthatdependsonhealthyenvironmentalinput.At
nootherpointindevelopmentistheresuchopportunitytoenrich—orrestrict—neurobehavioralpotential.Thereis
clearvalueinmaximizingenvironmentalenrichmentbeforebirth.Forexample,inasmallsampleofsubclinically
stressedpregnantwomen,cognitivebehavioraltherapeuticinterventionduringpregnancywasassociatedwith
reductioninpregnantwomen’swakingcortisollevelsfollowingtreatment(Richteretal.,2012).Thestress-reducing
effectsofprenatalinterventiononneuroendocrinefunctioningmaypersistafterbirth;UrizarandMuñoz(2011)
foundthataprenatalstressmanagementinterventionreducedcortisollevelsinpregnantwomenatriskfor
depression(havingahistoryofdepressionoractivelydepressed)at6and18monthspostpartum.Given
associationsbetweenmaternalantenatalstressandpoorerbirthandinfantoutcomes,suchevidencepointstothe
benefitsofearlyinterventionforbothmotherandfetus.Importantly,plasticityremainsongoingafterbirth,and
additionalresearchshowsthatprenatalprogrammingcanbemodifiedbypostnatalfactors.Forexample,Kaplan’s
workcitedearliershowedthatinfantsofdepressed/anxiousmothersonlyshowedsignificantlyhigherbasalcortisol
(comparedtoinfantsofhealthywomen)whenthequalityofmaternalpostnatalcarewaslow(Kaplanetal.,2008).
Hence,pre-andpostnatalfactorsoperateinconcerttoshapedevelopment.Conceptualizingpre-andpostnatal
developmentwithasenseofcontinuity,andwithappreciationthatbothstagesofdevelopmentarecharacterized
bycomplexandongoingperson-by-environmenttransactions,mayallowthefieldtodesignprevention/intervention
programmingthatistailoredforbothcontentandtiminginsuchawaythatneurobehavioralpotentialisprotected
fromcompromiseand/orenrichedinawindowofmaximumopportunity.
Page 23 of 41
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Notes:
(1)Thetermgestationalageusedhereinincludesthe2weekspriortoconception,beginningwiththefirstdayof
themenstrualcyclepriortoconception.
CatherineMonk
CatherineMonkDepartmentofPsychiatryBehavioralMedicine&DevelopmentalNeuroscienceAssociateDirectorofResearch,
TheWomen'sProgramColumbiaUniversityMedicalCenter
AmieAshleyHane
AmieAshleyHane,WilliamsCollege
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