0066-4308/96/0201-0541$08.00 541

Annu.Rev. Psychol. 1996.47:541–61Copyright© 1996by AnnualReviewsInc. All rightsreserved

ATTACHMENT AND SEPARATION INYOUNG CHILDREN

TiffanyField

Touch Research Institute, University of Miami School of Medicine, P.O.Box 016820,Miami, Florida33101

KEY WORDS: psychobiological attunement, stress andcoping

ABSTRACT

Attachment theory is criticized for being basedon momentary stressful situ-ations, for being limited to behaviors that occur with the primary attachmentfigure, for including only overt behaviors in its paradigm, and for faili ng toconsidermultipleattachmentsatdifferentstagesof li fe.A model of psychologi-cal attunement is then presented andsupportedby several studiesdocumentingbehavioral, physiological, and biochemical responsesto separationsfrom par-entsandpeers.

CONTENTSINTRODUCTION..................................................................................................................... 541

Individual Differences......................................................................................................... 542TheBowlby-Ainsworth Modelof Attachment...................................................................... 543

PHYSIOLOGICAL DATA ON SEPARATION ...................................................................... 545Stressand Copingwith Separation ..................................................................................... 546Biological Markers and Mechanismsin Animal Models.................................................... 553Applicationsto the Human Infant........................................................................................ 556

PSYCHOBIOLOGICAL ATTUNEMENT: AN ALTERNATIVE ATTACHMENTMODEL............................................................................................................................ 558

INTRODUCTION

Attachmentand separationhavetraditionally beenstudiedin the contextofmother-infantand mother-childdyads.However,more recentresearchsug-

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gests theexistence of bonds similar to those in mother-infantandmother-childdyads,betweenpeersand betweenindividuals of different agesboth in hu-mans(Field 1985)and innonhumanprimates(Reite& Capitanio1984). Thus,attachmentis increasinglyconsidereda life-span phenomenon (Antonucci1976,Field 1985).The physiological responsesaccompanyingthe major at-tachmentbehaviors—smiling andcrying—are,in fact, independentof parent-hood,age,andsex(Frodi 1985).Attachmentis alsoconsidereda near-univer-sal process.In thisregard, Petrovich& Gewirtz (1985)have raisedtwo impor-tantquestions. Whatis theevolutionaryexplanation for the remarkablebehav-ioral similarity amongphylogenetically relatedor distantlyrelatedorganisms?Why are there importantbehaviordifferencesbetweenphylogenetically re-latedspecies?As an exampleof the latterquestion, they discussthe work ofCullen(1957)showingthatcertaincliff-nestinggulls, kittiwakes,do not learnto identify their offspring becausetheir offspring must remainin the nesttosurvive. In contrast,ground-nestinggulls closely relatedto kittiwakes mustlearnto recognizetheiroffspring becausetheiroffspringwanderfrom thenest.

An exampleof culturalvariationin humanattachmentbehavior isprovidedby Tronick et al (1985). Although the Westernizedversion of attachmentinvolves a single caregiverand its offspring, multiple caregiverattachmentsoccur in othercultures,such asthat ofthe Efe pygmiesof Zaire. Themother isnot thefirst to hold thenewborn.Instead,thenewbornis passedamongseveralother women.Further,although the infant is constantlyheld and fed on de-mand,it is often fed by other lactatingwomen.As a result, the infantswerenotedto developmultiple attachments. Tronicket al interpretedthesemultipleattachmentsasadaptivefor the infant’s growth andgroupparticipation. Thegrowthadvantagefor thesmallEfe newbornis thatmultiple nursingmotherscan provide maturemilk, which is richer than the colostrumof the infant’sbiological mother. In this way fluid balance ismaintained andgrowth isaccelerated.

Cultural and ecologicalvariation might explain much of the varianceinattachmentbehavior,although individual differenceshave also beennotedwithin the samecultural and ecologicalniches.Thesedifferencesmay havetheir originsin genetic,prenatal,or early environmentvariations.

Individual Differences

Bowlby’s (1969)seminalmodelof attachmentwasa normativeonethat didnot dealwith individual differencesin attachmentbehavior,althoughBowlby(1978) subsequently extendedhis model to include this variable. MaryAinsworth (1967) facilitated the study of individual differencesby devisingwhat hasbeenlabeledthe strangesituation paradigmanda systemfor class-ifying individual differences ininfants’ responsesto reunionswith their moth-ers following brief separations.Differencesin infants’ responsesweredocu-

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mented,andthesewerethenrelatedto behaviorsof themotherssuchastheirsensitivity andresponsivenessto infantsignalsduringtheirearlierinteractions.The paradigmsfor studyingattachmentsin humaninfants (Ainsworth) andalso in infant monkeys(the Harlows and their students)inspireddozensofstudies.Most of theseearly studieswere limi ted to the descriptionof overtbehavior.

Morerecently,studiesenabledby improvedmonitoringdeviceshaveinves-tigatedsubtleindividual differences inbiologicalmechanisms.

The Bowlby-AinsworthModel ofAttachment

Bowlby (1969) describedthe behaviorsof infants and young children whowerein residentialnurseriesandhospitalwardsandthereforeseparatedfromtheir mothers.The children who had experienceda securerelationshipwiththeirmothersshowedapredictablebehaviorsequenceduringtheirseparations.The sequencehas three phaseswhich Bowlby called protest,despair,anddetachment.Theinitial phase(protest)beganalmostimmediatelyandlastedafew hours to a week or more. Children in this phaseappeareddistressed,crying loudly, throwing themselves about, and looked eagerly toward anysight or soundthat could be their missing mother. Somechildrenclung to anurse as a substitute.During thedespair phase,the childrenshowed increasinghelplessness.Theywere withdrawn,physicallyactive, and criedonly intermit-tently. This wasa quiet stateandsometimeswasmistakenfor recovery.Thephaseof detachmentwasoften welcomedbecausethe childrenshowedmoreinterest in their surroundings, often smiled, andwere sociable. Whenthechildren’s mothersvisited,however,they remainedremoteand apathetic.

Ainsworth (1967)andher colleaguesstudiedattachmentbehaviorexperi-mentally during a seriesof brief laboratorysequenceslabeledthe “strangesituation” and,asstatedabove,attendedto differencesin the infants’ behav-iors.This situationstarts withthemotherandinfant together in astrange roomwith toys andproceedsthrougha seriesof differentexperiences,eachlastingaboutthree minutes.First, a femalestranger joinsthemotherand infant. Then,themotherleavesthe infant with thestranger.Thenthemotherreturns.Next,the mother leavesthe infant alone, andafter a brief interval the strangerreturns. Finally, the motherreturns.Theinfantsaregivenanattachmentclassi-fication on thebasis oftheiravoidant, enthusiastic, or variableresponsesto themother’s return.

Although the datareviewedby Bowlby (1969) and the strangesituationstudiesby Ainsworth andher colleaguesconvincingly demonstratea specialattachmentto the mother on the part of theinfant, at least in the NorthAmericancultures,themodelof attachmentderivedfrom thesedatahassomelimitations.First, in this model attachmentis basedon behaviorsthat occurduring momentaryseparations(stressfulsituations) rather than during non-

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stressfulsituations.A broaderunderstandingof attachmentrequiresobserva-tion of howthemotherandinfant interactandwhattheyprovidefor eachotherduring natural,nonstressfulsituations. The strangesituation paradigmmaysimplybetappingindividualdifferencesin thechildren’s copingwith momen-tarystress.Whatchildrendoasthemotherleavesandhowtheygreetherwhenshereturnsmayprovidelessinsight into thefunctionalsignificanceof attach-mentthanthewaymotherandchild relateto eachotherwhentheyaretogetherandnot stressed. An illustrationof theproblemwith using thechild’s responseto separationfrom and returnof the mother is that amongchildrenwho areattachedto their mothersas evidenced,for example,by their harmoniousinteractionstogether,someseemto havedifficulty makingtransitions.Thesechildrencling to their motherswhenthey aredroppedoff at nurseryschool,andtheyignoretheir motherswhentheyarepickedup after school(Fieldet al1984a).Both theclinging andthe ignoringbehaviorsresultin a classificationof thesechildrenas having an attachmentdisorder.In addition, most youngchildren following a more prolongedseparation(threedaysinsteadof threeminutes)rejecttheir mothersratherthangreetthemandseekphysicalcontact(Field & Reite1984).This behavioralpatternimplieseitherthatmostchildrenhaveattachmentdisorders orthat valid classification canonly bemadefollow-ing a very unnatural,ecologicallystrangethree-minutesituation.

A secondproblemwith the model is that, as in a circular process,attach-menthasbeendefinedon the basisof thosebehaviorsdirectedto the personreferredto as the attachmentfigure during an impendingseparation(suchbehaviorsas crying and clinging) and following reunion(proximity-seekingand greetingbehaviors).

A third problemis that the list of attachmentbehaviorsis limi ted to thosethatoccurwith theprimaryattachmentfigure, typically themother.However,otherattachmentsarenot necessarilycharacterizedby thosesamebehaviors.For example,infantsdo notnecessarilycling to peers or siblings,follow them,or cry duringanimpending departure,nor do theytypically run toand clingtothem as they return, yet infants are unquestionably attachedto peersandsiblingssuchthat they losesleepandbecomefussywhenthey areseparatedfrom theirpeers (Field etal 1984b).

A fourth limitation of the attachmentmodel is that the behaviorlist onlyincludesovertbehaviors.Datareviewedbelowin this chaptershowthatphysi-ological changesalsoaccompanyseparationsand reunionsandmay suggestalternativeexplanationsfor theattachment/separation phenomena.

A fifth considerationis thatin themodelsandthedatapresentedby Bowlbyand Ainsworth, the mother is viewed as the primary attachmentfigure. Al -though both authors acknowledge that other attachments may occur, themotheris treatedas the primary attachmentobject,and the fatherandothermembersof the family are consideredonly secondaryattachmentfigures.

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However,multiple, simultaneous attachmentsmay occur betweenthe childand the mother, father, and siblings that may also be consideredprimaryattachments,particularly in families wherefathersand siblings sharein thecaregiving.As in infancy, multiple attachments may occur simultaneouslythroughoutadulthood;for example,to a spouseandfriend,aswell asto one’schildren.That raisesa sixth problem:In themodel,attachmentis confinedtothe infancy andearly childhoodperiod,ending,asnotedby Bowlby, duringpuberty.It doesnot considerattachmentsthat occurduring adolescence(thefirst love), during adulthood(spousesand lovers),and during later life (thestrongattachmentsnotedbetweenfriendsin retirement).Somemayclaim thattherecentlydesignedAdult AttachmentInterviewacknowledgesadultattach-ment.However,it is not focusedon adultattachmentsto otheradults.Rather,it is a memory-basedinstrument usedto assessadults’ attachmentsto theirparents duringchildhood.

A parsimoniousmodelof attachmentwould needto accommodate multipleattachmentsto a variety of figuresat differentstagesof life. We haveusedamore psychobiological approachin formulating a model that focuseson therelationshipbetween twoindividuals and whatthey share andwhatmight thenbemissing whentheyareseparated.In this model(Field 1985),attachmentisviewedasa relationshipthatdevelopsbetweentwo or moreorganismsastheybecomeattunedto eachother,eachproviding theothermeaningful stimulationandarousalmodulation.The lossof this importantsourceof stimulation andarousalmodulation, which occursin separation,invariably resultsin behav-ioral and physiological disorganization.Both this model and the Bowlby-Ainsworthmodelwill beconsidered throughout as Ireview thedata on attach-mentand separation.

PHYSIOLOGICALDATA ON SEPARATION

Physiologicaldata recordedduring the separationsof young primatesandchildrenfrom their mothersconfirm thebiphasicresponseto separationnotedby Bowlby (1969) as protest and despair,which is a period of agitation,followed by a periodof depression.Theprimatedataarebasedon mother-in-fant pigtail andbonnetmonkeyseparationsmonitoredby surgicallyimplantedtelemetry (Laudenslager etal 1982, Reite & Capitanio1984, Reiteetal 1981b,Reite & Snyder1982). Generally,in thesestudies behavioralagitation wasfollowed by depressionduring theseparationperiod.Shortlyafter thesepara-tion, the infantsexhibitedagitationcharacterizedby increasedmotor activityand frequentdistressvocalizations. Depressedbehaviorstypically emergedshortly thereafterandpersistedthroughoutthe separationperiod.The infantsmoved more slowly than normal, and their play behaviorwas diminished.Sleep disturbanceswere characterizedby decreasedrapid eye movement

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(REM) sleepas well as by increasedarousalsand time spentawake.Theagitatedbehavior thatoccurred immediately after separationwas accompaniedby increasedheartrateandbody temperaturefollowed by decreasesin thesevalues tobelowbaseline(Reite etal 1978).

In additionto behavioralandphysiological disorganization,alteredcellularimmuneresponseswerenotedin theseparatedpigtail monkeysby Reiteet al(1981a)andin thesquirrelmonkeysby Coeet al (1985).For example,duringtheseparationof two pigtail monkeys whohadbeenrearedtogether,analteredcellular immuneresponseoccurred(Reiteet al 1981a).At five weeksfollow-ing reunion,the cellular immuneresponseof both monkeyswasstill slightlydepressed.Pigtail infantsseparatedfrom their mothersalsoexperiencedper-sistentseparationeffects.For example,althoughheartratetendedto returntobaselineand arrhythmiastendedto disappearfollowing the infants’ reunionwith their mothers,thealteredcardiacactivity persistedfor someinfant mon-keys(Seileret al 1979).In anotherstudy,persistentdecreasesin infant heartrate and body temperaturewere noted following reunion with the mother(Reite& Snyder1982).Thus,the effectsof theseseparationsoften persistedevenafter reunionwith an attachmentfigure suchas the motheror a peer.Similar datahavebeenreportedfor hospitalizedpreschoolchildrenwho werereceivingchemotherapyfor childhood cancer(Hollenbecket al 1980). Thedisorganizingeffectsof separationgenerallyparalleledthosereportedfor pri-mates.Behaviorally, the childrenfirst showedagitation andthendepression,as manifested by their play behavior, behaviors that were paralleled bychanges inbodytemperature andheart rate.

StressandCoping with Separation

SEPARATION IN INFANTS AND CHILDREN In a study of preschoolchildren’sresponsesto separationfrom themotherduringthebirth of anotherchild (Field& Reite 1984), agitatedbehaviorand physiology during the period of themother’s hospitalizationwereobserved.Depressionthenfollowed in thechil-drenafterthemother’s returnfrom thehospital. In theField& Reitestudy,playsessionswere videotaped,night-time sleepwastime-lapsevideotaped,andtheparentswereadministeredquestionnairesonchangesin theirchild’s behaviors.Increasesin negativeaffect,activity level,heartrate,nightwakings,andcryingcharacterizedtheperiodof themother’s hospitalizationasoneof agitationforthe children(seeFigures1 and2). Longerperiodsof deepsleepat this stagewereinterpretedasconservation-withdrawal(asif withdrawingfrom stimula-tiontoconserveenergy)(seeFigure2).Followingthemother’s return,decreaseswere observedin positive affect, activity level, heart rate,and active sleep,suggestiveof depression(seeFigures1–3). Changesreportedby the parentsincludedgreaterclinging andaggressivebehaviors,eatingandtoileting prob-

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lems,anddisturbedsleepand illnessesthat persistedfollowing the mother’sreturnfrom thehospital(Figure4). Examplesof thechild’s disturbancewererevealedin parents’ commentsthat thechild “wantedto berockedandheld,”“revertedto babytalk, whining,andscreamingfor attention,” and“threatenedto run a truckacrossthebaby’s head.”Elevatedtonicheartratein thechildrenduringthemother’s hospitalizationanddepressedheartratefollowingherreturnmayhavebeenmediatedby theactivity level changes,asin somaticcouplingof activity andheartrate(Obrist1981).Theseelevatedlevelshavein turnbeenattributedto sympatheticadrenergicactivation(Breeseet al 1973).More pro-longedperiodsof deepsleepduring this phasemaybetheresultof conserva-tion-withdrawalnotedto follow stressin infantsandyoungchildren(Emdeetal 1971,Engel& Schmale 1972).

Decreasedactivity, depressedheart rate,and shorterperiods of activesleep,together with flat affectfollowing the mother’s return maysuggestdepression.Depressedchildrenhavelessactivesleep(Kupfer et al 1979),anddepressioncan be alleviatedby depriving subjectsof REM sleep(Vogel 1979). Thedecreasein active sleepmaybe a homeostatic copingmechanism.

Depressedactivity andheartratearecommonly reportedwhenindividualsarein situations inwhich they arehelpless,suchas anavoidance taskin whichhumansubjectshaveno control,situations in which adrenergicinfluencesareminimal (Obrist et al 1978).Bradycardia,associatedwith situations of help-lessness,hasalsobeenattributed to parasympathetic activationor vagaltone(McCabe& Schneiderman1983).The arrival of a new sibling; a lessactive,tired mother;and changesin children’s play interactionswith their mothermay havebeenviewedby the children in the Field & Reite (1984)studyassituations overwhich theyhadvery little control.The depressedbehavior may

Figure 1 Meanactivity level andheartratein beatsperminute (BPM) of childrenprior to theirmother’s hospitalization(PREHOSP),duringhospitalization(HOSP),andfollowingherreturn fromthehospital (POSTHOSP) (from Field& Reite 1984).

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havebeenexacerbatedin thesechildrenby thearrival of thenewsibling andan altered relationship with themother.

Heightened levelsof arousalmay stimulate the sympathetic adrenergicsystem,resulting in agitatedbehavior.This behavioris typically associatedwith activecoping,in this casewith attemptingto recall themother.Agitationduring separationmay occurbecauseof heightenedarousalin the absenceof

Figure 2 Children’s night wakings, crying, total sleeptime, andduration of deep-sleepstagesduring recordingsfor baseline(B), separationperiod (S),andfollowing reunion (R).

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thechild’s principalarousalmodulator,themother. Depressionmayemergeastheseparation continuesbecauseof thechild’s failureto bring themotherbackandof a lackof stimulationordinarilyprovidedby the mother. The depressionmay be an adaptivehomeostatic mechanismoffsetting the effectsof sympa-

Figure 3 Proportion ofmother-child play timein which smiling and animation wereobserved inthechild during videorecordingsfor baseline(B), separationperiod(S),andfollowing reunion(R).

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thetic arousal,or it may result from inadequateamountsof stimulation andlimitedbeta-adrenergicactivity. Confounds in theField & Reite(1984)studyon separationeffectswere the changedrelationshipbetweenthe motherandfirst-born becauseof the arrival of the new sibling, the exhaustionof themother,andvery frequentlythe postpartumdepressionof the mothersthem-selves.Theseconfounds,coupledwith theconcerngeneratedby datashowingthat repeatedseparationshadcumulative effectson monkeyinfants,led us toperform a study looking at repeatedseparationsof children from mothers

Figure 4 Numberof childrenwhoexperiencedfeeding, toiletingandsleepingchanges,andil lnessduring the separation-reunionperiod.

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goingon conference trips(Field1991).Althoughthepreschoolchildrenin thestudy showedsimilar separationbehavioras when the motherswent to thehospital,theydid not continueto showdepression-relatedbehaviorafter theirmothersreturned.In addition, thefirst trip hadtheworst effect, andthe effectswerenotcumulative.Perhapsit is notsurprisingthatbecauseof theircognitivecopingskills, the childrenwere able toadapt tothatstress.

PEER SEPARATIONS A surprisingfinding for manyattachmentresearchersisthat early peer separationsalso are distressingfor young children. A peerseparationthat occursnaturally and with somefrequencyresults from thetransferof childrento new schools.In a recentstudy,Field (1984)observedpreschool childrenwhohadbeentogetherfor threeto four yearsandwhoweretransferringto new schools.The observationsweremadeduring a two-weekperiodprior to theseparationfrom their classmates(Field 1984).Thechildrenwho wereleavingthe school,asopposedto thosewho werestaying, showedincreases(comparedwith baselineobservationsthreemonthsearlier)in fantasyplay,physicalcontact,negativestatementsandaffect,fussiness,activity level,tonic heartrate,andillness,aswell aschangesin eatingandsleepingpatterns(seeFigures5–8).In addition tothechangesin playbehaviorandin vegetativefunctions, the children’s drawings ofthemselves manifestedagitation anddisorganization. The drawings included distortedfacialandbody parts and sadfaces(see Figure 8).

The anticipatory reactions to separation by these childrenappeared tomimic the immediateresponsesto peerseparationsby youngmonkeys(Reiteet al 1981b).They were also very similar to the behaviorsnoted in youngchildren immediately following the hospitalization of their mothersfor thebirth of anotherchild (Field & Reite1984). In thesestudies,the increaseinfussiness,negativeaffect, aggressivebehavior,physical activity level, andtonicheartratearesuggestiveof agitation.Althoughchangesin eatingpatternswere variable,with somechildren eatingmore and otherseatingless,sleepdisturbancesuniformly involved more frequentnight wakings, crying, anddelayedonsetof sleep.Increasedillness during the children’s separationsisconsistentwith reportsof changesin the immunesystemof youngprimatesduringmotherand peer separations(Reiteet al 1981a,Reite& Snyder 1982).

Separationstressoccurswhenpeersevenasyoungas15 monthsaresepa-rated(Field et al 1984b).In the Field et al study,15-month-old infantsweretransferred, following14 monthsin aninfant nursery, to atoddler nursery, and24-month-old infants were graduatedfrom a toddler nurseryto a preschoolnursery.Many of thesamebehaviorchangesoccurredduringtheweekimme-diately preceding the transferand the weekfollowing the transfer.Theseincludedincreasedinactivity, negativeaffect,fussiness,andchangesin eatingandsleepbehaviors.Nap-timesleepbecamemoreirregularwith longerlaten-

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Figure5 Proportionof peer-play-timenegativefaces,fussiness,andverbalandphysicalaggressionoccurringduring the baseline (B)andpreseparation (P)observationperiods.

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ciesto sleepandmorefrequentarousalsduring naptime. In addition, erraticfeedingpatternswere notedas well as more frequentillness.A comparisonbetweenthoseinfantsandtoddlerswho weretransferredto thenewnurserieswithout closefriendsandthosewho weretransferredwith closefriendssug-gestedthat transferringwith closefriendsmay buffer the stressfuleffectsoftheseparation.Thus, thedata from this group ofstudies areapoignant demon-stration of thedisorganizingeffectsof mother andpeerseparations on boththebehavior andphysiology of youngmonkeysandchildren.

Biological MarkersandMechanismsin AnimalModels

Pankseppet al (1985) have advanceda model for attachmentbaseduponopiatesystems andderivedfrom dataonverydiversespeciesincludingchicks,guinea pigs, and dogs.Because thesocial-separationstate was similar toopioid withdrawal in their studies,opiatereceptoragonistswereexpectedtoreduceseparationdistress.TheopioidagonistsPankseppetal testeddid allevi-ateseparationdistress,andwhenthey blockedopioid receptorsby naloxone,separationdistressincreased.Theythenevaluatedthespecificityof theopioideffectsusinga varietyof agonistsandantagonistsfor cholinergic, noradrener-gic, dopaminergic,andserotonergicreceptorsystems. Only clonidine(whichalleviatesopiatewithdrawal symptoms in humans)approachedthe level ofefficacyof opioids.

Figure 6 Meanactivity levelandheartratein beatsperminute(BPM) of childrenduringpeerplayfor thebaseline(B) andpreseparation (P)observation periods.

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In anothermodel,Kraemer(1985)postulatedthat early socialdeprivationmay exert its effects through deprivation-induced(or denervation-induced)supersensitivity, possibly of noradrenergicsystems.Isolatedrodents,for ex-ample,becomehyperactivewhenplacedin a novelenvironment.This hyper-activity canbe preventedby antidepressantagents.Kraemerstatedthat “the

Figure 7 Number of childrenwho experiencedfeeding, toileting, sleeping, andil lnessproblemsduring the baseline (B)andpreseparation (P)observation periods.

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Figure8 Examplesof self-drawingsmadeprior to thedepartureof childrenattendingnewschools.

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behavioraleffectsof antidepressantagentsin previouslyisolatedsubjectsmaybe dueto their ability to reduceisolation-inducedsupersensitivity of corticalsystemswith noradrenergic inputs” (p. 152).

Coeetal (1985)havepresentedaseparationmodelin which theyarguethatanacuteresponseto separationmaybeadaptive,but dataon sustainedsepara-tions suggestthat prolongedcortisol elevationscan adverselyaffect the im-munesystem(at leastin squirrel monkeys).Sustainedelevationsof cortisoland theabsence of behavioralsymptoms maybe a manifestationof depressionnotunlike the sustainedelevationsof cortisolfrequentlynotedin depression.

Applications to theHumanInfant

In Bowlby’s (1969) descriptions, protestwas typically followed by despairduringthechild’s separationfrom its mother.Thedatareviewedin thischapteron the separationsof youngprimatesandyoungchildrenconfirm a biphasicresponseto separationwith an agitatedperiodtypically followed by a periodof depression.In the studiesby Reiteandhis colleagueson infant monkeys,infantsexhibited an agitationreactionthat includedincreasedmotor activity,frequentdistressvocalizations,andelevatedheartrateandbody temperatureimmediately after the separation.This agitation reactionwas typically fol-lowed by depressedbehaviorand decreasesto below baselinein both heartrate and body temperature.Similarly, in the Field & Reite (1984) study onchildren’s separationsfrom theirmothersduringhospitalizationfor thebirth ofanotherchild, agitatedbehavioroccurredimmediatelyfollowing the separa-tion, with increasesin negativeaffect,activity level,heartrate,night wakings,and crying. Following themother’s return, decreaseswere noted in thesemeasures, suggestive of depression.

Movesto newplacesweretheonly separationsituations thatdid not resultin a biphasic processof agitationfollowed by depression.For example,lessdepressionwas noted in separatedmonkeysmoved away from their socialgroup toan isolationcage(Reite 1983), andinfants, toddlers, andpreschoolersapparentlydid not experiencedepressionwhen they were moved to a newclassroom(Field et al 1984b)or a new school(Field 1984). In the studyoninfant monkeys,only approximately 15% of the infants becamedepressedwhentheywereseparatedfrom both their mothersandtheir socialgroupandplacedin isolation,while asmanyas80%of themonkeysbecamedepressedifthey remainedin their socialgroupwithout their mother(Reite1983).Reitespeculatedthat thepigtail infantswho wereseparatedfrom both their motherandpeersandplacedin isolation did not showbehavioralandphysiologicaldepressionperhapsbecauseisolation is a fearful experience.Fearmay coun-teract the expecteddecreasein beta-adrenergicactivity typically associatedwith depression.

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Remaining afterseparationin anenvironmentthatremindstheinfant of itsmother may be more distressing for the infant than moving to a differentenvironment.The children who were leaving their peersfor a new school(Field 1984) did not appearto experiencethe biphasicprocessof agitationfollowed by depression.The anxiety relatedto attendinga new schoolandmakingnew friendsmay haveoffset any expecteddepression.The stressofjoining a newgroup mayhave compoundedthe separationstress,thussustain-ing the agitatedbehaviorand physiology. New stressesmay presentactivecopingopportunitiesfor the departingchildren,while the remainingchildrenmayfeel “stuck” in a passivecopingor helplesssituation of continuallybeingremindedof their missing peersby thoseenvironmental featuresassociatedwith them.

Coe & Levine (1983) havesuggested that theabsenceor unpredictability ofreinforcementunderconditions where reinforcementhasbeencontinuouslypresentwill leadto a stressresponse.Similar to severalotherresearchers,hehasdesignatedcontrolor theability to makea copingresponseastheprimarymechanismin dealing with stressand the lack of control associatedwithhelplessness(Seligman1975,Weiss1971a,b).

Thesepropositions suggestthat separationmay be stressfulto the infantand young child becauseof the loss of a major sourceof reinforcement;reinforcementis typically provided by the mother in the form of adequatestimulation and arousalmodulation. Loss of control, feedback,and predict-ability, which areclearly importantfeaturesof their interaction(Field 1978),couldalsooccurduringseparation.An activecopingresponseof theinfant intheseparationsituation might beeitherto seekstimulation andreinforcementfrom othermembersof thegroup(asa substitute for mother)or to temporarilywithdrawfrom interactionswith the groupand becomeinactive.

We have arguedelsewhere(Field 1985) that separationdistressoccursprimarily becausethe infant has lost its primary sourceof stimulation andarousalmodulation.Auntsin thecaseof infantmonkeysandfathersin thecaseof humanchildrenmayserveassubstitutecaregivers.However,theymaynotbeaseffectiveasthemotherin providing stimulationandarousalmodulationbecausetheyaretypically not asfamiliar with thechild’s individual needsforstimulationandarousalmodulation.Thus,a monkeyor humaninfant,alreadyhighly agitatedbecauseof theabsenceof themother,maybecomeevenmoreagitatedduringanyattemptsmadeby substitutecaregiversto providestimula-tion andarousalmodulation. In this case,the mostadaptiveresponsefor theinfant may be to withdraw andremaininactivein orderto avoid thestimula-tion of othersor the stimulation of its own activity. Depressedactivity orconservation-withdrawalmaycontinueat leastuntil physiological equilibriumis restoredor until conspecificshavebecomefamiliar with the individual’suniquestimulation and arousalmodulation needs.In this model, temporary

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depression andinactivity maybe seenasadaptive behavior forwarding offthehighly stimulatingbehaviorof othermembersof thegroupat a time whentheinfant is vulnerableto heightenedarousallevels due to the absenceof itsprimaryarousal modulator, the mother.

Depressionalsoservesasa periodof physiological recuperationfrom thepreviousagitationphase.Depression,helplessness,andpassivecoping,how-ever,areoften consideredunhealthyexperiencesthat may contribute to dis-easeand death.This may especiallybe the casewhen depressionis experi-encedfor prolongedperiods.However,in theshorttermdepression,helpless-ness, and passive coping may be the only immediately effective copingmechanismsavailableto the young organismseparatedfrom an attachmentfigure.Temporarydepressionor conservation-withdrawalmayserveaseffec-tive coping mechanismsuntil physiological equilibrium is restoredand themotherreturns, oran effective substitute attachmentfigurebecomes available.

PSYCHOBIOLOGICALATTUNEMENT: AN ALTERNATIVEATTACHMENT MODEL

Researchon attachmenthasbeenconductedin theseparationcontext,andtheproposedpsychobiological mechanisms andtheoriesof attachmenthavebeeninferredfrom separationeffects.An attachmentmodelderivedfrom researchon mother-infantseparationeffectsis not only limited becauseit pertainstoonly onetypeof attachmentbutalsobecause separationmodelsdo not specifywhat is ordinarily presentin a relationship that is thenmissingduringsepara-tion. Further,thedisorganizing effectsof theseparationoftenpersistfollowingreunionof theattachedpair.Thus,separationperseis not theonly disruptionto anattachmentbond.As Field(1985,pp. 415–16)hasnoted:

A better understandingof theprocessmayrequire thestudy of multiple kindsof attachments at different li fe stages andmayinclude both overt and physi-ological behaviors that occur whenattached individuals areboth togetherandapart.…Attachment might instead beviewed asa relationship that developsbetweentwo or moreorganismsastheir behavioral and physiological systemsbecome attuned to each other. Each partner provides meaningful stimulationfor theotherand hasamodulating influenceon theother’s arousal level. Therelationship facil itatesanoptimal growth statethat is threatenedby changesinthe individuals or their relationship or by separation and the behavioral andphysiological disorganization that ensue. Thus, attachments are psychobi-ologically adaptive for theorganization,equili briumandgrowth of theorgan-ism.Becausetheorganism’s behavioral repertoire,physiological makeup,andgrowth needsarean integrated multivariate complex that changes develop-mentally, multiple and different typesof attachments areexperienced acrossthe lif espan.

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In a similar vein, Reite& Capitanio (1985)suggestedthat “attachmentinfact representsa neurobiologically basedandmediatedbiobehavioral systemoneof whosemajor functionsis to promotethe developmentandregulation(or modulation) of psychobiological synchronybetweenorganisms”(p. 224).Supportfor this modelcomesfrom different species.In separatedratsgivensubstitute milk and heat,physiological and behavioraleffectsof separationpersisted(Hofer 1981).Hofer suggested“a view of the motherasan eternalphysiological regulatingagentcontrolling autonomic cardiovascularbalanceby thelevel of milk shesupplies.”Similarly, simulatedmaternallicking of ratpupsreversedthegrowthhormonedeficitsassociatedwith separation(Kuhnetal 1978). In humanneonates,maternalcaretakingand sleep-wakeactivitycycles becamesynchronizedonly in the presenceof a consistentcaregiver(Sanderet al 1970).Similarly, behaviorandheartrateof slightly olderinfantsandmotherssharea commonvarianceduring early interactions(Lesteret al1982)andduring later strangesituationsessions(Donovan& Leavitt 1985).Thissynchronydoesnothappenduringinteractionswith strangers(Yogmanetal 1983). Married couplessharebehavioraland heart-raterhythms duringinteractions(Levenson& Gottman1984)aswell ascycling of cortisol levels(Lundberg etal 1981).

One of the most salientexamples,perhaps,is that providedby Reite &Capitanio(1985) on infant monkey peers.The heart ratesof two attachedpigtail infants who had been rearedtogetherwere highly correlated.Thisrelationshipdecreasedduringseparation.Followingreunionthecorrelationsoftheir heartratesandbody temperaturesreturnedto baseline.In contrast,heartrateandbody temperaturewerenot correlatedin two mother-rearedmonkeyswho werenot attachedto eachother.Similarly, time spentin deltasleepwashighly correlatedfor the attachedpair but not for the unfamiliar peers.Al -though Reite & Capitanio offered thesedata as tentativeevidencefor thepotencyof reciprocalentrainmentof rhythmsin attachedindividualswho areattached,theseinvestigators also raised important empirical questions:“Ifattachmentfacilitatessynchronyof rhythmsbetweenindividuals,is this cen-tral toattachment,a precondition for attachment, anoutcomeof attachment,oran epiphenomenon?” (p. 243). Thesequestions offer future directions forresearchon the psychobiology of attachmentand separation.

ACKNOWLEDGMENTS

This researchwas supported by an NIMH ResearchScientist Award(#MH00331)and an NIMHResearch Grant (#MH46586)to Tiffany Field.

Any Annual Reviewchapter, aswell asany arti clecited in an Annual Reviewchapter,may bepurchased fromthe Annual ReviewsPreprints and Reprints service.

1-800-347-8007; 415-259-5017; email: arpr@class.org

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Annual Review of Psychology Volume 47, 1996

CONTENTSASPECTS OF THE SEARCH FOR NEURAL MECHANISMS OF MEMORY, Mark R. Rosenzweig 1 THEORETICAL FOUNDATIONS OF COGNITIVE-BEHAVIOR THERAPY FOR ANXIETY AND DEPRESSION, Chris R. Brewin 33THE DESIGN AND ANALYSIS OF SOCIAL-INTERACTION RESEARCH, David A. Kenny 59PERSONALITY: Individual Differences and Clinical Assessment, James N. Butcher, Steven V. Rouse 87HEALTH PSYCHOLOGY: Psychological Factors and Physical Disease from the Perspective of Human Psychoneuroimmunology, Sheldon Cohen, Tracy B. Herbert 113VERBAL LEARNING AND MEMORY: Does the Modal Model Still Work?, Alice F. Healy, Danielle S. McNamara 143LONG-TERM POTENTIATION AND LEARNING, Joe L. Martinez Jr., Brian E. Derrick 173CROSS-CULTURAL SOCIAL AND ORGANIZATIONAL PSYCHOLOGY, Michael Harris Bond, Peter B. Smith 205STEREOTYPES, James L. Hilton, William von Hippel 237

EXPERT AND EXCEPTIONAL PERFORMANCE: Evidence of Maximal Adaptation to Task Constraints, K. A. Ericsson, A. C. Lehmann 273TEAMS IN ORGANIZATIONS: Recent Research on Performance and Effectiveness, Richard A. Guzzo, Marcus W. Dickson 307PSYCHOLOGY IN CANADA, J. G. Adair, A. Paivio, P. Ritchie 341METHODOLOGICAL ISSUES IN PSYCHOPATHOLOGY RESEARCH, K. J. Sher, T. J. Trull 371THE SOCIAL STRUCTURE OF SCHOOLING, Sanford M. Dornbusch, Kristan L. Glasgow, I-Chun Lin 401ORIGINS AND EARLY DEVELOPMENT OF PERCEPTION, ACTION, AND REPRESENTATION, Bennett I. Bertenthal 431AUDITORY PSYCHOPHYSICS AND PERCEPTION, Ira J. Hirsh, Charles S. Watson 461ENVIRONMENTAL PSYCHOLOGY 1989–1994, Eric Sundstrom, Paul A. Bell, Paul L. Busby, Cheryl Asmus 485COGNITIVE SKILL ACQUISITION, Kurt VanLehn 513ATTACHMENT AND SEPARATION IN YOUNG CHILDREN, Tiffany Field 541COVARIANCE STRUCTURE ANALYSIS: Statistical Practice, Theory, and Directions, Peter M. Bentler, Paul Dudgeon 563THE MOTIVATIONAL IMPACT OF TEMPORAL FOCUS: Thinking About the Future and the Past, Rachel Karniol, Michael Ross 593

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