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Elfenbein, H.A., & Ambady, N.(2002b). (See References)

Russell, J.A. (1994). (See References)

Acknowledgments—

We thank JamesRussell, Anita Williams Woolley, andKevyn Yong for their helpful commentson the manuscript.

Notes

1. Address correspondence to Hill-ary Anger Elfenbein, Haas School ofBusiness, University of California, Ber-keley, CA 94720-1900; e-mail: hillary@post.harvard. edu.

2. We do not refer to the universalaffect program as a facial affect pro-gram in order to emphasize that it in-cludes additional nonverbal channelsof communication, such as vocal toneand body movements.

3. We thank James Russell for thisobservation.

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of emotion from facial expression? A review ofthe cross-cultural studies.

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where are the primary affects: Some evidencefor a theory.

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Crib Death: A Biobehavioral Phenomenon?

Lewis P. Lipsitt

1

Department of Psychology, Brown University, Providence, Rhode Island

Abstract

In developed countries,more children under 1 year ofage die of crib death (suddeninfant death syndrome, SIDS)than of all other causes com-bined. Researchers and clini-cians have proposed manypossible causes of SIDS, but theabrupt, unexpected death ofsome babies remains mysteri-ous and frightening. Althoughinfant behavior may explainsome of these deaths, scant at-tention has addressed behav-ioral characteristics of babieswho die without medical ex-planation. Any explanation ofSIDS must account for the fact

that most SIDS deaths occur at2 to 5 months of age, acknowl-edging that a protective mech-anism appears to spare babiesbefore 2 months but then dis-appears. The respiratory occlu-sion reflex serves as an initialdefense against smotheringand can provide such an expla-nation. Infantile reflexes wane,after providing opportunities forlearned responses to be acquired.During this well-documentedneurobehavioral transition fromsubcortical to cortically mediatedresponding, some babies, viablefor the first 2 months, may be-come especially vulnerable ifthey fail to acquire sufficiently

strong defensive behaviorsneeded to prevent occlusion af-ter the waning of the life-pre-serving reflex. Recent successof back-to-sleep directives,urging that babies sleep ontheir backs to avoid smother-ing, supports this hypothesis.

Keywords

sudden infant death syn-drome; crib death

Until about 40 years ago, when ababy died of no apparent or diag-nosable cause, the medical exam-iner was likely to state that thedeath was due to pneumonia. Ag-grieved parents usually acceptedthis medical explanation, believingtheir baby died of a “disease.” Inthe 1960s, however, parents’ dis-pleasure with gratuitous diagnosesand chagrin over false accusationsof neglect and abuse, among otherfactors, led to a change in attitude.A small group of sympathetic pedi-

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CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE 165

atricians and pathologists joinedparents in lobbying for researchinto the causes of crib death, orsudden infant death syndrome(SIDS). Doctors and researchers be-gan to question the processes un-derlying the death of infants in theabsence of foreboding signs of ill-ness. Funds were invested in crib-death research and counseling forfamilies trying to cope with SIDS.This collaboration of parents, prac-ticing physicians, and researchersprovided helpful but inconclusiveinsights that pointed to multiplecauses of SIDS (Hunt, 2001). It alsoled to great disappointments, doc-umented by Firstman and Talan(1997), when it was discovered thatsome cases previously diagnosedas SIDS were infanticides. Al-though murder is itself a behav-ioral act, there remain other behav-ioral issues—in particular, theneurobehavioral development ofthe baby victim—to be studied fur-ther in connection with SIDS. It ismy contention that insufficient at-tention has been paid to the likeli-hood that the behavior of babiesplays a significant role in infantdeaths that occur without medicalexplanation. The importance ofdiscovering the cause of crib deathis made poignant by the fact thatmore infants die of SIDS than of allother causes combined.

The definition of SIDS, estab-lished in 1969, has been solidifiedthrough legislation (upon recom-mendation of a consensus team ofexperts assembled by the NationalInstitute of Child Health and Hu-man Development) as the suddendeath of an infant younger than 1year that remains unexplained af-ter a thorough investigation in-cluding complete autopsy, exami-nation of the death scene, and reviewof the clinical history (Hunt, 2001,p. 346). Even after refinements ofdiagnosis, however, the phenome-non remains a mystery, and thou-sands of cases are still diagnosed as“unexplained.” The term unex-

plained, of course, indicates that theSIDS phenomenon remains a mys-tery, and that SIDS is essentiallyused as a residual diagnosis (i.e.,the SIDS designation is used afterall plausible causes are investi-gated and discarded). Although adiagnosis of “no finding” canhardly be satisfying, the designa-tion of a medically accepted “syn-drome” has had the effect of mini-mizing parents’ feelings of guiltand averting callous accusations,by reducing the likelihood of im-plied neglect or abuse.

THE SIDS PHENOMENON

In developed countries, the mostcommon cause of death in the firstyear of life after the first few daysis SIDS, which usually occurs atnight while the infant and familysleep. In the absence of anythingmore than circumstantial evi-dence, the death is sometimes at-tributed to an upper respiratory in-fection, such as a cold. Usually, thebaby is regarded as having beennormal and of good health whendeath occurred. The incidence ofcrib death today in the UnitedStates is between 2 and 3 deathsper 1,000 births, higher for Blacksthan Whites, and for males than fe-males.

Raring (1975), who lost a child toSIDS, attempted to arouse medicalconcern when he wrote that thedisorder probably killed 10,000 to20,000 infants in the United Stateseach year. Numerous hypothesesto account for SIDS had been ad-vanced unsuccessfully, he said, in-cluding disorders of the thymusgland, prematurity or low birthweight, accidental overlaying (roll-ing over on the baby while sleep-ing), suffocation by vomit, hyper-sensitivity to cow’s milk, immatureheart, sleep disorder, calcium ormagnesium deficiency, prenatal orpostnatal drug abuse, air pollution,

fluoridation of the water supply,parental smoking, use of bleach indiapers, venomous insect bite, andapnea (a brief interruption of nor-mal respiration, usually lasting 5–10 s). He chided medical scienceand the government for not search-ing deeply enough for answers.

Interestingly, Raring (1975) dis-missed the possibility of suffoca-tion:

Doctors have made very carefully con-trolled experiments which prove con-clusively that even the smallest andweakest of babies have no trouble at allin squirming out from under un-wanted coverings. All parents knowthat well. Besides, the idea is incompat-ible with the well-known facts that thevery young baby and therefore the oneleast likely to be able to put aside cov-ers and to turn its head away from thepillow, is far less likely to become a cribdeath victim than are older, strongerbabies. (pp. 63–64)

Raring was correct that very youngbabies are less vulnerable to SIDSthan are older infants, but he drewthe wrong inference from this be-cause he did not consider an im-portant behavioral feature of earlyinfant development. In this article,I propose a psychobiological expla-nation for vulnerability to SIDSthat is based on the behavior of thebaby and the developmental courseof infantile behavior. This psycho-biological hypothesis can accountfor the fact that about 85% of SIDSdeaths occur between 2 and 5months of age. I return to this hy-pothesis after discussing the back-to-sleep movement, which pro-vides context for my proposal.

THE BACK-TO-SLEEP MOVEMENT

Many hypotheses as to the ori-gin of SIDS have emerged in recentyears, and some studies have docu-mented lifestyle conditions, such as

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smoking, bed sharing, and alcoholingestion, that are correlated withheightened risk of crib death.However, no specific hypothesishas yet earned empirical support.Moreover, no one has offered a hy-pothesis taking into considerationboth babies’ developmental stagesand environmental events imping-ing on babies in the early monthsof life, along with the apparent suc-

cess of a recent effort to reduce theSIDS rate through a behavioralchange—the back-to-sleep move-ment.

A 1992 recommendation by theAmerican Academy of Pediatricsand a 1994 campaign initiated bythe U.S. Public Health Service anda consortium of organizations sug-gested a simple change in parentaland caretaker behavior—placing

babies on their backs for sleeping(Task Force, 2000). This changemay already have had a marked ef-fect on the occurrence of crib death;in the 8 years following the 1992recommendation, SIDS declined tohalf its previous rate (see Fig. 1).

Back sleeping might have ad-dressed a multiplicity of causes ofSIDS. Any conditions, such as ma-ternal smoking or prematurity,

Fig. 1. The incidence of sudden infant death syndrome (SIDS) in the United States from 1988 through2000. Note that Black and Native American babies are at greater risk than White or Hispanic babies, evenas the incidence of SIDS has been reduced by half. The arrows indicate when the American Academy ofPediatrics (AAP) recommended placing babies on their back for sleeping and when the back-to-sleepcampaign was begun by the U.S. Public Health Service.

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CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE 167

which might compromise defen-sive responses to inadvertentsmothering, could be well servedby protection of the respiratorypassages from blockage. Still, thedata constitute at least tentativecorroboration of the usefulness ofthis behavioral intervention.

The question remains as to howthe back-to-sleep movement mayhave reduced the crib-death rate. Ipropose that back sleeping sparesthose infants who have a behav-ioral insufficiency that might causethem to succumb to accidentalsmothering (Lipsitt, 1976; Swift &Emery, 1973) when placed to sleepon their abdomen. In the next sec-t ion , I d i scuss the processesthrough which the initial reflexesof the newborn are eventually sup-planted by learned behaviors, andthe hazard that may be associatedwith the transitional phase forsome infants.

A VIABLE NEUROBIOLOGICAL

HYPOTHESIS

Epidemiological and actuarialdata indicate that there are someconditions that might predispose achild to SIDS (e.g., Protestos, Car-penter, McWeeny, & Emery, 1973;Scragg et al., 1993). Babies who areborn to young mothers who smokeor to mothers who receive inade-quate or late prenatal care are atspecial risk for SIDS, as are babiesborn under compromising condi-tions, such as with the umbilicalcord around the neck. In theUnited States, SIDS babies are dis-proportionately Black, of low so-cioeconomic level, male, and pre-mature. What might explain theserisk factors? Perhaps the answerlies in the reflexes with which hu-man infants are born. Babies varyin the intensity and threshold forelicitation of these reflexes (Brazel-ton, 1973; McGraw, 1943), and

these differences could help ex-plain vulnerability to SIDS. I pro-pose that the factors just men-tioned contribute to later risk ofcrib death because they tend tolower reflex strength and ease ofelicitation soon after birth. That is,initial nonfatal risks may nonethe-less contribute to greater risk forSIDS at a later age. This is becausein the orderly developmentalcourse of neuromotor capacity(McGraw, 1943), the reflexive re-sponses sufficient to protect thebaby early in life inevitably waneas the nervous system develops,and are supplanted by learned re-sponses. During this transitionalperiod when brain and behaviorare developing, newborns withweak defensive reflexes are ingreater jeopardy than are new-borns with stronger reflexes, be-cause learning depends on earlierreflexes of some minimal strength;that is, the behavioral responsesembodied in reflexes form the basisfor later learned behavior.

More than 60 years ago, beforeSIDS had been identified, the emi-nent psychobiologist and develop-mental researcher Myrtle McGrawnoted behavioral transitions thatshe believed were related to impor-tant changes in brain structure andfunction during the first year oflife. Noting that there are gross dif-ferences between the cerebral cor-tex of the human brain (the outerlayer of gray matter) and the sub-cortical brain structures, she docu-mented carefully the developmen-tal progress of infantile reflexes,especially evident in the firstweeks of life, and presumed theywere under the control of subcorti-cal structures. She showed empiri-cally that these reflexes, such as thegrasping, stepping, and swimmingreflexes, gradually wane in strength.

During those first few weeks oflife, the reflexes that were initiallyobligatory in execution becomeslower, more deliberative, andseemingly voluntary. McGraw la-

beled the first, reflexive systemsType A behavior and the eventu-ally achieved deliberate type of re-sponse Type C. McGraw consid-ered Type A behav ior to bemediated principally by the brainstem (lower brain structures) andType C to be mediated by the cere-bral cortex as myelin tissue (sheath-ing around the nerves) matured andconnections among neurons prolif-erated. McGraw noted a third typeof response, which she called TypeB, because it came between TypesA and C chronologically. Type Bresponses represented what sheobserved to be curiously disorga-nized and confused behavior, whichshe regarded as indicative of twoconflicting psychobiological pro-cesses, the Type A process thatcame before and the Type C pat-tern that followed. (As an example,the developmental changes in theswimming reflex are depictedschematically in Figs. 2 and 3).When asked to elaborate on thestate of the baby during this inter-mediary period, she replied that atthis stage, “the baby doesn’t knowwhether he is supposed to be a re-flexive creature or a learned organ-ism” (personal communication,May 25, 1979).

Of special note is that the onsetand peak of McGraw’s intermedi-ate period of confusion occurlargely during the 2- to 5-monthage period. The peak of confusionfor most reflexes McGraw studiedwas around 130 to 150 days of age,approximating the period duringwhich most crib deaths occur. I be-lieve that an aberration in the tran-sitional period of the respiratoryocclusion reflex (or respiratory de-fense response) may contribute tothe risk of crib death.

The respiratory defense re-sponse involves the baby reactingto any covering of its nostrils andmouth. This reflex can be assessedin the first days of life and appearsin standardized scales of infant be-havior (e.g., Anderson & Rosen-

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blith, 1971; Brazelton, 1973). It wasdescribed in detail by Gunther(1961; see also Swift & Emery, 1973,and Anderson & Rosenblith, 1971)as a “fixed action pattern” (i.e., achain of responses that occurs in agenerally fixed order) in which theinfant shakes its head from side toside, pulls i ts head back, andbrings its hands up to the facewhen its respiration is compro-mised (this can happen duringbreast-feeding). Facial vasodila-tion (blushing, an emotional re-sponse) occurs if none of theseprior responses succeeds in freeingthe respiratory passages. The endpoint of the response pattern is cry-ing, with a thrust of the offendingobject away from the baby’s face,whereupon a great sigh of relieffrequently occurs. This reactionsuggests that a learning process isunder way, with the final fail-safelink in the fixed reaction patternbeing highly reinforcing. Gunther,in fact, noted that normal babies of-ten show signs of learning to avoidocclusion after just one or two ex-periences.

The respiratory occlusion re-sponse does seem to be related tothe risk of crib death. The normalnewborn, when placed face downon a surface, is usually capable oflifting its head and turning to oneor the other side, freeing the face ofocclusion. However, Anderson andRosenblith (1971) found that new-borns with a weak respiratory oc-clusion reflex are more likely tosuccumb to SIDS later in the firstyear of life than are babies whomanifest vigorous thwarting of oc-clusion as newborns.

In a study of infants’ responsesto nasal occlusion in which largenumbers of newborns and 6-week-old infants were compared, Swiftand Emery (1973, p. 950) foundthat 44% of the older infants butonly 17% of the newborns “werewholly or partially unable to estab-lish an oral airway within 25 sec-onds.” Thus, the newborns had astronger response to respiratoryocclusion than the older infantsdid. Evidence from this study, car-ried out by pathologists, is consis-tent with the hypothesis that the

respiratory defense reflex protectsbabies from SIDS in the first 2months of life, and that the gradualdiminution of reflex strength in-creases vulnerability over the ensu-ing few months. Infants’ responseswere measured with a scale thatincluded behaviors critical for self-protection, such as “signs of protestbuild-up,” “avoidance reactions,”“crying persists,” and “no struggleor cry.” Another team of patholo-gists, Naeye, Messmer, Specht, andMerrit (1976), were among the firstto call attention to “temperamen-tal” characteristics as relevant tocrib death. They found that whenparents compared a survivingchild with a SIDS sibling, the crib-death child was reported to bemore easygoing, less fussy, andquieter than their surviving sib-lings; these characteristics might beindicative of underresponsivenessor a lack of strong defensive behav-iors.

Recent ly , L i jowska , Reed ,Mertins Chiondi, and Thach (1997)studied the behavior of infants 2 to26 weeks old when subjected to re-

Fig. 2. McGraw’s (1943) schematic of the developmental change in the swimming reflex from reflexive (A), to “disorganized” (B),to “voluntary, deliberate” (C). The illustration shows three patterns of behavior seen when an infant in a prone position is placedin water while being supported. From The Neuromuscular Maturation of the Human Infant, by M.B. McGraw. Copyright 1943 by Co-lumbia University Press. Reprinted with permission of the publisher.

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CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE 169

spiratory compromises. Theyfound four highly stereotyped be-haviors: sighs, startles, limb thrash-ing, and full arousal (eyes openand crying). These behaviors, in-dicative of strong defensive re-sponding to respiratory challenges,seem comparable to Gunther’s(1961) description of infants’ defen-sive fixed actions when regainingrespiratory control over threatenedocclusion. Lijowska et al. reporteda stereotypic sequence analogousto Gunther’s and observed that thebehavior was “variably effective inremoving the bedding covering the

airway” (p. 226). This was a re-markable demonstration (from thelaboratory of research pediatricianThach) of the variable effectivenessof coping behaviors for retrievingsufficient levels of fresh air follow-ing periods of oxygen deprivation.

I am proposing, then, that (a)strong reflexive behaviors that pro-tect the infant from respiratory oc-clusion during the first months oflife are gradually replaced bylearned, deliberate responses and(b) if these reflexive behaviorswane too quickly, before learnedbehavior is sufficient, or if they are

not strong enough to enable ade-quate learning, the infant is in jeop-ardy. Thus, a biobehavioral theorybased on McGraw’s developmentalprogression suggests that infantswith reflex insufficiency are vul-nerable to crib death during the pe-riod between 2 and 5 months be-cause of deficits in learned, adaptive,life-saving responses (Lipsitt, 1976,1979).

CONCLUSIONS AND IMPLICATIONS

The new cautions that babiesshould be placed on their backs forsleeping, along with the data (seeFig. 1) suggesting that back sleep-ing has reduced the SIDS rate byabout 50%, support the contentionthat behavioral factors are relevantto an understanding of crib death.

A fair assessment of our state ofknowledge concerning the causesof SIDS must include the caveatthat it is still a mystery. Nonethe-less, the back-to-sleep movement,formally introduced in 1992 by pe-diatricians and reinforced by agovernmental consensus state-ment in 1994, was followed by asignificant decline in diagnosedSIDS cases, and this apparent suc-cess supports the supposition thatrespiratory occlusion plays a rolein SIDS. SIDS appears to be due tosuffocation that occurs when somebabies lying prone fail to lift theirheads and free their mouths andnostrils during a respiratory chal-lenge. Some infants are more agilethan others in responding defen-sively to smothering stimulation,and even those with fairly weak re-flexes are generally able in the first2 months to maneuver into a safeposition when respiration is threat-ened. However, I suggest that in-fants with especially weak reflexesor high thresholds for eliciting therespiratory defense response are inextra jeopardy when threatened

Fig. 3. The developmental course of swimming behavior (McGraw, 1943). The fre-quency of the three types of response changes with the age of the child. The reflexive“obligatory” behavior is most frequent at birth and wanes over time, to be sup-planted eventually by learned, voluntary responses. During the transitional period,“confused” behavior is manifested; this disorganized behavior reaches a peakaround 2 to 5 months of age, when most crib deaths occur. From The NeuromuscularMaturation of the Human Infant, by M.B. McGraw. Copyright 1943 by Columbia Uni-versity Press. Reprinted with permission of the publisher.

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with smothering during the periodwhen reflexes wane and corticallymediated learned responses musttake their place. If the transitionfrom predominantly reflexive tolearned behavior does not takeplace seamlessly, because of aweak or rapidly waning respira-tory defense reflex, the child of 2 to5 months will be at greater risk forSIDS.

There seems a good basis forcontinuing to caution caretakers toplace infants on their back durings leep. There may be an evengreater urgency to provide babieswith ample exercise in the proneposition while they are awake andtheir caretakers are present, so thatthe infants may practice maneu-vers important to keeping respira-tion clear of obstruction. An argu-ment may also be made that infantsshould be given deliberate practicein resisting respiratory occlusion sothat during the transition when therespiratory defense reflex wanes,they are more likely to engage inbehaviors aimed at removing theoffending object.

An enhanced program of gov-ernmentally sponsored research onthe reflexive behavior of infants inthe early months of life should bemounted, with special focus on thetransitional stage marked by the2- to 5-month critical period associ-ated with crib death. Studies oflearned reactions in the first 6

months of life, the neuromuscularmaturation of the infant, and envi-ronmental hazards that may con-tribute to inadequate responsive-ness by the baby must be carriedout using research designs that ac-knowledge interacting conditionsrather than single antecedents ascausing the tragic deaths of thou-sands of infants.

Recommended Reading

Firstman, R., & Talan, J. (1997). (SeeReferences)

Naeye, R. (1980). Sudden infant death.Scientific American, 242, 52–56.

Swift, P.G.F., & Emery, J.L. (1973).(See References)

Acknowledgments—I thank Matthew S.Goodwin for helping with the figures,and Marian Willinger of the National In-stitute of Child Health and Human De-velopment for providing recent data onSIDS rates.

Note

1. Address correspondence to LewisP. Lipsitt, Department of Psychology,Brown University, Providence, RI02912; e-mail: lewis_lipsitt@brown.edu.

References

Anderson, R.B., & Rosenblith, J.F. (1971). Suddenunexpected death syndrome: Early indicators.Biologia Neonatorum, 18, 395–406.

Brazelton, T.B. (1973). Neonatal Behavior AssessmentScale. Philadelphia: Lippincott.

Firstman, R., & Talan, J. (1997). The death of inno-cents: A true story of murder, medicine, and high-stakes science. New York: Bantam.

Gunther, M. (1961). Infant behavior at the breast.In B. Foss (Ed.), Determinants of infant behavior(pp. 37–44). London: Methuen.

Hunt, C.E. (2001). Sudden infant death syndromeand other causes of infant mortality: Diagno-sis, mechanisms, and risk for recurrence of sib-lings. American Journal of Respiratory andCritical Care in Medicine, 164, 346–357.

Lijowska, A.S., Reed, N.W., Mertins Chiondi, B.A.,& Thach, B.T. (1997). Sequential arousal andairway-defensive behavior of infants in as-phyxial sleep environments. Journal of AppliedPhysiology, 83, 219–228.

Lipsitt, L.P. (1976). Developmental psychobiologycomes of age. In L.P. Lipsitt (Ed.), Developmen-tal psychobiology: The significance of infancy (pp.109–127). Mahwah, NJ: Erlbaum.

Lipsitt, L.P. (1979). Critical conditions in infancy:A psychological inquiry. American Psychologist,34, 973–980.

McGraw, M.B. (1943). The neuromuscular matura-tion of the human infant. New York: ColumbiaUniversity Press.

Naeye, R., Messmer, J., III, Specht, T., & Merrit, F.(1976). Sudden infant death temperament syn-drome before death. Journal of Pediatrics, 88,511–515.

Protestos, C., Carpenter, R., McWeeny, P., & Em-ery, J. (1973). Obstetric and perinatal historiesof children who died unexpectedly (cot death).Archives of Disease in Childhood, 48, 835–841.

Raring, R.A. (1975). Crib death: Scourge of infants—shame of society. Hicksville, NY: ExpositionPress.

Scragg, R.K.R., Mitchell, E.A., Taylor, B.J., Stewart,A.W., Ford, R.P.K., Thompson, J.M.D., Allen,E.M., & Becroft, D.M.O. (1993). Bed sharing,smoking, and alcohol in the sudden infantdeath syndrome. British Medical Journal, 307,1312–1318.

Swift, P.G.F., & Emery, J.L. (1973). Clinical obser-vations on response to nasal occlusion in in-fancy. Archives of Disease in Childhood, 48, 947–951.

Task Force on Infant Sleep Position and SuddenInfant Death. (2000). Report at year 2000. Pedi-atrics: American Academy of Pediatrics, 105, 650–656.