EVOLUTION AND SUDDEN INFANT DEATH SYNDROME (SIDS) Part 2: Infant Responsivity to Parental Contact

James J. McKenna Pomona College

This paper and its subsequent parts (Part II and Part III) build on an earlier publication (McKenna 1986). They suggest that important clinical data on the relationship between infantile constitutional deficits and microenvironmental factors relevant to SIDS can be acquired by examining the physiological regulatory effects (well documented among nonhuman primates) that parents assert on their infants when they sleep together. I attempt to show why access to parental sensory cues (movement, touch, smell, sound) that induce arousals in infants while they sleep could possibly help one of many different subclasses of infants either to override certain kinds of sleep-induced breathing control errors suspected to be involved in SIDS or to avoid them altogether. I do not suggest that solitary nocturnal sleep "causes" SIDS, that all parents should sleep with their infants, or that traditional SIDS research strategies should be abandoned. However, using evolutionary data, I do suggest that an adaptive fit exists between parent-infant sleep contact and the natural physiological vulnerabilities of the neurologically immature human infant, whose breathing system is more complex than that of other mammals owing to its speech-breathing abilities. This "fit" is best understood, it is argued, in terms of the 4-5 million years of human evolution in which parent-infant contact was almost certainly continuous during at least the first year of an

Received July 17, 1989; accepted September 11, 1989. Address all correspondence to James J. McKenna, Department of Sociology and Anthropology, Pomona College, Claremont, CA 91711.

Copyright 9 1990 by Walter de Gruyter, Inc. New York Human Nature, Vol. 1, No. 2, pp. 145-177. 145

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infant's life. Thus, to dismiss the idea that solitary sleep has no physiological consequences for infants does not accord with scientific facts. KEY W O R D S :

Sudden Infant Death Syndrome (SIDS); Human evolution; Parent-infant contact; Sensory cues; Microenvironment

OVERVIEW

[SIDS is] a sudden death of any infant or young child which is unexpected by history and in whom a thorough postmortem examinationfails to demonstrate an adequate cause for death. (Bergrnanet al. 1970:18) In the second half of the twentieth century perhaps no infant malady remains as stubbornly resistant to the challenges of so m a n y scientific disciplines as sudden infant death syndrome (SIDS). In the words of one investigator, "The shock, trauma, and bewilderment of parents whose infants die of SIDS are matched only by the confusing number of hypotheses, postulated causes, feelings of consternation and puzzlement by pediatricians and others who have attempted to explain SIDS" (Call 1986:56). And, of course, "Few killers strike with the unexpectedness and cruelty to both victim and family" as does this syndrome (Laitman 1986:65). SIDS claims the lives of approximately 2 of 1000 infants annually in the United States alone (Hoffman et al., 1988); it remains the leading cause of nonaccidental death for infants between the ages of 1 month and 1 year. It is the most age-constricted of all infant maladies k n o w n - - m o s t deaths occur when the child is between 2 and 4 months old. Although general perinatal mortality rates for infants 0-6 days old have decreased significantly, SIDS rates remain relatively stable (Bryan 1984; Kraus 1984; Peterson 1983; Peterson et al. 1988; Tildon et al. 1983). More than 25 years of persistent, rigorous, and interdisciplinary research involving scientists from all over the world supported by millions of dollars of biomedical research grants have failed to discover "one positive criterion that can be employed by the clinician to identify the future victim," or even "one positive criterion that the pathologist can use to recognize the subject at autopsy" (Valdes-Dapena 1980b; also see Bass et al. 1986). Although the causes of SIDS remain a mystery, and a single common pathway leading to SIDS has yet to be identified (Hodgman and Hoppenbrouwers 1988), the collective body of research conducted during the past 25 years has led to an evolution of an understanding (Valdes-Dapena 1980b). For example, it is now believed by some SIDS researchers that the structural-functional defects involved may be quite subtle (Haddad and Mellins 1983) and that infants who eventually succumb to SIDS develop

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differences from healthy infants during intrauterine life (Hoffman et al. 1988; Valdes-Dapena 1980b, 1988). Apparently, SIDS victims are not as "healthy" before death as both physicians and parents once presumed. The most recent epidemiological evidence suggests that infants b e t w e e n 1 and 5 months of age, born to poor, unmarried w o m e n under 20 years of age w h o smoked during their pregnancies, are at the greatest risk of dying from SIDS (Hoffman et al. 1988; also see Taylor and Emery 1988). That SIDS victims represent an extremely heterogeneous population is consistently confirmed by epidemiological studies (Bergman 1986; Hoffman et al. 1988; Peterson 1983; Valdes-Dapena 1980a, 1980b). For example, SIDS occurs within all industrial cultures studied (though rates vary significantly--see below); among all races studied; at all times of the day; among infants with diverse clinical histories; among the rich and the poor; during every season (but especially in winter); while infants are in contact with and out of sight of the caregiver; while infants are in cribs, in their parents' bed, in car seats, in strollers, and/or in shopping carts (see McKenna 1986 for review). So diverse is the SIDS population and the circumstances within which infants die, Schwartz and Segantini argue, "It is important that the idea of the multifactorial origin of SIDS with all its implications be accepted by investigators. One critical implication is the fact that SIDS will never completely be eliminated because it will be impossible to deal with all the potential causes" (Schwartz and Segantini 1988:218). Bergman, w h o has spent the majority of his medical career searching for clues to the SIDS conundrum and fighting political battles on behalf of SIDS victims and their families, sums up and underscores the interplay of factors involved. He states, "SIDS is like a nuclear explosion where a critical mass must be attained before the event is to occur" (Bergman 1986:17). SIDS researchers are not sanguine about the prospects of understanding for all victims how and w h y constitutional factors coalesce or converge with environmental ones at a particularly "vulnerable" time in an infant's life (Barnett 1980) to produce this "critical mass"; still, this sobering appraisal leaves room for optimism. If there is no "typical" SIDS victim and if SIDS victims differ from one another and from healthy surviving infants in some degree rather than in kind, it stands to reason that by improving the conditions within which infants develop prenatally, as well as improving the socioenvironmental conditions within which infants are nurtured and cared for postnatally, survival chances for some potential victims should be increased (see Emery 1983). This proposition is supported not only by the heterogeneity of the SIDS population, but also by the fact that SIDS rates generally parallel changes in infant mortality; that is, as infant mortality decreases, so does the number of SIDS cases per 1000 live births, although it is not k n o w n

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specifically w h y (Bergman 1986; H o d g m a n and H o p p e n b r o u w e r s 1988). The most recent and most comprehensive epidemiological study (the NICHD SIDS Cooperative Epidemiological Study) found that "medical risk factors (of the mother) were not as high as the social, behavioral, and demographic risk factors enumerated in the maternal interview" (Hoffman et al. 1988:18). Insofar as these and other epidemiological studies suggest that access to prenatal care, maternal education, maternal age at first birth, marital status, breast-feeding, and general socioeconomic status affect the infant's risk of dying from SIDS (at least for some of many different subclasses of SIDS victims), it seems important to examine specifically h o w or what kinds of prenatal factors may conspire with infantile deficits and w h y they do so to increase or decrease SIDS risk (Lipsitt 1981). This paper and those to be published in this and a subsequent issue reiterate, update, and expand the biosocial SIDS research model I proposed a few years ago (McKenna 1986). It was argued that parental breathing constituted one set of several related factors in the infant's sleeping environment that possibly could assist sleeping infants to weather the critical developmental respiratory control shift that occurs especially between 2 to 4 months of age, when human infants are at the greatest risk of dying from SIDS. The related hypotheses put forth suggested that solitary sleeping environments deprive infants of sensory cues more important to some infants than to others, perhaps making it easier for the "critical mass" of which Bergman speaks to be achieved, and making it possible for the SIDS deficit to be expressed in a fatal form. Because of additional work that has been done since the publication of that paper, I would like to restate the case in Parts I and II and in a following paper (Part III) integrate the perspective with the most significant recent work on SIDS and with some preliminary work of my o w n on the sleep and breathing patterns of infants sleeping with their mothers. These papers do not propose any new "causes" of SIDS, nor are they meant to suggest that if parents slept with their infants, SIDS would be eliminated. Research strategies require underlying theoretical justifications before they can be taken seriously, however, especially if these strategies differ from ones that are traditionally employed. The data used here indicate strongly that infantile constitutional factors interact with microenvironmental factors in nontrivial ways and that cosleeping parents assert potentially protective physiological regulatory effects on their infants. Specifically, because it induces infant arousals, the sensory communication involving tactile, vestibular (rocking), auditory (vesicular sounds), temperature, and CO2 sensory exchanges that continuously occurs between co-sleeping pairs should help to reduce the number of what some researchers have called adaptive failures, in-

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duced during the development of breathing, sleep, and arousal mechanisms by any number of infantile central nervous system (CNS) deficits. At very least, it is shown w h y we should expect that a solitary sleeping infant faces a set of environmental or experiential circumstances extraordinarily different from a co-sleeping infant, which may not be in its biological best interest. To accomplish this task, anthropological data (cross-cultural, crossspecies, paleoanthropological) are integrated with experimental, clinical, and epidemiological research bearing on the evolution of h u m a n infant development. This integration forces us to depart from the traditional SIDS research paradigm, which assumes the primacy of deficient internal control mechanisms in the infant that in an as-yet-unknown w a y create the conditions most conducive to respiratory-cardiac collapse. The relative neurological immaturity of the human neonate-infant and its unique developmental trajectory, including its prolonged and intense dependent status on the caregiver at the time of its death from SIDS, are considered vital analytic parameters in understanding from this evolutionary perspective how some infants' physiological systems go awry. Finally, human infants are conceptualized here not in terms of h o w industrialized and urban cultural ideologies define them biologically or socially; rather, in this analysis of SIDS the infant is accorded its evolutionary past and is conceptualized as an organism w h o s e social and physiological needs are inseparable, having been designed over 3 - 5 million years in caregiving environments within which prolonged parental contact (one form of which is co-sleeping) regularly and predictably occurred (McKenna 1986). The infants' physiological systems, including sleep, arousal, and breathing, are viewed as being much more biologically conservative and much less able to change than are the caregiving styles of their parents, w h o define and respond to infant needs according to prevailing cultural ideologies. That is, in accordance with cross-species and recent developmental studies of infants, the infant is seen to be adapted to physiological regulation by, and responsivity to, a caregiver and is seen as being far less physiologically autonomous during the first 6 months of life than we in this culture, including SIDS researchers, have come to presume (see Bowlby 1969; Isaac 1978; Konner 1981; Lancaster and Lancaster 1982). PARENT-INFANT PHYSIOLOGICAL REGULATORY EFFECTS: EVIDENCE OF SENSORY EXCHANGES Table 1 summarizes a variety of current research on the diverse ways parents and infants affect each other physiologically, socially, and psy-

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Table 1. Synthesis of Research on the Effects of Parent-Infant Contact and Separation

Primary reference

Secondaryreference

Ainsfield and Lipper 1983

Trevathan 1 9 8 7

Ainsworth et al. 1978

Reite 1984

Arnon 1 9 8 3

McKenna 1986

Barnett et al. 1970; Elmer and Gregg 1967; Klein and Stern 1971; Sarnoroff and Chandler 1975 Blakemore and Cooper 1970

Trevathan 1987

Bowlby 1953, 1960; Robertson 1953

Reite 1984

Bowlby 1958

Trevathan 1987

Trevathan 1987

Main effect

Description

Increased Uninterrupted contact affectionate for first hour after behavior birth caused mothers to behave more affectionately toward their infants Anxious vs "Anxiously attached" secure infants tended to attachment have mothers who demonstrated aversion to close body contact Protection Mother's milk contains against a maternal antibody, bacteria which destroys the vegetative cells of bacteria that can kill the infant Child Extensive postpartum abuse separation can result in poor or abusive care-taking

Development Development of visual of visual acuity is directly acuity related to postpartum stimulation Anaclitic Mother-infant depression separation results in anaclitic depression in humans Adaptive Clinging, crying, smilsignificance; ing, following, and infant sucking are adaptive survival and have evolutionary significance

Evolution and Sudden Infant Death Table 1.

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Continued

Primary reference

Secondaryreference Main effect

Bowlby 1969

Trevathan 1987

Bradford 1 9 7 5

McKenna 1 9 8 6

Brody 1 9 8 1

Trevathan 1987

Coe and Levine 1981

McKenna 1 9 8 6

Increase in hormonal levels

Coe et al. 1 9 8 5

McKenna 1 9 8 6

Decrease in antibodies

Coombs and McLaughlin 1986

McKenna 1986

Prevention from allergic reactions

Description

Attachment

Attachment of infants through the five primary behaviors are part of the "environment of evolutionary adaptedness" that ensures survival Breathing Infants display acute sensitivity to decibel ranges equivalent to human breathing sounds (15-30 dB) and respond by breathing MotherThe "'simple infant pleasures" of the interaction postpartum period motivate the mother and infant to continue interacting Infant squirrel monkeys show an increase in adrenal (stress) secretions and plasma cortisol levels when separated from mothers Infant squirrel monkeys show a lower level of antibodies when separated from mothers Breast-feeding lowers chance of death from allergic reactions to cow's milk

(continued)

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Table 1. Synthesis of Research on the Effects of Parent-Infant Contact and Separation (Continued)

Primary reference Secondaryreference

Main effect

Description

Crook 1 9 7 9

Trevatban 1 9 8 7

Perceptual, emotional, and social development

Patterns of breast-feeding and food acquisition ultimately function in infant's perceptual, emotional, and social development

DeChateau 1976

Trevathan 1 9 8 7

Decrease in crying, increase in smiling

Infants cried less and smiled more when allowed an extra half-hour of skin-to-skin contact immediately after birth

Detterman 1978

Trevathan 1 9 8 7

Pacification

Mother's heartbeat pacified infants in the short term

Dollard and Miller 1950; cited in Bowlby 1969

Trevathan t987

Increased Nursing socializes companioninfants to "like to be ability with others"

Fardig 1 9 8 0

McKenna 1 9 8 6

Decrease in Infants do not temperature maintain skin and core temperatures when removed from skin-to-skin contact even if ambient temperatures are equal; possible link with increase in stress hormones owing to separation

Fleming 1 9 8 4

McKenna 1986

Shift of control for breathing

External sensory cues may be most useful to infants during neurological shifts of control for breathing

Evolution and Sudden Infant Death Table 1.

153

(Continued)

Primary reference Secondary reference Main effect

Description

Gunnar et al. 1981

Reite 1984

Protest, Postpartum separation agitation, of pigtail monkeys and can result in protest, physiological agitation, and changes physiological changes, such as increased heart rate and serum cortisol levels Bonding Physical contact is central to the bond between mother and infant primates

Harlow 1962

Reite 1984

Harlow and Harlow 1965

Trevathan 1 9 8 7

Attachment

Food is less important than "contact comfort" in attachment

Hofer 1 9 8 1

McKenna 1986

Lack of growth

Hofer 1 9 8 3 ; Schwartz and Rosenblum 1985

McKenna 1 9 8 6

Physiological effects

Mother's presence is necessary for the release of growth hormones in rat pups Touching causes short-term physiological effects

Kattwinkel 1977

McKenna 1 9 8 6

Decrease in apneas

Rubbing an infant's feet decreases the duration and frequency of apneas

Klaus and Kennell 1976

Trevathan 1 9 8 7

Synchrony of biorhythms

Infants develop an interactive synchrony conforming to the mother's biorhythms

Klaus and Kennell 1982

Trevathan 1 9 8 7

Bonding

Reciprocal interaction between mothers and infants "locks" them together

in utero

(continued)

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Table 1. Synthesis of Research on the Effects of Parent-Infant Contact and Separation (Continued)

Primary reference Secondary reference

Main effect

Description

Kontos 1 9 7 8

Trevathan 1 9 8 7

Decrease in crying, increase in smiling

Extra skin-to-skin contact immediately following birth decreased crying and increased smiling in infants; behaviors persisted over time

Korner 1 9 8 1

McKenna 1 9 8 6

Breathing patterns

Vestibular movement (rocking), such as parent's chest movement, affects infant's breathing patterns, especially during sleep

Kuhn et al. 1978

Trevathan 1987

Lack of growth

Rats removed from their mothers show a significant decline in the production of ODC despite the fact that pups were warm and well-fed

Laudenslager et al. 1982; Reite et al. 1981

McKenna 1 9 8 6 ; Reite 1 9 8 4

Reduced Mother-infant physiological separation decreases immunological responses functioning and autonomic physiological responses

Le Vine 1977

Trevathan 1987

Attachment Socialization of children achieved and socialization through Bowlby's (1969) processes of attachment

Lipsitt 1 9 8 1

McKenna 1 9 8 6

Breathing

Some infants require help in learning how to "defend" respiratory passages

Evolution and Sudden Infant Death Table 1.

155

(Continued)

Primary reference Secondary reference Main effect

Description

MacFarlane 1977

Trevathan 1987

Sleep patterns

Infant coincides with mother's sleep patterns in utero

Maloney 1949; cited in McBryde 1951

Trevathan 1987

Nutritional Infant gets improved and care when "rooming psychological in" with parents; benefits first step in close family relationship; infant thrives nutritionally and psychologically

Masi 1979

McKenna 1986

Sensorirnotor functioning

Vestibular stimulation improved sensorimotor functioning

McGinty and Hoppenbrouwers 1983

McKenna 1986

Augmented neuronal firing

Vestibular stimulation augments reticularformation neuronal firing "in parallel" with responsive behavior in some mammals

Mead 1 9 5 6

Trevathan 1987

Cultural adaptation

Rhythmic interaction, such as entrainment, between the mother and infant prepares infants for cultural adaptations

Montagu 1964

Trevathan 1987

Increased heartbeat and movement

Fetal heartbeat and movement increase in response to sounds

Montagu 1 9 7 1

Trevathan 1987

Exterogestation

Psychological and emotional factors affect development after birth for several months

(continued)

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Table 1. Synthesis of Research on the Effects of Parent-Infant Contact and Separation (Continued)

Primary reference Secondary reference

Main effect

Description

Growth

Tactile stimulation is important for humans and nonhumans for both physiological and psychological growth

Physiological functioning

Most mammals would die from failures of the genitourinary or gastrointestinal systems if they were not licked following birth

Newman 1 9 7 5

Trevathan 1987

Identification

Vocalization and auditory communication identify infant as an individual, then as part of a group

Patrick et al. 1980

McKenna 1 9 8 6

Breathing rhythm

Fetus's circadian breathing rhythm tied to that of the mother

Powell et al. 1967; Reite and Capitanio 1985

McKenna 1 9 8 6

Failure to thrive

Hofer's (1981) connection of mother's presence and the release of growth hormones could relate to "failure to thrive" syndrome

Prescott 1970a, 1970b

McKenna 1986

SocioIn the long run, touch emotional may be crucial to development healthy socioemotional development, such as decreasing aggressive behavior

Evolution and Sudden Infant Death Table 1.

157

(Continued)

Primary reference Secondary reference Main effect

Description

Reite and Short 1983

Disturbed sleep patterns

Mother-infant separation results in agitation followed by disturbed sleep patterns

Protestdespair, agitationdepression

Mother-infant separation in both monkeys and humans results in protest-despair and agitation-depression behaviors On separation from mothers, pigtail monkeys demonstrated agitation followed by depression and decreasing heart rate and body temperature Mother's sleep cycles affected circadian rhythms of offspring in rat pups Children who had extensive contact with mothers immediately after birth had higher IQ and language test scores Crying and clinging increase survival by maintaining proximity, but visual following, smiling, and facial expressions increase the quality of that survival through sensory and cognitive development

Reite 1984

Reite et al. 1978

McKenna 1986; Reite 1984

Agitation and depression

Reppert and Schwartz 1983

McKenna 1986

Circadian rhythms

Ringler et al. 1976

Trevathan 1987

Increased test scores

Rivinus and Katz 1971

Trevathan 1987

Increased survival and survival value

(continued)

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Table 1. Synthesis of Research on the Effects of Parent-Infant Contact and Separation (Continued)

Primary reference Secondaryreference

Main effect

Description

Robson 1 9 6 7

Trevathan 1 9 8 7

Attachment

Increased eye contact improves quality of attachment

Salk 1 9 6 0

Trevathan 1 9 8 7

Soothing, growth

Mother's heartbeat soothes infant and produces greater weight gain in early infancy

Salk 1 9 6 1 , 1962; Salk et al. 1974

McKenna 1 9 8 6

Reduction of anxiety

Mother's heartbeat is "imprinted" during gestation; carrying infant on left side reduces infant anxiety

Seiler et al. 1979

McKenna 1 9 8 6 ; Reite 1 9 8 4

Cardiac Mother-infant arrhythmias separation resulted in agitation followed by increase in cardiac arrhythmias

Smith and Steinschneider 1975

McKenna 1 9 8 6

Postnatal sleep and arousal behavior

Infants born to mothers with low heart rates slept for longer periods of time, fell asleep faster, and cried less than did infants born to mothers with higher heart rates

Southall et al. 1979

McKenna 1 9 8 6

Resumed breathing

Most infants who experienced apneas resume breathing when touched or picked up

Spencer-Booth and Hinde 1971

Reite 1984

Long-term changes

Long-term effects of early maternal separation are still visible after 2 years, even after reunion

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Table 1. (Continued)

Primary reference

Secondary reference Main effect

Description

Spitz 1946

Retie 1984

Anaclitic depression

Stratton 1983

Trevathan 1 9 8 7

Sucking

Wetland and Serber 1970

Trevathan 1 9 8 7

Anxiety reduction

Anac|itic depression results from motherinfant separation of monkeys Tactile stimulation around mouth elicits sucking Holding infants on left side reduces maternal anxiety, thereby reducing anxiety in infant

chologically. These data provide a general background against which McKenna (1986), Reite (1984), and Trevathan (1987) use evolutionary models to explain aspects of contemporary h u m a n development with important clinical implications. Trevathan (1987) proposes an evolutionary interpretation of human birth and midwifery, Reite (1984) discusses the evolutionary significance of touch (see also Reite and Capitanio 1985), while I describe my perspective on the possible role of parental cues in regulating infant sleep and breathing (McKenna 1986). To appreciate the possible importance of the external sensory stimuli in helping to stabilize the infant's developing breathing patterns, we should remember that perhaps for as many as 3 months before birth, "sensory stimulation alone in the absence of blood gas changes (i.e., oxygen/CO2) regularly initiated rhythmic breathing [amniotic or liquid breathing] in the human fetus" (Jansen and Chernick 1983:466). The data on which this statement is based should force us to consider more carefully both the extent to which sensory stimuli in the infant's microenvironment influence the infant's breathing stability and the circumstances in which, and the extent to which, the infant's respiratory system is protected from environmental disturbances by contact with its caregiver. Of course, at a basic level, the anatomy and physiology of the neonatal respiratory system must be sufficiently developed to permit the infant to breathe on its o w n at birth, or it surely will die. Interestingly, during the first few weeks of life, the full-term newborn seems to have a natural immunity to SIDS, possibly because of a gasping reflex that promotes oxygenation during periods of asphyxia. Soon afterwards,

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however, according to Guntheroth (1977), the infant loses this reflex, becoming more vulnerable to breathing control errors (apneas, or periodic breathing). Galef's (1981) comparative evolutionary perspective on mammalian parent-infant relationships predicts this period of vulnerability, though not necessarily with respect to respiration. He compares mammalian infants (unflattering as it may be) with parasites, who lose some structural and functional integrity once attached to a host. That is, once the human infant begins to engage, or, more appropriately, reengage, with its mother--becoming increasingly d e p e n d e n t on the nature and timing of her care (see Field 1985) while simultaneously losing reflexive behaviors to higher-brain (labile) behaviors as its development proceeds--it also loses some of its structural and physiological integrity. It thus becomes vulnerable to neurological control system errors, especially during these early, critical transitions or developmental shifts. The arguments made in this paper revolve around this viewpoint, espoused by Lipsitt (1981, 1982).

Vestibular Stimulation and Breathing The effects of rhythmic rocking and movement (vestibular stimulation) on the human infant have been recognized since prehistoric times (McKenna 1986), but their precise physiological and social correlates, especially with respect to how they promote breathing, have been delineated only during the past 20 years or so (see Baker and McGinty 1977; Barnard 1981; Chisholm 1983; McGinty and Hoppenbrouwers 1983; for reviews see Korner and Thoman 1972; Ornitz 1983). Gregg et al. (1976) suggest that rocking stimulation may prove to be more helpful than tactile stimulation in soothing and alerting h u m a n infants because of its effect on their reticular activating system. According to studies conducted by McGinty and Hoppenbrouwers (1983) and DonneUy (1984), it is clear that vestibular stimulation directly augments reticularformation neuronal firing "in parallel" with respiratory behavior in many mammalian species, including humans (McGinty and Hoppenbrouwers 1983). McGinty (1984) reports that rapid eye movement (REM) sleep stage was altered and lengthened w h e n kittens were rocked. In another study, McGinty and Hoppenbrouwers (1983) describe kittens whose sleep tended to be synchronized by a rocking stimulus and whose respiration increased w h e n the rocking frequency reached onehalf the baseline frequency of their quiet-sleep respiration rate. In other words, the kittens' breathing was more strongly influenced by an external pacemaker when the rocking movement approximated the breathing rate of an adult cat (an adult breathes much more slowly than a kitten).

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Likewise, it has been demonstrated in h u m a n s that the kind of vestibular movement provided by the parent's chest m o v e m e n t (particularly w h e n the parent and infant sleep together) also can affect the infant's breathing patterns. For example, Korner and colleagues (1978; Korner 1981) describe the positive results of placing apnea-prone premature infants on oscillating waterbeds: w h e n set at a m o v e m e n t of between 12 and 14 oscillations per m i n u t e - - t h e approximate breathing rate of an adult--the rates of apnea per sleep hour in 7 of the 8 infants studied were reduced by 13-48%. Most exciting is Thoman's recent preliminary success in stabilizing the breathing patterns of some high-risk premature infants by placing mechanically breathing teddy bears in their cribs, which provides a constant source of rhythmic vestibular stimulus that closely resembles the parent's chest movement (see Thoman 1986). The discovery that external rhythmic cues (in this case, movement) influence infants' breathing patterns implies that there is continuity in the ways that mothers' biorhythms physiologically regulate their offspring both prenatally and postnatally, a point of view confirmed by recent research on parent-infant regulatory effects among a variety of mammals (see Reite and Field 1985). For example, Korner (1981) suggests that a defective Zeitgeber, or rhythm giver, may well contribute to the disorganization of the premature infant's behavior, including its breathing. This perspective is supported by a great deal of research conducted and discussed by Barnard (1981), Dreyfus-Brisac (1974), and Hofer (1981) and reviewed by Field (1985) and Jansen and Chernick (1983). The fact that vestibular stimulation helps in the development of some fetal and infant systems is not surprising; like the auditory and respiratory nuclei, the vestibular nuclei located on the brain stem develop structurally and functionally very early. For example, the large neurons of the vestibular nuclei are functional at 21 weeks gestation, and by 6 months of age, according to Ornitz (1983), the vestibular system is well advanced. That both prenatal and postnatal vestibular stimuli may help to develop the infant's motor skills has been documented. Masi (1979) found that the vestibular stimulation of premature infants improved their sensorimotor functioning relative to those of unstimulated infants. Chisholm and Heath (1987) explain this finding by reminding us that during at least 3-4 million years of hominid evolution, h u m a n fetuses developed in the context of the vestibular stimulation received as their mothers foraged. Thus, Chisholm and Heath hypothesize, the fetus is preadapted for high levels of postnatal maternal locomotion because humans are a "carrying," as compared to a "caching," species; that is, infants are not kept in nests w h e n their mothers or fathers forage for food but are transported on the parent's chest (see also Lozoff and Breittenham 1978).

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Most interesting is that the h u m a n infant's vestibular system is functioning at its "highest level of reactivity" after the first few months of life (Ornitz 1983:527), the very time w h e n infants are at greatest risk of dying from SIDS. In other words, at the time their respiratory control systems are the most vulnerable, infants may be most sensitive to respiratory augmentation through external vestibular and auditory stimu l i - c u e s regularly available in the infant's expected microenvironment of close parent-infant contact, including co-sleeping. The "'Breathing Teddy Bear": Almost as G o o d as M o m or Dad? Thoman and Graham (1986) investigated the effects of placing a "breathing companion" in an isolette with premature infants "with the objective of facilitating the development of their irregular physiological rhythms" (Thoman 1986:68). This companion was a stuffed teddy bear with a p u m p connected by way of a plastic tube placed within its torso. The bear's "stomach" was made to expand and contract in smooth "sinusoidel motion," simulating the breathing of the infant. The pace of the bear's breathing was matched to one-half of the baby's breathing during its quiet sleep. The hypothesis that the baby's breathing would be entrained to that of the bear, becoming more regular or more stable, was confirmed. Thoman and Graham demonstrated, much like my model predicts, that given the opportunity to do so, a sleeping companion can, in fact, stabilize the breathing pattern of a premature infant (Thoman 1986). Of course, this study proves nothing about a sleeping companion's ability to counteract SIDS, but it does show that at birth infants are indeed prepared or sensitized to breathing movement cues. My contention is that prenatal experiences and evolutionary processes best explain this responsivity. Physiological Changes Induced by Touching Touching also stimulates breathing. I will not review here the extensive literature on the effects of tactile stimulation (see Montagu 1978; Smeriglio 1981; Suomi 1982); suffice it to say that, in the short run, touching has significant physiological effects (see Hofer 1983; Schwartz and Rosenblum 1985), and in the long run it may be crucial to healthy socioemotional development, such as reducing the likelihood of aggressive behavior (Prescott 1970a, 1970b). Specifically with respect to breathing, Kattwinkel (1977) demonstrated that rubbing an infant's feet for about 5 minutes at 15- to 30-minute

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intervals reduced both the duration and the frequency of apneas. And most infants who experience apneas resume breathing w h e n they are touched or picked up, although some infants require more acute therapies (see Southall et al. 1985). Although the longitudinal deprivation studies of nonhuman primates conducted at the University of Wisconsin, beginning with Harlow's (1958) classic surrogate mother studies, clearly document the need for infants to cling to a warm and soft object, to feel "contact comfort," these studies concentrated on the long-term psychosocial effects of loss and not on their short-term physiological effects (see McKenna 1979 for a review). The relative effects of, for example, tactile deprivation vs auditory vs vestibular-specific sensory stimulation loss were not specifically monitored. During the past 15 years or so, however, studies of the physiological correlates of isolation, including the deprivation of tactile contact with other animals (particularly mothers), have revealed dramatic and important findings (Table 2). Studies conducted in the laboratories of Hofer, Reite, and Levine (see Reite and Field 1985) have shown that to understand the consequences for the infant of separation (primarily from the mother), we must know h o w the infant's body changes physiologically after separation, and thus how, through contact, the mother physiologically regulates her infant's temperature, metabolic rate, hormone levels, enzyme production, antibody titer, sleep cycle, heart rate, and respiration to promote her infant's health and survival. Together, these data disclose the overall impact of immediate separation and remind us that when human infants are regularly isolated (e.g., for nocturnal sleep--which can be regarded as an evolutionally novel situation) their physiological systems are probably also affected. For example, Fardig (1980) found that infants placed in radiant-heated cribs could not maintain the mean skin and core temperatures characteristic of h u m a n newborns placed on their mothers' bare chests, even w h e n the ambient temperatures were equivalent. The difference, she suggests, may be the produc~ tion of stress hormones (such as cortisol) produced by the infant w h e n separated from its mother, which causes a drop in its body temperature. Studies using telemetry on a variety of macque monkey species (bonnets, pigtail, and rhesus) indicate that w h e n separated from their mothers, primates as old as 4 - 6 months also lose body temperature and can experience disturbances in sleep, with decreased REM sleep periods (Reite and Short 1978), changes in EEG activity (Short et al. 1977), alterations in cellular immune responses (Reite et al. 1981), and increases in cardiac arrhythmias (Seiler et al. 1979). It has been demonstrated in squirrel monkeys that separation increases their adrenal (stress) secretions and plasma cortisol levels (Coe and Levine 1981) and decreases their ability to combat pathogens because of decreases in immunoglob-

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Table 2. Immediate and Short-Term Physiological Consequences of Parent-Infant Separation in Monkeys and Rats a Physiological consequences of separation

Investigator(s)

Bonnet or pigtail monkeys Initial period Increase in heart rate and body temperature Subsequent period of depressed behavior Decrease in heart rate and body temperature Increase in cardiac arrhythmias Alterations in heart rate, body temperature, and circadian rhythms Disturbances in sleep Increased arousals; increase in REM latency; decrease in time in REM Changes in regulation of EEG activity Alterations in cellular immune response accompanying mother-infant or peer separation

Reite and Snyder 1982 Reite et al. 1978 Seller et al. 1979 Reite et al. 1982 Reite and Short 1978

Short et al. 1977 Reite et al. 1982 Reite et al. 1981 Laudenslager et al. 1982 Other references: McKenna 1979, 1982 Reite and Capitanio 1985 Coe et al. 1985 Hofer 1978, 1981, 1983

Squirrel monkey (Saimiri sciureus) Increase in adrenal secretion and plasma cortisol levels Serum levels of immunoglobulins Decline after 7 days; back to normal in 14 days Complement proteins to cortisol diminish Lower level of antibody production in response to bacteria (Escherichia coli)

Coe and Levine 1981 Coe et al. 1978, 1985 Coe et al. 1985

Coe et al. 1985 Coe et al. 1985

Rats, 2 weeks old Bradycardia Increased sleep latency Augmented sleep Decrease in REM sleep

Hofer 1978, 1981, 1983

Rats, 10 days old 50% reduction in brain and heart enzyme (ornithine decarboxylase) owing to separation-induced suppression of growth hormone ~From McKenna (1986).

Butler et al. 1978 Kuhn et al. 1978

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ulins (after 7 days). Lower levels of antibodies against certain bacteria strains have also been found (Coe et al. 1985). When 2-week-old rat pups were separated from their mothers, they immediately experienced a drop in growth hormone levels concomitant with a corresponding drop in a brain enzyme (ornithine decarboxylase, ODC) needed for the synthesis of several brain proteins (Butler et al. 1978; Kuhn et al. 1978). Apparently, a drop in these two substances was not related to the nutritional or body temperature changes associated with separation, as these changes had been taken into account. Much to the researchers' surprise, the drop in growth hormones seemed to be related to some unknown aspect of the pup's interaction with its mother; her presence seemed to be important to the release and/or production of the growth hormone (see Hofer 1981 for additional discussion). Reite and Capitanio (1985) think that this finding m a y help to explain the "failure to thrive syndrome" defined by Powell et al. (1967). When parents abuse infants by depriving them of physical affection, the children can gradually lose weight and may even die, even though they are fed a diet sufficient to sustain life. Much like the collective physiological data on the effects of parent-infant separation among primates, this finding implies that food intake alone is not enough to guarantee normal weight gain and survival in the absence of physical (and, one presumes, vestibular and auditory) stimulation. For other mammal infants, but especially primate infants, short-term separations lead to physiological consequences. This conclusion forces us to consider the possible effects of nocturnal separation on h u m a n infants who, in Western and urban societies, regularly sleep in separate rooms from their parents. It is ironic that the h u m a n primate infant-which is born the most immature neurologically, develops the most slowly, and is thus more, rather than less, dependent physiologically on its caregiver is the only primate that is expected to sleep alone at a very young age. Anthropologists have noted that some peoples living in preindustrial societies regard Western urban parent-infant sleeping arrangements as a form of child abuse. But the question here is whether it is easier for an infant's respiratory, immunological, or general central nervous system defects to appear in microenvironments from which species-specific auditory, tactile, and vestibular cues are missing. The question is not whether solitary infant sleeping arrangements cause SIDS, because surely they do not. Rather, the question is whether, as Lipsitt phrased it, the microenvironments of some small class of potential SIDS victims lack such stimuli and so conspire with neonatal or infantile defects, thus creating favorable conditions in which SIDS can occur (Lipsitt 1981). For some apnea-prone infants, such as those with rib cages that collapse, as Southall and associates (1985) discovered,

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parent-infant co-sleeping and all the available "compensatory" stimulation probably cannot help. But those infants with more "subtle" defects (see Haddad and Mellins 1983) may be aided in microenvironments that more closely approximate the conditions in which the h u m a n infant's physiological and developmental systems evolved, such as cosleeping, and that more closely approximate the prenatal sensory experiences discussed earlier.

Do Parents and Infants Breathe Each Other's

Expelled CO2? Do They Affect Each Other's Body Temperature? As I discussed in an earlier paper (McKenna 1986), Galef (1981) reminds us that a parent-infant huddle reduces the participants' surfaceto-volume ratio and thus conserves energy. Surely this is relevant to Fardig's (1980) study of infants in radiant-heated cribs and infants in their mothers" arms. The exchange of heat between and its conservation by parents and infants while sleeping together or in a ventral-ventral embrace are other examples of a process and a set of stimuli denied to infants encouraged to sleep alone. Such deprivation is, once again, perhaps not serious for the "healthy" infant, but it is well k n o w n that breathing depends on environmental (ambient) and b o d y temperature (Lahiri and Delaney 1975). In fact, temperature is also one of the most important external modulators of sleep, especially REM sleep (McGinty 1984). Cooling of an infant's body, even by a few degrees, will depress expiratory neuron firing, thereby diminishing respiration. Thus, the protection that a co-sleeping parent's body warmth offers is perhaps not to be considered insignificant, although there are surely other ways to compensate for the parent's contribution to maintaining the infant's resting temperature. When a parent sleeps with or near an infant, it is likely, at least for much of the night, that not only will their body heat be exchanged but also their expelled carbon dioxide gases. Sullivan (1984) suggests that during REM sleep, infants can smell carbon dioxide, in part because of the presence of carbon dioxide chemoreceptors in their nasal mucosa (see also Widdicombe 1981). In the microenvironment created by its parent the infant could therefore respond to the parent's exhaled carbon dioxide; that is, the infant's upper nasal chemoreceptors may receive enough of its parent's CO 2 to increase the chance of a brain-stemdirected inspiration. Guz (1977, cited in Tenney and Bartlett 1981) discusses recent evidence that CO2-sensitive receptors, which generate reflexive breathing, lie in mammals' respiratory tracts, possibly the lungs.

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The addition of CO 2 to air inspired by dogs increased their respiration frequency because of a decrease in their expiration duration. If these findings are generalized to humans, proximity to the parent might increase the likelihood of the infant's taking the next breath, should its other internal respiratory signals falter. Obviously, this gaseous exchange occurs simultaneously with touch, movement, heat exchange, scents, and auditory stimuli. It is one of many factors in the infant's evolutionally expected environment that, if operating alone, might be insufficient to promote continuous rhythmic breathing, but in concert with other stimuli, might reduce the likelihood of some forms of respiratory failure.

Relationship between Auditory Stimuli and Respiration The relationship between auditory stimuli and respiration has not been explored to the extent that, for example, auditory cues and heart rate (see Brackbill 1975; Schmidt 1975) or tactile and vestibular stimulation (see Barnard 1981) have. Abundant clinical and experimental evidence indicates that very young infants can detect and then respond to rapidly changing sounds, although there is no direct evidence, as far as I am aware, that human breathing sounds per se can effectively drive infant breathing. (This question is currently being studied by a team of researchers, including myself, by monitoring the breathing of mothers and infants as they sleep in the same bed.) But the evidence does suggest that 2- to 5-month-old infants can detect and respond to sound within the decibel range of human breathing and, indeed, to a variety of repetitive and rhythmic sounds in general (Brackbill 1973; Laufer 1980; Salk 1962; Schmidt et al. 1980; and reviews in Morse and Cowan 1982). Eisenberg's (1976, 1983) studies demonstrate that infants respond especially to speechlike sounds, such as the synthetic vowel sound ah at 60 dB, and that this sound is processed at what can be considered high levels of the auditory system. In other studies, Brackbill (1973, 1975) found that intermittent auditory stimulation tended to raise infants' arousal levels. More pertinent to the question raised here, though, is Bradford's (1975) finding that normal infants display an acute sensitivity (and respond by breathing) to levels ranging between about 15 and 30 dB, the decibel range of h u m a n vesicular breathing sounds. These infants most consistently responded to repetitive mechanical clicks at an average of 15 dB. Relative to other mammals, human infants, in addition to displaying auditory precocity, have clearly evolved a greater ability to detect subtle

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changes in the intensity of sound frequencies or pitch (Eisenberg 1983; Fobes and King 1982). Fobes and King (1982) found that, when compared with other mammals and other primates, a h u m a n primate's "best frequency"--a designation referring to the sound level that humans can hear most easily and respond to most quickly--is a low frequency level. This makes sense when one considers that language is the primary communicative system on which our survival, and thus our fitness, has depended for a considerable period of time. This kind of communication system demands attention to soft, rapidly changing tones and pitch, as well as to vocal, respiratory, and social cues related to turn-taking during interactions (Brazelton et al. 1974; Field 1985; Laufer 1980). It is obvious that in the environment in which infants evolved, auditory cues did not occur in isolation from tactile, vestibular, thermal, and gaseous sensory signals. All of these signals, especially the tactile, gaseous, and vestibular ones, directly enhance auditory cues. Recall that the physical proximity and mother-infant contact or contact with sibling caregivers (see Tronick et al. 1985) evolved concomitantly with delayed infantile maturity. Infants must be carried for at least the first year and must rely on continuous rather than periodic nursing, as a result of the relatively low fat and protein content of h u m a n milk (Blurton-Jones 1972). This means that even if the continuous-contact-and-carrying model that has been criticized by Tronick and colleagues (1985) is not the only model possible for human infant care throughout evolution, the infant will still be in close contact with a caregiver's breathing sounds and also with a variety of important alternating rhythmic and arrhythmic stimulation, not the least of which is the locomotor movement of its caregiver. Of course, when sleeping, the infant will feel the rhythmic chest movement of its parent's respiratory behavior as well as disruptive sleep movements and activities.

CONCLUSION A prolonged developmental period of physical dependence on a primary caregiver characterizes the evolutionary history of the human infant. A variety of research, particularly on the effects of short- and long-term separation on the physiology of n o n h u m a n primates and to a limited extent of h u m a n infants, has s h o w n that caregiving figures have significant regulatory effects on altricial mammals, especially primates whose brains are less developed at birth (relative to eventual adult size) and develop more slowly than other mammals. In fact, of all the primates the human infant is the least developed neurologically (approximately 25% of adult size) and, thus, we should expect that natural

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selection w o u l d favor infants especially r e s p o n s i v e to the e x t e n s i v e care o n w h i c h their survival d e p e n d s . Since h u m a n infant vulnerabilities c o e v o l v e d w i t h c o n t i n u o u s p a r e n t a l s e n s o r y contact, it is s u r p r i s i n g that investigations into an inexplicable infant m a l a d y s u c h as SIDS c o n t i n u e to ignore the potential c o n s e q u e n c e s of n o c t u r n a l p a r e n t a l contact a n d separation. Except for one general p a p e r b y t w o SIDS r e s e a r c h e r s (see H o p p e n b r o u w e r s a n d H o d g m a n 1986) the u n i q u e e v o l u t i o n a r y attributes of the h u m a n infant are n o t t h o u g h t to be r e l e v a n t e n o u g h to h e l p to s h a p e SIDS research questions. This p a p e r p r o v i d e s the b a c k g r o u n d against w h i c h h u m a n infant res p o n s i v i t y to p a r e n t a l contact can be a p p r e c i a t e d for future SIDS research. The s u c c e e d i n g p a p e r (Part II) f u r t h e r d e v e l o p s a n e x p l a n a t i o n of infant b r e a t h i n g characteristics a n d e x a m i n e s the r e l e v a n c e of p r e n a tal m a t e r n a l - f e t a l d e v e l o p m e n t a l p r o c e s s e s to p o s t n a t a l infant r e s p o n sivity to p a r e n t a l b r e a t h i n g cues, Part III relates c o n t e m p o r a r y SIDS research findings to o u r o w n p r e l i m i n a r y s t u d y of the b r e a t h i n g a n d sleep p a t t e r n s of co-sleeping h u m a n m o t h e r - i n f a n t p a i r s - - t h e first s t e p t o w a r d testing the general h y p o t h e s i s p r o p o s e d in this a n d a p r e v i o u s p a p e r (see M c K e n n a 1986). James J. McKenna is Associate Professor of Anthropology and Chair of the Department of Sociology and Anthropology at Pomona College. He also has an appointment as an Adjunct Clinical Assistant Professor in the Departments of Pediatrics, Child Psychiatry, and Human Behavior at the University of California, Irvine, School of Medicine. His primary research interests and many of his publications concern aspects of primate parenting and infant development among both human and nonhuman primates. For the past seven years he has been investigating from an anthropological perspective possible environmental correlates of the sudden infant death syndrome (SIDS) and has just finished a preliminary study on the physiological correlates of human parent-infant co-sleeping. His earlier monograph on the subject (cited in this paper) has received much international attention. He and his colleagues (Mosko and Dungy) are the first to have used standard polysomnographic techniques to document simultaneously human parent-infant co-sleeping. He has won three awards for distinguished teaching at Pomona College.

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