Physiological data recorded during the separations of young primates and
children from their mothers confirm the biphasic response to separation noted
by Bowlby (1969) as protest and despair, which is a period of agitation,
followed by a period of depression. The primate data are based on mother-in-
fant pigtail and bonnet monkey separations monitored by surgically implanted
telemetry (Laudenslager et al 1982, Reite & Capitanio 1984, Reite et al 1981b,
Reite & Snyder 1982). Generally, in these studies behavioral agitation was
followed by depression during the separation period. Shortly after the separa-
tion, the infants exhibited agitation characterized by increased motor activity
and frequent distress vocalizations. Depressed behaviors typically emerged
shortly thereafter and persisted throughout the separation period. The infants
moved more slowly than normal, and their play behavior was diminished.
Sleep disturbances were characterized by decreased rapid eye movement (REM) sleep as well as by increased arousals and time spent awake. The
agitated behavior that occurred immediately after separation was accompanied
by increased heart rate and body temperature followed by decreases in these
values to below baseline (Reite et al 1978).
In addition to behavioral and physiological disorganization, altered cellular
immune responses were noted in the separated pigtail monkeys by Reite et al
(1981a) and in the squirrel monkeys by Coe et al (1985). For example, during
the separation of two pigtail monkeys who had been reared together, an altered
cellular immune response occurred (Reite et al 1981a). At five weeks follow-
ing reunion, the cellular immune response of both monkeys was still slightly
depressed. Pigtail infants separated from their mothers also experienced per-
sistent separation effects. For example, although heart rate tended to return to
baseline and arrhythmias tended to disappear following the infants’ reunion
with their mothers, the altered cardiac activity persisted for some infant mon-
keys (Seiler et al 1979). In another study, persistent decreases in infant heart
rate and body temperature were noted following reunion with the mother
(Reite & Snyder 1982). Thus, the effects of these separations often persisted
even after reunion with an attachment figure such as the mother or a peer.
Similar data have been reported for hospitalized preschool children who were
receiving chemotherapy for childhood cancer (Hollenbeck et al 1980). The
disorganizing effects of separation generally paralleled those reported for pri-
mates. Behaviorally, the children first showed agitation and then depression,
as manifested by their play behavior, behaviors that were paralleled by
changes in body temperature and heart rate.
Stress and Coping with Separation
SEPARATION IN INFANTS AND CHILDREN In a study of preschool children’s
responses to separation from the mother during the birth of another child (Field
& Reite 1984), agitated behavior and physiology during the period of the
mother’s hospitalization were observed. Depression then followed in the chil-
dren after the mother’s return from the hospital. In the Field & Reite study, play
sessions were videotaped, night-time sleep was time-lapse videotaped, and the
parents were administered questionnaires on changes in their child’s behaviors.
Increases in negative affect, activity level, heart rate, night wakings, and crying
characterized the period of the mother’s hospitalization as one of agitation for
the children (see Figures 1 and 2). Longer periods of deep sleep at this stage
were interpreted as conservation-withdrawal (as if withdrawing from stimula-
tion to conserve energy)(see Figure 2). Following the mother’sreturn, decreases
were observed in positive affect, activity level, heart rate, and active sleep,
suggestive of depression (see Figures 1–3). Changes reported by the parents
included greater clinging and aggressive behaviors, eating and toileting problems, and disturbed sleep and illnesses that persisted following the mother’s
return from the hospital (Figure 4). Examples of the child’s disturbance were
revealed in parents’ comments that the child “wanted to be rocked and held,”
“reverted to baby talk, whining, and screaming for attention,” and “threatened
to run a truck across the baby’s head.” Elevated tonic heart rate in the children
during the mother’s hospitalization and depressed heartrate following herreturn
may have been mediated by the activity level changes, as in somatic coupling
of activity and heart rate (Obrist 1981). These elevated levels have in turn been
attributed to sympathetic adrenergic activation (Breese et al 1973). More pro-
longed periods of deep sleep during this phase may be the result of conserva-
tion-withdrawal noted to follow stress in infants and young children (Emde et
al 1971, Engel & Schmale 1972).
Decreased activity, depressed heart rate, and shorter periods of active sleep,
together with flat affect following the mother’s return may suggest depression.
Depressed children have less active sleep (Kupfer et al 1979), and depression
can be alleviated by depriving subjects of REM sleep (Vogel 1979). The
decrease in active sleep may be a homeostatic coping mechanism.
Depressed activity and heart rate are commonly reported when individuals
are in situations in which they are helpless, such as an avoidance task in which
human subjects have no control, situations in which adrenergic influences are
minimal (Obrist et al 1978). Bradycardia, associated with situations of help-
lessness, has also been attributed to parasympathetic activation or vagal tone
(McCabe & Schneiderman 1983). The arrival of a new sibling; a less active,
tired mother; and changes in children’s play interactions with their mother
may have been viewed by the children in the Field & Reite (1984) study as
situations over which they had very little control. The depressed behavior mayhave been exacerbated in these children by the arrival of the new sibling and
an altered relationship with the mother.
Heightened levels of arousal may stimulate the sympathetic adrenergic
system, resulting in agitated behavior. This behavior is typically associated
with active coping, in this case with attempting to recall the mother. Agitation
during separation may occur because of heightened arousal in the absence ofthe child’s principal arousal modulator, the mother. Depression may emerge as
the separation continues because of the child’s failure to bring the mother back
and of a lack of stimulation ordinarily provided by the mother. The depression
may be an adaptive homeostatic mechanism offsetting the effects of sympa thetic arousal, or it may result from inadequate amounts of stimulation and
limited beta-adrenergic activity. Confounds in the Field & Reite (1984) study
on separation effects were the changed relationship between the mother and
first-born because of the arrival of the new sibling, the exhaustion of the
mother, and very frequently the postpartum depression of the mothers them-
selves. These confounds, coupled with the concern generated by data showing
that repeated separations had cumulative effects on monkey infants, led us to
perform a study looking at repeated separations of children from mothers going on conference trips (Field 1991). Although the preschool children in the
study showed similar separation behavior as when the mothers went to the
hospital, they did not continue to show depression-related behavior after their
mothers returned. In addition, the first trip had the worst effect, and the effects
were not cumulative. Perhaps it is not surprising that because of their cognitive
coping skills, the children were able to adapt to that stress.
PEER SEPARATIONS A surprising finding for many attachment researchers is
that early peer separations also are distressing for young children. A peer
separation that occurs naturally and with some frequency results from the
transfer of children to new schools. In a recent study, Field (1984) observed
preschool children who had been together for three to four years and who were
transferring to new schools. The observations were made during a two-week
period prior to the separation from their classmates (Field 1984). The children
who were leaving the school, as opposed to those who were staying, showed
increases (compared with baseline observations three months earlier) in fantasy
play, physical contact, negative statements and affect, fussiness, activity level,
tonic heart rate, and illness, as well as changes in eating and sleeping patterns
(see Figures 5–8). In addition to the changes in play behavior and in vegetative
functions, the children’s drawings of themselves manifested agitation and
disorganization. The drawings included distorted facial and body parts and sad
faces (see Figure 8).
The anticipatory reactions to separation by these children appeared to
mimic the immediate responses to peer separations by young monkeys (Reite
et al 1981b). They were also very similar to the behaviors noted in young
children immediately following the hospitalization of their mothers for the
birth of another child (Field & Reite 1984). In these studies, the increase in
fussiness, negative affect, aggressive behavior, physical activity level, and
tonic heart rate are suggestive of agitation. Although changes in eating patterns
were variable, with some children eating more and others eating less, sleep
disturbances uniformly involved more frequent night wakings, crying, and
delayed onset of sleep. Increased illness during the children’s separations is
consistent with reports of changes in the immune system of young primates
during mother and peer separations (Reite et al 1981a, Reite & Snyder 1982).
Separation stress occurs when peers even as young as 15 months are sepa-
rated (Field et al 1984b). In the Field et al study, 15-month-old infants were
transferred, following 14 months in an infant nursery, to a toddler nursery, and
24-month-old infants were graduated from a toddler nursery to a preschool
nursery. Many of the same behavior changes occurred during the week imme-
diately preceding the transfer and the week following the transfer. These
included increased inactivity, negative affect, fussiness, and changes in eating
and sleep behaviors. Nap-time sleep became more irregular with longer latencies to sleep and more frequent arousals during nap time. In addition, erratic
feeding patterns were noted as well as more frequent illness. A comparison
between those infants and toddlers who were transferred to the new nurseries
without close friends and those who were transferred with close friends sug-
gested that transferring with close friends may buffer the stressful effects of
the separation. Thus, the data from this group of studies are a poignant demon-
stration of the disorganizing effects of mother and peer separations on both the
behavior and physiology of young monkeys and children.
Biological Markers and Mechanisms in Animal Models
Panksepp et al (1985) have advanced a model for attachment based upon
opiate systems and derived from data on very diverse species including chicks,
guinea pigs, and dogs. Because the social-separation state was similar to
opioid withdrawal in their studies, opiate receptor agonists were expected to
reduce separation distress. The opioid agonists Panksepp et al tested did allevi-
ate separation distress, and when they blocked opioid receptors by naloxone,
separation distress increased. They then evaluated the specificity of the opioid
effects using a variety of agonists and antagonists for cholinergic, noradrener-
gic, dopaminergic, and serotonergic receptor systems. Only clonidine (which
alleviates opiate withdrawal symptoms in humans) approached the level of
efficacy of opioids.


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