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(e.g. rejection, or neglect), and/or when infant complications
such as low birth weight, poor sucking reflex, or illness make
it unlikely that
infancy and aggressiveness in adolescence ( Harlow and
Harlow, 1965 ). Infant peer-reared monkeys reacted to
minor changes in the environment by vocalizing and
clutching other members of their peer group for a pro-
longed period of time. They also displayed more intense
reactions to social separation than normally reared
monkeys ( Higley et al., 1991 ). Juvenile peer-reared male
monkeys showed lower levels of affiliative behavior and
were less likely to have their stress levels reduced by the
presence of a companion than normally reared males
( Winslow et al., 2003 ). Adolescent peer-reared monkeys
were much more likely to develop impulsively aggressive
patterns of response than their mother-reared counterparts
( Higley et al., 1996 ).
the infant will survive without nursery
intervention.
Peer-only Rearing
In the peer-rearing condition, infants are removed from
their mothers shortly after birth, reared in a nursery for
several weeks or more, and then placed in social groups
consisting of other like-reared infants. Although peer-only
rearing is the typical procedure for rearing infants in
a nursery, there has been considerable variation in how it
has been implemented at different facilities. Procedures
vary with respect to whether infants are removed from
mothers at birth or at a somewhat later point in time, how
long the infants are maintained in the nursery, whether they
receive any social contact during this period, and the size of
the social group into which they are ultimately placed
(Wisconsin National Primate Center, see Clarke 1996 ;
California National Primate Center, see Capitanio et al.,
2005 ; Laboratory of Comparative Ethology, National
Institutes of Child Health, see Roma et al., 2006 ; Yerkes
Primate Center, see Sanchez et al., 1998; Winslow et al.,
2003 ). Much of the discussion below is based on the orig-
inal paradigm in which infants were removed from their
mothers very shortly after birth.
Physiological Effects Peer-only rearing has been associ-
ated with changes in several physiological systems,
particularly the monoaminergic and neuropeptide systems.
Cerebrospinal fluid (CSF) measurements have provided
evidence for increased noradrenergic system activity,
decreased serotonergic activity, and reduced oxytocin
concentrations in peer-reared compared to normally reared
monkeys ( Higley et al., 1992; Clarke et al., 1996; Winslow
et al., 2003; Shannon et al., 2005 ). CSF oxytocin levels
were positively correlated with affiliative social behavior
( Winslow et al., 2003 ). Neuroimaging approaches have
revealed additional neurochemical and neuroanatomical
differences related to rearing condition. For example,
a positron emission tomography (PET) study revealed
significantly less serotonin binding potential and lower
rates of cerebral blood flow in many brain regions of
juvenile peer-reared monkeys relative to that of mother-
peer-reared counterparts ( Ichise et al., 2006 ). Peer-reared
monkeys also showed reductions in corpus callosum size
and decreased white matter volume in the parietal and
prefrontal cortex in comparison to normally reared
monkeys as determined by magnetic resonance imaging
(MRI) ( Sanchez et al., 1998 ). At present, the relationships
between structural brain changes, neurotransmitter and
neuropeptide alterations, and stereotypic behavior remain
largely unknown.
Because heightened fearfulness is a key characteristic of
peer rearing, the hypothalamic-pituitary-adrenocortical
(HPA) axis has been the focus of a number of studies
examining stress responsiveness. Initial studies of cortisol
levels were inconclusive in that peer-reared monkeys were
reported to have higher basal concentrations of cortisol
( Higley et al., 1992 ) or decreased stress responsivity with no
difference in basal levels ( Clarke, 1993 )comparedto
mother-peer reared controls. Shannon and coworkers (1998)
subsequently found lower concentrations of cortisol in peer-
reared compared to mother-reared infants during the first
2 months of life, although there was no difference in their
response to 30-minute separation periods. Yet another study
Behavioral Effects In contrast to early isolation rearing,
monkeys separated from their mothers at birth and reared
with other infants (peers) developed most of the species-
typical social responses and showed substantially lower
levels of stereotypic behavior ( Harlow and Harlow, 1965 ).
Infant
peer-reared monkeys
displayed
stereotypic
behavior
(typically digit sucking and rocking) about
4
20% of the time. Some stereotypic patterns of behavior
were observed in adulthood but at considerably lower
levels than observed in isolation-reared monkeys. In some
cases, peer-reared males also failed to develop the double
foot-clasp mount needed for mating ( Goy et al., 1974; Goy
and Wallen, 1979 ). This finding is particularly noteworthy
inasmuch as peer-rearing was, at one time, a relatively
common rearing procedure employed at several primate
facilities until a few of these peer-reared males proved
unsuitable as replacements for old feral males in the
breeding colony. Maternal behavior, on the other hand,
appeared to be unaffected by peer-rearing. Peer-reared
mothers maintained in stable social groups displayed
appropriate maternal behavior and produced infants whose
behavior was indistinguishable from the infants of nor-
mally reared mothers ( Roma et al., 2006 ).
Despite the relatively mild effects on abnormal
behavior, peer-reared monkeys showed marked deficits in
emotion regulation manifested by heightened fearfulness in
e
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