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found no rearing condition differences in either baseline
cortisol levels or stress responses ( Winslow et al., 2003 ).
These disparate findings are likely related to methodological
differences in peer-rearing procedures, age of the animals at
the time of sampling, and the outcome measures used in
each case. Some resolution of the rearing condition issue (as
it relates to HPA function) seems to have emerged from
a more recent, comprehensive study of 778 infant monkeys
that found lower cortisol levels in the afternoon, lower
cortisol rises in response to social separation, and less
responsiveness to both a dexamethasone suppression test
and an ACTH challenge test in peer-reared compared to
normally reared animals ( Capitanio et al., 2005 ). Together,
these findings provide evidence that peer rearing results in
a reduced cortisol set-point for the HPA axis.
Peer rearing can also result in long-lasting changes in
the immune system. Peer-reared monkeys showed greater
lymphocyte proliferation responses than mother-reared
monkeys ( Coe et al., 1989 ). This vulnerability was associ-
ated with lower proportions of CD8 cells and lower natural
killer cell activity ( Lubach et al., 1995 ) and a substantially
increased risk of diarrhea ( Elmore et al., 1992 ).
Research has indicated that many of the above-reported
behavioral and biological consequences of peer-rearing
are in part mediated by genetic factors, reflecting gene-
environment (G
result in neurochemical, physiological, and behavioral
dysfunction when the animals are compared either to
mother-reared subjects or to peer-reared subjects that lack
the vulnerability-conferring alleles.
Surrogate-peer Rearing
For many years, peer rearing was the primary way in which
nursery-reared monkeys were maintained. In recent years,
a second rearing procedure initially developed as a part of
Harlow's pioneering research on early experience has been
re-examined. The surrogate-peer rearing condition was
instituted in part to overcome the problem of infants
serving in the dual role as a maternal figure and as play-
mate. Surrogate-peer-reared monkeys were reared with
continuous exposure to an inanimate “terry cloth”-covered
mother and were given brief daily exposure to similarly
reared peers. Depending on the study, the exposure to peers
ranged from 30 minutes to 2 hours per day ( Meyer et al.,
1975, Rosenblum, 1961; Hansen, 1966 ). The goal of
surrogate-peer rearing was to simulate features of the early
mother
infant relationship wherein infants spent most of
their time with the mother and moved away briefly for short
play bouts with other infants. Thus, in surrogate-peer
rearing, the importance of a brief play period cannot be
overstated. More play time is not better; lengthier contact
during the day causes the infant monkeys to develop their
primary attachment to peers, thereby resulting in repeated
attachment object separation when group members are
returned to their individual enclosures at the end of each
day (S. Suomi, personal communication). Such conditions
create an early rearing environment that is not only anxiety
eliciting because of the peer rearing but also stressful
because of the separations. The adverse consequences of
rearing infant monkeys on a daily regimen of 8 hours
together followed by 16 hours of separation have been
described by Rommeck and associates (2009a). The
discussion below is, therefore, generally restricted to
studies in which the play period did not exceed 2 hours and
thus such separation effects are not observed.
e
E) interactions. For example, the behav-
ioral and physiological consequences of allelic variation in
the serotonin transporter (5-HTT) gene are far more
pronounced for peer-reared rhesus monkeys than for their
mother-reared counterparts. Specifically, peer-reared
monkeys carrying the “short” (less transcriptionally effi-
cient) allele of the 5-HTT gene exhibit significantly more
aberrant patterns of early neurobehavioral functioning than
peer-reared monkeys carrying the “long” (more transcrip-
tionally efficient) allele ( Champoux et al., 2002 ). These
effects include higher levels of aggression ( Barr et al.,
2003 ), lower CSF concentrations of the serotonin metabolite
5-HIAA ( Bennett et al., 2002 ), greater HPA activation
following social separation ( Barr et al, 2004a ), and higher
rates of alcohol consumption ( Barr et al., 2004b ). Of great
importance, there were no significant differences attribut-
able to 5-HTTallelic variation in any of these behavioral and
physiological measures among mother-reared monkeys of
comparable age and sex. A similar pattern of G
Behavioral Effects In contrast to peer rearing, the surro-
gate-peer-rearing procedure yielded normal social behavior
without the intense fearful reactions noted in peer-reared
monkeys ( Hansen, 1966; Ruppenthal et al., 1991 ). Some
forms of stereotypic behavior were observed (mostly digit
sucking and some rocking against the surrogate surface),
occurring about 5
Einter-
action involving allelic variation in the MAO-A gene and
peer- vs. mother-peer rearing has been reported for various
measures of aggressive behavior in rhesus monkey males
( Newman et al, 2005 ).
Based on the information presented above, it is clear that
peer-only rearing is a dramatically better rearing environ-
ment than partial isolation. Monkeys reared in this manner
develop many species-typical social behaviors and show
only some residual kinds of abnormal behavior. However,
peer rearing in association with specific genotypes does
10% of the time. But these patterns
declined across age such that surrogate-peer-reared
monkeys behaved more like normally reared monkeys than
peer-reared monkeys at 1 year of age ( Hansen, 1966 ).
Surrogate-peer-reared animals continued to develop
socially, showing adequate skills in grooming, reproduc-
tion, and parental care in adulthood ( Novak et al., 1992;
e
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