Behavioural Brain Research 175 (2006) 90–95
Research report
Influence of parenting style on the offspring’s behaviour and CSF
monoamine metabolite levels in crossfostered and
noncrossfostered female rhesus macaques
Dario Maestripieri
a,b,∗
, Kai McCormack
b,c
, Stephen G. Lindell
d
,
J. Dee Higley
d
, Mar M. Sanchez
b,e
a
Department of Comparative Human Development, The University of Chicago, Chicago, USA
b
Yerkes National Primate Research Center, Emory University, Atlanta, USA
c
Department of Psychology, Spelman College, Atlanta, USA
d
Section for the Study of Primate Models of Psychopathology, National Institute on Alcohol Abuse and Alcoholism, Poolesville, USA
e
Department of Psychiatry, Emory University, Atlanta, USA
Received 15 June 2006; received in revised form 27 July 2006; accepted 2 August 2006
Available online 12 September 2006
Abstract
We investigated the association between variation in parenting style and the offspring’s behaviour and CSF monoamine metabolite (5-HIAA,
HVA, and MHPG) levels in rhesus monkeys. Study subjects were 25 two-year-old females reared by their biological mothers and 15 same-aged
females that were crossfostered at birth and reared by unrelated mothers. Subjects that were rejected more by their mothers in the first 6 months
of life engaged in more solitary play and had lower CSF concentrations of 5-HIAA than subjects that were rejected less. The relation between
these variables was generally similar in crossfostered and noncrossfostered females. CSF levels of 5-HIAA were negatively correlated with rates of
scratching, a behavioural indicator of anxiety. These results suggest that that early exposure to high rates of maternal rejection can result in higher
anxiety later in life, and that this effect may be mediated by serotonergic mechanisms. Variation in maternal protectiveness did not affect offspring
behaviour and neither protectiveness nor rejection affected CSF levels of HVA and MHPG. CSF levels of MHPG, however, were negatively
correlated with solitary play behaviour and avoidance of other individuals, suggesting that individuals with lower CSF MHPG were more fearful
and socially phobic than those with higher CSF MHPG. Taken together, these findings suggest that individual differences in anxiety and fearfulness
in young rhesus monkeys are accounted for, at least in part, by variation in CSF levels of monoamine metabolites, and that the development of
brain monoamine systems, particularly serotonin, can be affected by early exposure to variable maternal behaviour.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Parenting style; Early experience; Behavioural development; Brain monoamines; Primates
1. Introduction
Nonhuman primates (hereafter primates) are excellent ani-
mal models for investigating the effects of early experience
on the development of brain and behaviour [19,21]. Similar to
humans, primates have an extended period of post-natal growth
and maturation, in which the developing neural systems have
ample opportunity to be influenced by experience [18]. Most
∗
Corresponding author at: Department of Comparative Human Development,
The University of Chicago, 5730 S. Woodlawn Avenue, Chicago, IL 60637,
USA. Tel.: +1 773 834 4104; fax: +1 773 834 0320.
E-mail address: dario@uchicago.edu (D. Maestripieri).
of a primate infant’s early experience occurs in interaction with
its mother and this experience can be highly variable. In cerco-
pithecine monkeys such as macaques (Macaca spp.), baboons
(Papio spp.) and vervet monkeys (Chlorocebus aethiops), there
is a great deal of interindividual variation in parenting style
along the two orthogonal dimensions of maternal protectiveness
and rejection [13,22]. The protectiveness dimension includes
variation in the extent to which the mother physically restrains
infant exploration, initiates proximity and contact, and cradles
and grooms her infant. The rejection dimension includes vari-
ation in the extent to which the mother limits the timing and
duration of contact, suckling, and carrying. Although studies
of rodents have demonstrated that offspring reared by mothers
0166-4328/$ – see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbr.2006.08.002