Early Adoption Modifies the Effects of
Prenatal Stress on Dopamine and Glutamate
Receptors in Adult Rat Brain
Virginia G. Barros,
1
Marı ´a A. Berger,
1
Irene D. Martijena,
2
Marı ´a I. Sarchi,
3
Adriana A. Pe ´rez,
4
Victor A. Molina,
2
Frank I. Tarazi,
5,6
and Marta C. Antonelli
1
*
1
Instituto de Quı ´mica y Fisicoquı ´mica Biolo ´gicas (UBA-CONICET), Facultad de Farmacia y Bioquı ´mica,
Universidad de Buenos Aires, Buenos Aires, Argentina
2
Departmento de Farmacologı ´a, Facultad de Ciencias Quı ´micas, Universidad de Co ´rdoba, Co ´ rdoba, Argentina
3
Departamento de Fisicomatema ´tica, Facultad de Farmacia y Bioquı ´mica, Universidad de Buenos Aires,
Buenos Aires, Argentina
4
Laboratorio de Biometrı ´a, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires,
Buenos Aires, Argentina
5
Department of Psychiatry and Neuroscience Program, Harvard Medical School, Boston, Massachusetts
6
Mailman Research Center, McLean Division of Massachusetts General Hospital, Belmont, Massachusetts
Stressful stimuli during pregnancy induce complex effects
that influence the development of offspring. These effects
can be prevented by environmental manipulations during
the early postnatal period. Repeated restraint during the
last week of pregnancy was used as a model of prenatal
stress, and adoption at birth was used to change the post-
natal environment. No differences were found in various
physical landmarks, except for testis descent, for which all
prenatally stressed pups showed a 1-day delay in compar-
ison with control rats, regardless of the postnatal adoption
procedure. Levels of dopamine (DA) D
2
and glutamate (Glu)
N-methyl-D-aspartate (NMDA) receptors were differentially
regulated in different forebrain regions of cross-fostered
adult offspring. Increased concentrations of cortical D
2
re-
ceptors detected in stressed pups, raised by a gestationally
stressed biological mother, were not detected when the
pups were raised by a control mother. Control pups raised
by a foster mother whether gestationally stressed or not
had higher levels of NMDA receptors in cortical areas.
These findings suggest that the normal expression of DA
and Glu receptors is influenced by in utero experience and
by lactation. The complex pattern of receptor changes re-
flects the high vulnerability of DA and Glu systems to vari-
ations both in prenatal and in postnatal environment, par-
ticularly for cortical D
2
receptors and NMDA receptors in
cerebral cortex and nucleus accumbens. In contrast, testis
descent appears to be more susceptible to prenatal than to
postnatal environmental events. © 2004 Wiley-Liss, Inc.
Key words: dopamine D
2
receptors; glutamate NMDA
receptors; testis descent; prenatal stress; cross-foster-
ing; quantitative autoradiography
Offspring of pregnant female animals exposed to
stress prenatally have higher vulnerability to anxiety, ab-
normal circadian rhythm, impaired sexual function, and
enhanced propensity to self-administer drugs of abuse
(Henry et al., 1995; Valle ´e et al., 1999). Such vulnerability
may result from abnormalities in the development and
integration of forebrain dopamine (DA) and glutamate
(Glu) projections during the prenatal period. In this re-
gard, prenatal stress altered DA neurotransmission, evi-
denced by a higher DA turnover in prefrontal cortex and
a lower turnover in striatum and nucleus accumbens (Fride
and Weinstock, 1988; Alonso et al., 1997). In addition,
DA D
2
and D
3
receptors were increased and decreased,
respectively, in nucleus accumbens of mature adults sub-
jected to restraint prenatal stress (Henry et al., 1995). We
have recently assessed the effects of prenatal stress on DA
and Glu receptor expression in adult rats subjected to
repeated restraint stress during the last week of pregnancy
and found that these animals have higher levels of DA D
2
and Glu metabotropic group III receptors in cortical re-
gions and higher concentrations of N-methyl-D-aspartate
(NMDA) receptors in cerebral cortex and basal ganglia
compared with their control littermates (Berger et al.,
2002).
Several behavioral strategies have been employed to
modify the postnatal environment, namely, postnatal han-
dling, early adoption (or cross-fostering), and maternal
Contract grant sponsor: Agencia Nacional de Promocio ´n Cientı ´fica y
Tecnolo ´ gica; Contract grant number: PICT 02287; Contract grant sponsor:
CONICET; Contract grant number: PIP 6266.
*Correspondence to: Marta C. Antonelli, IQUIFIB, Facultad de Farmacia
y Bioquı ´mica, Junı ´n 956, 1113 Buenos Aires, Argentina.
E-mail: mca@mail.retina.ar
Received 2 December 2003; Revised 5 February 2004; Accepted 17
February 2004
Published online 9 April 2004 in Wiley InterScience (www.
interscience.wiley.com). DOI: 10.1002/jnr.20119
Journal of Neuroscience Research 76:488 – 496 (2004)
© 2004 Wiley-Liss, Inc.