Behavioural Brain Research 153 (2004) 211–216
Research report
Stress during gestation induces lasting effects on emotional
reactivity of the dam rat
Muriel Darnaudéry
a,∗
, Isabelle Dutriez
b
, Odile Viltart
a
,
Sara Morley-Fletcher
a
, Stefania Maccari
a
a
Laboratoire du Stress Périnatal, JE 2365, Université de Lille 1, Villeneuve d’Ascq 59655, France
b
Laboratoire de Neuroendocrinologie du Développement, UPRES-EA 2701, Université de Lille 1, Villeneuve d’Ascq 59655, France
Received 1 August 2003; received in revised form 14 November 2003; accepted 2 December 2003
Available online 4 February 2004
Abstract
Human and animal studies indicate that repeated stress during pregnancy can produce long-term biological and behavioural disorders in
the offspring. In contrast, although maternal stress is supposed to induce an increase of maternal anxiety, few studies have been conducted
to demonstrate it. Therefore, in the present study we examined the emotional reactivity in stressed (chronic restraint stress applied 3×
45 min per day during the last week of pregnancy) and unstressed females rats after the weaning of their pups. Restraint stress procedure
reduced the body weight gain both during pregnancy and up to four weeks after the stress period. Stressed dams presented a reduction of
exploration and of corticosterone levels when exposed to a novel environment (25 and 49 days post-stress). They spent less time in the
open arms of the elevated plus-maze (26 days post-stress). Finally, they showed no increase in the time spent in immobility after a second
exposure to the forced-swim test (35–36 days post-stress). In the contrary, such differences were not observed when the chronic stress
procedure was applied on virgin females. Overall, our results show that, chronic stress during gestation induces lasting effects on emotional
reactivity of the dams, thus indicating that gestation constitutes a critical period in the vulnerability to stressful events also for the mother.
© 2003 Elsevier B.V. All rights reserved.
Keywords: Gestation; Rat dams; Chronic restraint stress; Anxiety; Novelty; Forced-swim test; Exploration; Corticosterone
1. Introduction
Stressful events such as pregnancy, labour and lactation
occur simultaneously with marked fluctuations in plasma
levels of steroid hormones, known to be involved in the vul-
nerability to emotional disorders. The first days postpartum
are often associated with the onset of major emotional vul-
nerability. However, pregnancy and lactation are generally
described as hyporesponsive periods to stress [15,34,53].
Thus, it remains unclear if pregnancy constitutes a critical
period involved in the vulnerability to stress. In rats, chronic
maternal stress during pregnancy has been used to study the
impact of early stress on development and later vulnerability
to stress in offspring. Several paradigms of stress including
daily subcutaneous injection [8], water immersion [9], over-
crowding [14] or restraint stress [24,49] induce long-term
behavioural [7,17,48,55] and neurobiological [19,24,28] ab-
∗
Corresponding author. Tel.: +33-320-43-40-80;
fax: +33-320-43-46-02.
E-mail address: muriel.darnaudery@univ-lille1.fr (M. Darnaud´ ery).
normalities in the offspring. Processes mediating the effect
of prenatal stress on the offspring have been proposed to in-
volve both prenatal [3] and postnatal [38,42] maternal fac-
tors.
While the impact of maternal stress during pregnancy on
physiology and behaviour of the offspring has been well
documented (for review, see [23,50]), up to date few studies
have explored the effect of gestation stress on the mater-
nal behaviour [25,29,35,36] and none on the behaviour of
the dams after weaning. Measurement of maternal anxiety
during lactation is difficult to validate since it involves the
reactivity to pup’s separation [43]. In the present study, we
evaluate reactivity of stress in several paradigms, 1–5 weeks
after the weaning of the pups. Our results demonstrate that
stress during pregnancy durably decreases maternal body
weight growth, increases anxiety-like behaviour and affects
reactivity to stress in primiparous females more than one
month after the stress procedure. Finally, in another exper-
iment we show that chronic stress has no effect on virgin
females suggesting that gestational state is a period of par-
ticular vulnerability to stress.
0166-4328/$ – see front matter © 2003 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbr.2003.12.001