Psychological stressors as a model of maternal adversity: Diurnal modulation
of corticosterone responses and changes in maternal behavior
Marion Léonhardt
a
, Stephen G. Matthews
b
, Michael J. Meaney
a
, Claire-Dominique Walker
a,
⁎
a
CIHR program in Maternal Adversity, Vulnerability and Neurodevelopment (MAVAN) Douglas Hospital Research Center, Department of Psychiatry,
McGill University, Montreal, Quebec, Canada H4H 1R3
b
Department of Physiology, Medicine and Obstetrics and Gynaecology, University of Toronto, Toronto, Canada M5S 1A8
Received 24 May 2006; revised 23 August 2006; accepted 28 August 2006
Available online 10 October 2006
Abstract
Maternal adversity is associated with long-lasting consequences on cognitive development, behavior and physiological responses in rat
offspring. Few studies have examined whether repeated maternal stress produces repeated activation of the hypothalamus–pituitary–adrenal
(HPA) axis in mothers and whether it modifies maternal behavior. Here, we tested a novel model of perinatal stress using repeated exposure to
“purely” psychological stressors throughout the gestation and lactation periods in rats. We first tested the diurnal influences of repeated 1-h strobe
light exposure on maternal corticosterone secretion. Despite the hyporesponsiveness to stress documented in late pregnant and lactating mothers,
we observed an enhanced response to strobe light in the afternoon compared to the morning in stressed mothers during lactation. Next, dams were
exposed to 24-h forced foraging followed by 10-h wet bedding during the diurnal peak of corticosterone secretion. Although no corticosterone
responses to forced foraging and wet bedding were observed, the combination of both stressors had a significant effect on maternal behavior.
Mother–pup interactions were significantly altered during the first 8 days of lactation. Taken together, these findings suggest that lactating mothers
maintain responsiveness to specific and repeated psychological stressors, in particular at the time of the diurnal peak in corticosterone secretion.
Depending on the stressor applied, either neuroendocrine activation or changes in maternal behavior might be important determinants of the long-
term consequences in the offspring. The combination of forced foraging, wet bedding and strobe light might represent a novel model of mild
maternal adversity using “purely” psychological stressors.
© 2006 Elsevier Inc. All rights reserved.
Keywords: Maternal stress; Corticosterone; Maternal behavior; Diurnal stress response; Forced foraging; Wet bedding
Introduction
Human epidemiological data as well as animal studies
consistently show that early life stress is associated with defects
in cognitive and affective development as well as impaired
physiological stress responses (Meaney and Szyf, 2005; Pryce et
al., 2005; Mirescu et al., 2004; Chapillon et al., 2002; Lemaire et
al., 2000; Vallee et al., 1999; Cianfarani et al., 1998; Maccari et
al., 1995), which increases the susceptibility to physiological
and psychological pathologies later in life (for reviews see
Seckl, 2001; Weinstock, 2001; Matthews, 2002). Such
programming is thought to be a consequence of complex
interactions between differential gene expression or vulnerabil-
ity factors, stress hormones released by the hypothalamic–
pituitary–adrenal (HPA) axis in mothers (Kapoor et al., 2006),
and variations in maternal care (for reviews see Fish et al., 2004;
De Kloet et al., 2005). In rats, the perinatal period represents a
critical window for brain development (Avishai-Eliner et al.,
2002; Morgane et al., 1993). A burst of brain growth and a rapid
neuroendocrine maturation occur during this period which
makes the brain highly vulnerable to environmental program-
ming (Meaney and Szyf, 2005; Ozanne and Hales, 2002;
Matthews, 2002). Several paradigms of prenatal and perinatal
maternal stress have been used to induce behavioral and
biological dysfunctions in rodent offspring, including immobi-
lization or restraint in a plastic cylinder (Maccari et al., 1995;
Rojo et al., 1985; Smith et al., 2004), novel environment
exposure (Muir et al., 1985; Maestripieri et al., 1991), immersion
Hormones and Behavior 51 (2007) 77 – 88
www.elsevier.com/locate/yhbeh
⁎
Corresponding author. Douglas Hospital Research Center, 6875 Lasalle
Blvd, Verdun, QC, Canada H4H 1R3. Fax: +1 514 762 3034.
E-mail address: waldom@douglas.mcgill.ca (C.-D. Walker).
0018-506X/$ - see front matter © 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.yhbeh.2006.08.008