Early motherhood in rats is associated with a modification of hippocampal function
Introduction
The delivery and the onset of maternal experience constitute one of the greatest challenges experienced by female mammals. In rats, motherhood involves a myriad of new behavioral responses such as retrieving, crouching over and licking the newborn pups (Rosenblatt and Snowdon, 1996). The peripartal period is associated with marked fluctuations of several hormones, which play a significant role in the onset of maternal behavior (Rosenblatt et al., 1988). Many works have explored the neurobiology of maternal behavior in rodents and it is known that motherhood produces strong brain modifications in particular in the hypothalamic, ventral striatum and olfactory circuitries (Freund-Mercier et al., 1994; Fleming et al., 1999; Theodosis, 2002; Shingo et al., 2003; Numan, 2007). Furthermore, some of the hormones affected by parturition, such as estrogens and glucocorticoids (Atkinson and Waddell, 1995; Escalada et al., 1996) can also have drastic effects on systems and functions not directly linked to maternal behavior. The hippocampus plays a crucial role in spatial learning and memory processes (Squire et al., 2004). This structure shows a remarkable plasticity and is strongly influenced by hormonal and environmental challenges (McEwen, 2001; Ciriza et al., 2004; Li et al., 2004). It also constitutes one of the few neurogenic areas of the adult brain (Gould and Gross, 2002). Neurogenesis occurs in the olfactory bulbs and in the hippocampus of the mammal adult brain throughout life. This phenomenon takes place continuously, but the rate of proliferation and the fate of new cells may be affected by several factors (Gould et al., 2000; Abrous et al., 2005). Although, the exact function of the neurogenesis in the adult hippocampus remains to be clarified, several works suggest a possible implication in cognitive processes (Shors et al., 2001; Kee et al., 2007).
In humans, the period around parturition is a critical phase that is sometimes associated with cognitive disturbances (Eidelman et al., 1993; Brett and Baxendale, 2001; De Groot et al., 2006). In contrast, in rats, the reproductive experience seems to have a beneficial impact on learning and memory. The majority of the studies concerning rodents, however, are conducted after the lactating period (Kinsley et al., 1999; Gatewood et al., 2005; Lambert et al., 2005; Lemaire et al., 2006; Pawluski et al., 2006a, Pawluski et al., 2006b), while the peripartal period remains poorly explored.
The dramatic changes in the mother's hormonal milieu that occur just before and during the first 24 h following birth (Rosenblatt et al., 1988) could lead to marked changes of the hippocampal function and plasticity. The aim of this study, therefore, was to examine the hippocampal function after parturition in female rats. We assessed spatial performances in the water maze and neurogenesis in the hippocampus of mothers. Finally, corticosterone and estradiol levels, known to modulate both cognitive function and hippocampal neurogenesis were also measured.
Section snippets
Subjects
Nulliparous female Sprague–Dawley rats (Charles River, France) were housed by pairs for 1 week with a male for mating (mother group) or with a female (virgin group). Female rats were single-housed and not disturbed until the beginning of the study. Dams gave birth to 13.47 pups±1.47 (range 6–20 pups). Animals were maintained in a 12-h light/12-h dark cycle (lights on at 08:00 h) with free access to food and water. Manipulation of the animals was performed following the principles of laboratory
Early motherhood impairs spatial performances but enhances long-term retention of the spatial learning
Both virgin and mother rats exhibited a decrease in the latency (session effect, F(3,51)=12.16; p<0.0001, Fig. 1A) and in the distance covered (session effect, F(3,51)=20.11; p<0.0001, Fig. 1B) to reach the hidden platform across the four sessions of learning (six trials each) in the water maze task (group×session×trial effect, latency, F(15,255)=0.45; p=0.95; distance, F(15,255)=0.44; p=0.94). During the learning phase, however, lactating rats showed impaired performances as indicated by their
Discussion
Despite severe changes inherent to the transition from pregnancy to early postpartum, little attention has been paid to possible cognitive alterations during this period (Galea et al., 2000; Bodensteiner et al., 2006). Our work provides the first evidence of plasticity of the hippocampal function after delivery in rats. We show that spatial performances during learning phase were reduced after the delivery, while spatial retention ability was improved. In addition, early motherhood was
Role of funding sources
Funding for this study was provided by the University of Lille 1, the University has no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.
Conflict of interest
None declared.
Acknowledgments
This work was supported by University of Lille 1 and Ministerio de Educación y Ciencia, Spain. We thank D. Deschamps and S. Lefèvre for animal care and Dr. H. Bouwalerh for the analysis of the distance in the water maze. We thank Dr. C. Rampon and Professor J. Micheau for their helpful discussions and Roory Moody for the linguistic corrections of this manuscript. We also want to express our thanks to the anonymous reviewers for their pertinent criticisms and suggestions.
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Contributed equally.