Elsevier

Psychoneuroendocrinology

Volume 32, Issue 7, August 2007, Pages 803-812
Psychoneuroendocrinology

Early motherhood in rats is associated with a modification of hippocampal function

https://doi.org/10.1016/j.psyneuen.2007.05.012Get rights and content

Summary

The transition to motherhood results in a number of hormonal, neurological and behavioral changes necessary to ensure offspring survival. However, little attention has been paid to changes not directly linked to reproductive function in the early mother. In this study, we demonstrate that spatial performances during the learning phase were impaired after the delivery in rats, while spatial retention ability was improved 2 weeks later. In addition, we also report that early motherhood reduced the cell proliferation in the dentate gyrus of the hippocampus without inducing a decrease in the newborn cells 2 weeks later. The decrease of estradiol levels and high levels of glucocorticoids after delivery could in part explain the changes in the hippocampal function. In summary, our findings suggest that early postpartum period is associated with a modification of hippocampal function. This may reflect a homeostatic form of hippocampal plasticity in response to the onset of the maternal experience.

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.

References (56)

  • J.D. Gatewood et al.

    Motherhood mitigates aging-related decrements in learning and memory and positively affects brain aging in the rat

    Brain Res. Bull.

    (2005)
  • E. Gould et al.

    Regulation of hippocampal neurogenesis in adulthood

    Biol. Psychiatry

    (2000)
  • A. Graziano et al.

    Automatic recognition of explorative strategies in the Morris water maze

    J. Neurosci. Methods

    (2003)
  • H. Karhunen et al.

    Long-term functional consequences of transient occlusion of the middle cerebral artery in rats: a 1-year follow-up of the development of epileptogenesis and memory impairment in relation to sensorimotor deficits

    Epilepsy Res.

    (2003)
  • K.G. Lambert et al.

    Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats

    Physiol. Behav.

    (2005)
  • B. Leuner et al.

    Learning during motherhood: a resistance to stress

    Horm. Behav.

    (2006)
  • P. Mohapel et al.

    Working memory training decreases hippocampal neurogenesis

    Neuroscience

    (2006)
  • I.D. Neumann

    Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats

    Prog. Brain Res.

    (2001)
  • J. O’Keefe

    A computational theory of the hippocampal cognitive map

    Prog. Brain Res.

    (1990)
  • J.L. Pawluski et al.

    Reproductive experience differentially affects spatial reference and working memory performance in the mother

    Horm. Behav.

    (2006)
  • J.L. Pawluski et al.

    First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or ‘mothering’ alone

    Behav. Brain Res.

    (2006)
  • J.S. Rosenblatt et al.

    Hormonal basis during pregnancy for the onset of maternal behavior in the rat

    Psychoneuroendocrinology

    (1988)
  • D.T. Theodosis

    Oxytocin-secreting neurons: a physiological model of morphological neuronal and glial plasticity in the adult hypothalamus

    Front. Neuroendocrinol.

    (2002)
  • D.N. Abrous et al.

    Adult neurogenesis: from precursors to network and physiology

    Physiol. Rev.

    (2005)
  • H.C. Atkinson et al.

    The hypothalamic–pituitary–adrenal axis in rat pregnancy and lactation: circadian variation and interrelationship of plasma adrenocorticotropin and corticosterone

    Endocrinology

    (1995)
  • Butovsky, O., Koronyo-Hamaoui, M., Kunis, G., Ophir, E., Landa, G., Cohen, H., Schwartz, M., 2006. Regulation of...
  • I.C. Chou et al.

    Behavioral/environmental intervention improves learning after cerebral hypoxia-ischemia in rats

    Stroke

    (2001)
  • I. Ciriza et al.

    Selective estrogen receptor modulators protect hippocampal neurons from kainic acid excitotoxicity: differences with the effect of estradiol

    J. Neurobiol.

    (2004)
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