Hippocampal morphology is differentially affected by reproductive experience in the mother.

Pregnancy and mothering result in a number of hormonal, neurological, and behavioral changes that are necessary to ensure reproductive success. With subsequent reproductive experience (multiparity and mothering), further neurological and behavioral changes may result. Recent research has shown that previous motherhood enhances both hippocampus-dependent learning and memory and long-term potentiation (LTP); together with decreases in hippocampus volumes during pregnancy it is suggested that the hippocampus is affected by pregnancy and/or mothering. The present experiment aimed to investigate the effect of reproductive experience (nulli, primi-, and multiparity and mothering) on dendritic morphology in the CA1 and CA3 regions of the hippocampus. Brains were stained with a modified version of the single-section Golgi impregnation technique, and dendritic length, number of branch points, and spine density was analyzed for apical and basal regions of CA1 and CA3 pyramidal neurons. Primiparity and/or mothering resulted in dendritic remodeling in both the CA1 and CA3 hippocampal regions, and multiparity resulted in enhanced spine density in the basal CA1 region, which was positively correlated with number of male pups in a litter. These findings point to the effect of reproductive experience and offspring on plasticity in the hippocampus, an area not traditionally associated with motherhood.

[1]  L. Galea,et al.  Reproductive experience differentially affects spatial reference and working memory performance in the mother , 2006, Hormones and Behavior.

[2]  A. Rasia-Filho,et al.  Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method , 2004, Neuroscience.

[3]  O. Kremmyda,et al.  Spatial Performance and Corticosteroid Receptor Status in the 21‐Day Restraint Stress Paradigm , 2004, Annals of the New York Academy of Sciences.

[4]  J. Feldon,et al.  Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within‐subject, within‐task comparison of reference and working spatial memory , 2004, The European journal of neuroscience.

[5]  C. Léránth,et al.  Androgens Increase Spine Synapse Density in the CA1 Hippocampal Subfield of Ovariectomized Female Rats , 2004, The Journal of Neuroscience.

[6]  T. Insel,et al.  The Neurobiology of Parental Behavior , 2003, Hormones, Brain, and Behavior.

[7]  L. Galea,et al.  Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. , 2003, Journal of neurobiology.

[8]  Sheng-tian Li,et al.  Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade , 2003, Nature Neuroscience.

[9]  L. Galea,et al.  Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. , 2002, Behavioral neuroscience.

[10]  G. Dohanich Gonadal Steroids, Learning, and Memory , 2002 .

[11]  J. Hajnal,et al.  Change in brain size during and after pregnancy: study in healthy women and women with preeclampsia. , 2002, AJNR. American journal of neuroradiology.

[12]  B. McEwen Estrogen actions throughout the brain. , 2002, Recent progress in hormone research.

[13]  V. Luine,et al.  Chronic restraint stress enhances radial arm maze performance in female rats , 2001, Brain Research.

[14]  S. Healy,et al.  A larger hippocampus is associated with longer-lasting spatial memory , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  S. Côté,et al.  Erratum to: Offspring sex ratio in relation to maternal age and social rank in mountain goats (Oreamnos americanus) , 2001, Behavioral Ecology and Sociobiology.

[16]  Morris Moscovitch,et al.  Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions , 2000, Nature Neuroscience.

[17]  N. Sousa,et al.  Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement , 2000, Neuroscience.

[18]  J. Goodhouse,et al.  Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice , 2000, Nature Neuroscience.

[19]  D. Wilkie,et al.  Spatial Working Memory and Hippocampal Size across Pregnancy in Rats , 2000, Hormones and Behavior.

[20]  Gordon W. Gifford,et al.  Motherhood improves learning and memory , 1999, Nature.

[21]  Larry R. Squire,et al.  Memory for places learned long ago is intact after hippocampal damage , 1999, Nature.

[22]  A. Fleming,et al.  Neurobiology of mother–infant interactions: experience and central nervous system plasticity across development and generations , 1999, Neuroscience & Biobehavioral Reviews.

[23]  P. Shughrue,et al.  Comparative distribution of estrogen receptor‐α and ‐β mRNA in the rat central nervous system , 1997, The Journal of comparative neurology.

[24]  A. Fleming,et al.  Cortisol, Hedonics, and Maternal Responsiveness in Human Mothers , 1997, Hormones and Behavior.

[25]  B. Mcewen,et al.  Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress , 1997, Neuroscience.

[26]  B. McEwen,et al.  Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. , 1996, Behavioral neuroscience.

[27]  A. Fleming,et al.  Plasticity in the maternal circuit: effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. , 1996, Behavioral neuroscience.

[28]  B. McEwen,et al.  Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors , 1995, Neuroscience.

[29]  R. Morris,et al.  Spatial learning with a minislab in the dorsal hippocampus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P Andersen,et al.  An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Bruce S. McEwen,et al.  Repeated stress causes reversible impairments of spatial memory performance , 1994, Brain Research.

[32]  C. Woolley,et al.  Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat , 1993, The Journal of comparative neurology.

[33]  B. McEwen,et al.  Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function , 1993, Brain Research.

[34]  R. Hammer,et al.  Parity-associated alterations of medial preoptic opiate receptors in female rats , 1992, Brain Research.

[35]  E Gould,et al.  Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  Bruce S. McEwen,et al.  Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons , 1990, Brain Research.

[37]  C. Woolley,et al.  Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  A. D. Mayer,et al.  Hormonal basis during pregnancy for the onset of maternal behavior in the rat , 1988, Psychoneuroendocrinology.

[39]  R. Bridges,et al.  Parity-associated reductions in behavioral sensitivity to opiates. , 1988, Biology of reproduction.

[40]  A. Fleming,et al.  Experience with pups sustains maternal responding in postpartum rats , 1987, Physiology & Behavior.

[41]  J. Atherton,et al.  Hormone profiles for progesterone, oestradiol, prolactin, plasma renin activity, aldosterone and corticosterone during pregnancy and pseudopregnancy in two strains of rat: correlation with renal studies. , 1987, The Journal of endocrinology.

[42]  B D Sachs,et al.  Maternal discrimination of pup sex in rats. , 1984, Developmental psychobiology.

[43]  J. Blank,et al.  Offspring sex ratio in red-winged blackbirds is dependent on maternal age. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[44]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[45]  C. L. Moore Maternal behavior of rats is affected by hormonal condition of pups. , 1982, Journal of comparative and physiological psychology.

[46]  G. Morelli,et al.  Mother rats interact differently with male and female offspring. , 1979, Journal of comparative and physiological psychology.

[47]  A. D. Mayer,et al.  Progress in the Study of Maternal Behavior in the Rat: Hormonal, Nonhormonal, Sensory, and Developmental Aspects , 1979 .

[48]  M. Diamond,et al.  Effects of pregnancy and differential environments on rat cerebral cortical depth. , 1977, Behavioral biology.

[49]  R. Gandelman,et al.  A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. , 1976, Developmental psychobiology.

[50]  R. Bridges Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat , 1975, Physiology & Behavior.

[51]  S. Levine,et al.  Pituitary-adrenal responsiveness during lactation in rats. , 1973, Neuroendocrinology.

[52]  M. Leon,et al.  Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. , 1970, Physiology & behavior.

[53]  R. Hawkins,et al.  Estrogen secretion by the rat ovary in vivo during the estrous cycle and pregnancy. , 1969, Endocrinology.

[54]  H. Moltz,et al.  Maternal behavior of primiparous and multiparous rats. , 1965, Journal of comparative and physiological psychology.