Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol
Section snippets
Experimental procedures
All animals were treated in accordance with the guidelines set forth by the Canadian Council on Animal Care and with the policies on animal care established by The University of British Columbia. Every effort was made to minimise the number of animals used per group and to minimise the suffering of animals used throughout all experimental procedures.
Density of bromodeoxyuridine-labelled cells and pyknotic cells in the granular cell layer and hilus
A BrdU-labelled cell found in the subgranular zone of an adult female meadow vole is shown in Fig. 1A. BrdU-labelled cells were observed to occur primarily in clumps located in the subgranular zone. The density of BrdU-labelled cells in the granule cell layer was significantly greater in RI and EB4 females compared to RA females (P ≤ 0.0007) and EB48 females (P ≤ 0.0013, see Table 1). Similarly, the density of BrdU-labelled cells in the hilus (see Table 1) of RI females was greater compared
Discussion
The density of proliferating cells in the dentate gyrus was elevated in RI relative to RA females and was negatively correlated with serum estradiol level. These findings indicate that reproductive status regulates cell proliferation in female meadow voles. The degree of suppression in cell proliferation observed in RA versus RI females could be reproduced by exposing female meadow voles to EB for 48 h, but not 4 h. In fact, exposure to EB for 4 h tended to elevate the number of proliferating
Conclusions
Reproductive status, possibly through estradiol, regulates cell proliferation and survival in the dentate gyrus of adult female meadow voles. Initially, estradiol tends to increase cell proliferation in the dentate gyrus of rodents but subsequently induces a mechanism (perhaps CORT mediated) that suppresses cell proliferation. Although the density of labelled cells remains elevated in RI females relative to RA females, five weeks later, the rate of survival of newly formed granule cells in the
Acknowledgements
We wish to thank Wayne Yu and Joanne Weinberg for their assistance with the corticosterone radioimmunoassays and Catharine Rankin for her helpful comments regarding this manuscript. This research was funded by an Alzheimers Society of British Columbia grant to LAMG and an NSERC postgraduate scholarship to BKO. A portion of these data was presented at the 1999 Society for Neuroscience Meeting in Miami.
References (87)
- et al.
Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats
Neuroscience
(1999) - et al.
Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus
Neuroscience
(1994) - et al.
Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat
Neuroscience
(1993) - et al.
Male stimuli are necessary for female sexual behavior and uterine growth in prairie voles (Microtus ochragaster)
Horm. Behav.
(1987) - et al.
Ovarian hormones regulating sexual and social behaviors in female prairie voles, Microtus ochragaster
Physiol. Behav.
(1979) - et al.
Estrogens up-regulate Type I and Type II glucocorticoid receptors in brain regions from ovariectomized rats
Life Sci.
(1991) - et al.
Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles
Neuroscience
(1999) - et al.
Spatial working memory and hippocampal size across pregnancy in rats
Horm. Behav.
(2000) - et al.
Lesion-induced proliferation of neuronal progenitors in the denate gyrus of the adult rat
Neuroscience
(1997) - et al.
Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus
Neuroscience
(1990)
Immunocytochemical localization and quantification of estrogen binding sites in the male and female (virgin, pregnant, lactating) mouse brain
Brain Res.
Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat
Neurosci. Lett.
Kindling induced neurogenesis in the dentate gyrus of the rat
Neurosci. Lett.
Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus
Horm. Behav.
Postnatal neurogenesis in the guinea-pig
Nature
Arvicola richardsonii: ecology and biochemical polymorphism in the front ranges of southern Alberta
Acta. Therio.
Time of neuron origin in the hippocampal region: an autoradiographic study in the mouse
Expl Neurol.
Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees
Proc. natn. Acad. Sci. USA
Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning
Proc. natn. Acad. Sci. USA
Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures
Proc. natn. Acad. Sci. USA
Spring declines in Microtus pennsylvanicus and the role of steroid hormones
J. Animal Ecol.
Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with foetal raphe neurons
Eur. J. Neurosci.
Activity of the pituitary-adrenocortical system and thyroid gland during the oestrous cycle of the rat
J. Endocr.
Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrous cycle of the rat
Endocrinology
Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus
J. Neurosci.
Restoring production of hippocampal neurons in old age
Nature Neurosci.
Adrenal steroids and N-methyl-d-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats via a common pathway
Neuroscience
Oestrus and induced ovulation in the meadow vole, Microtus Pennsylvanicus
J. Rep. Fert.
Males increase serum estrogen and estrogen receptor binding in the brain of female voles
Physiol. Behav.
Effect of ovariectomy on pituitary secretion of ACTH
Endocrinology
Neurogenesis in the adult human hippocampus
Nat. Med.
Gonadal hormone levels and spatial learning performance in the Morris water-maze in male and female meadow voles, Microtus pennsylvanicus
Horm. Behav.
Differential regulation of NMDAR1 and mRNA and protein by estradiol in the rat hippocampus
J. Neurosci.
Adult neurogenesis: from canaries to clinic
J. Neurobiol.
Learning enhances adult neurogenesis in the hippocampal formation
Nature Neurosci.
Adrenal hormones suppress cell division in the adult rat dentate gyrus
J. Neurosci.
Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation
J. Neurosci.
Hippocampal neurogenesis in old world primates
Proc. natn. Acad. Sci. USA
Neurogenesis in the neocortex of adult primates
Science
Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress
Proc. natn. Acad. Sci. USA
Naturally occurring cell death in the developing dentate gyrus of the rat
J. comp. Neurol.
Subgranular zone of the dentate gyrus of young rabbits as a secondary matrix
Devl Neurosci.
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