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Science 299 (5603): 117-120

Copyright © 2003 by the American Association for the Advancement of Science

Pregnancy-Stimulated Neurogenesis in the Adult Female Forebrain Mediated by Prolactin

Tetsuro Shingo,* Christopher Gregg, Emeka Enwere, Hirokazu Fujikawa, Rozina Hassam, Colleen Geary, James C. Cross, Samuel Weissdagger

Neurogenesis occurs in the olfactory system of the adult brain throughout life, in both invertebrates and vertebrates, but its physiological regulation is not understood. We show that the production of neuronal progenitors is stimulated in the forebrain subventricular zone of female mice during pregnancy and that this effect is mediated by the hormone prolactin. The progenitors then migrate to produce new olfactory interneurons, a process likely to be important for maternal behavior, because olfactory discrimination is critical for recognition and rearing of offspring. Neurogenesis occurs even in females that mate with sterile males. These findings imply that forebrain olfactory neurogenesis may contribute to adaptive behaviors in mating and pregnancy.

Genes & Development Research Group, Department of Cell Biology and Anatomy and Department of Biochemistry and Molecular Biology, University of Calgary Faculty of Medicine, Calgary, Alberta, Canada T2N 4N1.
*   Present address: Department of Neurological Surgery, Okayama University Medical School, 2-5-1 Shikata-cho, Okayama 700-8558, Japan.

dagger    To whom correspondence should be addressed. E-mail: weiss{at}ucalgary.ca



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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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