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Origin and Ontogeny of Mammalian Ovarian Neurons

Department of Veterinary Integrative Biosciences (W.L.D., J.K.H., N.H.M., G.A.J.), College of Veterinary Medicine, Texas A&M University, College Station, Texas 77843-4458; and Division of Neuroscience (G.A.D., S.R.O.), Oregon National Primate Research Center/Oregon Health and Science University, Beaverton, Oregon 97006-3448

Address all correspondence and requests for reprints to: Dr. W. Les Dees, Department of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas 77845-4458. E-mail: ldees{at}cvm.tamu.edu.

Mammalian ovaries contain sympathetic neurons expressing the low affinity neurotropin receptor (p75^NTR). To date neither the role these neurons might play in ovarian physiology nor their embryological origin is known. Immunohistochemistry was used to detect postnatal changes in distribution and number of both p75^NTR-positive and tyrosine hydroxylase-positive neurons in rhesus monkey ovaries. Pig fetuses were used to map the pathway of ovarian neuronal migration during embryonic development. Antiserum to p75^NTR revealed the presence of isolated neurons and neurons clustered into ganglia in 2-month-old monkey ovaries. After 8 months, the neurons exhibited well-developed processes, and other than being more extensively interlaced, the localization and morphology did not change after 2 yr of age. Total number of p75^NTR-positive neurons present decreased gradually between 2 months and 12 yr of age and declined markedly with reproductive aging. Conversely, the subpopulation of neurons immunoreactive to anti-tyrosine hydroxylase increased significantly at puberty and then declined with the loss of reproductive capacity. By d 21 of fetal life in the pig, p75^NTR neurons had migrated medially from the neural crest to form the paraaortic autonomic ganglia. Some neurons migrated ventrally from the ganglia and then continued ventrolaterally to enter the genital ridge. By d 27, neurons had entered the developing ovary, and by d 35, the migration was complete with neurons demonstrating immunoreactivity to NeuN, a neuron-specific marker. Results demonstrate that p75^NTR-expressing ovarian neurons originate from the neural crest and that a catecholaminergic subset is associated with pubertal maturation of the ovary and subsequent reproductive function.

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