Innervation of the female reproductive system provides an important signal for a variety of neuroendocrine reflexes and behaviors in the female rat. Although some studies suggest that afferent feedback from the gonads is involved in the hypothalamic control of gonadal function and pituitary hormone release, the extent and function of afferent feedback from the gonads in these neuroendocrine reflexes has yet to be clarified. Deafferentation studies have provided only partial support for the afferent control of the gonads. Some studies even suggest functional asymmetries in the neural control of the gonads, but knowledge regarding the neuroanatomical substrate for these possible neurogonadal interactions remains incomplete. Studies with retrograde tract tracers indicate that the ovaries receive a substantial afferent supply from lower thoracic-upper lumbar dorsal root ganglia. Despite stringent precautions to prevent diffusion of tracers following injections into the ovary or related nerves, many of the retrogradely labeled cell bodies identified by these studies may represent an overestimation of the extent of afferent innervation. We have reexamined the afferent innervation of the female reproductive tract by means of the anterograde transport of horseradish peroxidase (HRP) from thoracic, lumbar and sacral dorsal root ganglion to pelvic visceral organs and have studied the effects of unilateral ganglionectomy on substance P containing fibers in the ovary, oviduct and uterus. The neuroanatomical results show that the T 13 and L 1 dorsal root ganglia provide major afferent innervation to the cranial portion of the reproductive tract and the L 6 and S 1 dorsal root ganglia provide primary afferent fibers to the caudal portion of the reproductive tract as well as the bladder, rectum and perineum. Numerous afferent fibers accompany the ovarian artery and the majority of these fibers continue past the ovary towards the oviduct and uterus. Afferent fibers were identified throughout the entire length of the uterine horns but they were generally widely dispersed. In contrast, the afferent innervation of the oviducts appeared to be more extensive than the uterine homs. Only 2 out of 14 tracer injections into the T 13 and l 1 dorsal root ganglia produced labeled fibers within the ovary and in both cases, the fibers accompanied blood vessels. However, labeled fibers were generally identified in the ovarian bursa and associated peritoneum following tracer injections into the T 13 and L 1 ganglia. In contrast to the dispersed and modest amount of afferent labeling observed in the cranial portion of the female reproductive tract, HRP injections into the L 6 and S 1 dorsal root ganglia produced many labeled fibers in the cervical portion of the uterus, vagina, base of the bladder and rectum. Also, numerous labeled fibers and nerve bundles supplying the perineum and external genitalia were observed. Innervation of the vagina was generally more extensive than the innervation of the cervix. Numerous HRP labeled fibers were found at the base of the cervix, but afferent fibers were rarely found cranial to the bifurcation of the uterine horns following injections into the L 6 and S 1 dorsal root ganglia. Substance P immunocytochemistry indicated numerous substance P-like immunoreactive fibers in the oviducts, a moderate numbers of substance P-like fibers in the uterine homs and a few substance P-positive fibers in the ovary. This was the same relationship in terms of numbers of afferent fibers revealed by the neuroanatomical results. Unilateral removal of the T 13 and l 1 dorsal root ganglia eliminated or markedly reduced the number of substance P-like immunoreactive fibers in the uterine horn, oviduct, ovary and ovarian bursa on the same side as the surgery, relative to the unoperated side and sham operated animals. These results verify a dual origin of the afferent innervation to the female reproductive system. The cranial structures receive a modest and diffuse afferent supply from the thoraco-lumbar dorsal root ganglia via the ovarian and hypogastric nerves and the caudal portion of the reproductive tract, as well as the bladder, rectum and perineum, receive an extensive afferent innervation from the lumbo-sacral dorsal root ganglia via the pelvic and pudendal nerves. Finally, these results indicate that there is a modest afferent innervation to the ovarian bursa and surrounding peritoneum but a very limited number of afferent fibers enter the gonad. This verifies the presence of afferent fibers to the ovary and its bursa, but the functional role of this limited afferent pathway in gonadal regulation remains to be clarified.
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