Number, size, conduction, and vasoconstrictor ability of unmyelinated fibers of the ovarian nerve in adult and aged rats

doi:10.1016/j.autneu.2011.05.001

Autonomic Neuroscience

Volume 164, Issues 1–2, 28 October 2011, Pages 6-12

https://doi.org/10.1016/j.autneu.2011.05.001 Get rights and content

Abstract

The effect of aging on the number, size, conduction velocity, and vasoconstrictive function of unmyelinated fibers in ovarian nerve accompanying the ovarian artery was studied in adult (4–7 mo) and aged (28–31 mo) rats. Morphological observation by electron microscopy showed that the ovarian nerve contains mainly unmyelinated fibers with only a small percentage (less than 4%) of myelinated fibers in either age group. The number of unmyelinated fibers tended to decrease in aged rats (717 ± 59) compared to adult rats (801 ± 48), especially in fibers of smaller diameter, although this difference was not statistically significant. The maximum conduction velocity of unmyelinated fibers within the ovarian nerve was similar when compared between adult (1.05 ± 0.04 m/s) and aged (1.02 ± 0.05 m/s) rats. Under anesthesia, electrical stimulation of the distal portion of a severed ovarian nerve reduced ovarian blood flow, as measured by laser Doppler flowmetry, when the stimulus intensity was above the threshold for unmyelinated C fibers. Stimulation of the ovarian nerve with supra-maximum intensity (10 V) at 2–20 Hz frequencies produced frequency-dependent reductions in ovarian blood flow in both adult and aged rats. There were no significant differences in magnitude of the reduction in ovarian blood flow with comparable frequencies of electrical stimulation of the ovarian nerve between adult and aged rats. Collectively, these data indicate that unmyelinated C fibers in ovarian nerve are maintained in number, size, conduction ability, and vasoconstrictor function in aged rats.

Introduction

The female reproductive system undergoes senescence relatively early during the aging process. There have been many studies on age-related changes at each level of the hypothalamic-pituitary-ovarian axis (Finch et al., 1984, Faddy et al., 1992, Weiss et al., 2004, Brann and Mahesh, 2005). Recent studies have shown that the ovary is controlled not only by hormones but also by autonomic nerves (Burden, 1985, Owman and Stjernquist, 1988, Traurig and Papka, 1993).

In our laboratory, we have recently demonstrated in anesthetized rats that stimulation of the sympathetic nerve that innervates the ovary (splanchnic nerve and ovarian nerve along the ovarian artery) causes a reduction of ovarian blood flow (Uchida et al., 2003, Uchida et al., 2007). This suggests ovarian sympathetic nerves regulate ovarian blood flow by playing a role in vasoconstriction. Ovarian sympathetic vasoconstriction may have a role in regulating ovarian blood flow in order to adapt to internal and external conditions in a manner similar to other autonomic regulatory systems in each organ (Uchida et al., 2003). Although it is important to understand how the regulation by ovarian sympathetic nerve of ovarian blood flow is affected during aging, only a few studies have investigated the effect of aging on autonomic innervation of the ovary. Ferrante et al. (1990) reported a reduction of noradrenergic innervation of the ovary of aged rats (24 months old) compared to young rats (3 months old) by measuring ovarian noradrenaline levels and by catecholamine histofluorescence techniques. No data are available concerning the effects of aging on ovarian autonomic nerves, especially in terms of structure and function.

The present study aimed to clarify if ultrastructure, conduction ability and blood flow regulation of ovarian nerves are affected during the aging process. In order to accomplish this, we used adult (4–7 months old) and aged (28–31 months old) rats, and observed firstly the ultrastructure of ovarian nerve fibers by electron microscopy. Secondly, we examined the conduction ability of ovarian nerves using electrophysiological techniques. Finally, we examined ovarian blood flow response to efferent stimulation of the ovarian nerve.

Section snippets

Animals

Experiments were performed on twelve adult (4–7 months old, weighing 180–210 g) and ten aged (28–31 months olds, weighing 185–300 g) female Wistar rats. Animals were obtained by breeding at our Institute of Gerontology. Each animal's estrous cycle was determined by monitoring vaginal smears. Adult rats showing regular estrous cycles of 5 days were used for experimentation on the day of diestrous. Aged rats showed persistent diestrous for 10 consecutive days of monitoring before the day of

Ovarian weight and morphology

Ovarian weights were measured in 5 adult and 5 aged animals, whose body weights were 193 ± 4.4 g and 290 ± 3.5 g, respectively (Fig. 1A). The average combined weight of both ovaries decreased from 58.1 ± 3.2 mg at 4–7 months of age to 48.6 ± 4.1 mg at 28–31 months of age (Fig. 1B), although this difference was not statistically significant. Histological examination showed that the adult rat ovary contained growing and mature follicles along with corpora lutea. Even in the aged ovary, a small number of

Discussion

This is the first study to demonstrate the effect of age upon ovarian nerves that regulate ovarian blood flow, with particular emphasis upon structure and function. Our results demonstrate that the ovarian nerves of both adult and aged rats contain mostly unmyelinated C fibers. In addition, we identified that (1) the number and size of unmyelinated C fibers in ovarian nerve, (2) the maximum conduction velocities of unmyelinated C fibers in ovarian nerve, and (3) the reduced response of ovarian

Acknowledgments

We are grateful to Ms. Chieko Kanai for her excellent technical assistance, to Ms. Yuka Okuno for her partial participation in the experiments, and particularly to Emeritus Professor Yuko Sato of the University of Human Arts and Sciences for her encouragement in the performance of this study. This work was supported by Grant-in-Aid for Scientific Research (Young Scientists B) to SU (No. 22790238).

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Number, size, conduction, and vasoconstrictor ability of unmyelinated fibers of the ovarian nerve in adult and aged rats

Abstract

Introduction

Section snippets

Animals

Ovarian weight and morphology

Discussion

Acknowledgments

Mech. Ageing Dev.

Neurosci. Lett.

J. Auton. Nerv. Syst.

Neurosci. Lett.

Neurosci. Lett.

Auton. Neurosci.

J. Auton. Nerv. Syst.

Auton. Neurosci.

The aging reproductive neuroendocrine axis

Steroids

The adrenergic innervation of mammalian ovaries

The sensory innervation of the ovary: a horseradish peroxidase study in the rat

Anat. Rec.

Characterization of the LH surge in middle-aged female rats

Biol. Reprod.

Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause

Hum. Reprod.

Ovarian and steroidal influences on neuroendocrine aging processes in female rodents

Endocr. Rev.

Noradrenaline content and release in male and female rat tail arteries

J. Cardiovasc. Pharmacol.

Age-related changes in adrenergic vasoconstrictor responses of the rat hindlimb

Am. J. Physiol.

An analysis of the axon populations in the nerves to the pelvic viscera in the rat

J. Comp. Neurol.