Organization of the Subdiaphragmatic Vagus Nerve and Its Connection with the Celiac Plexus and the Ovaries in the Female Rat

Overview

Journal Brain Sci

Publisher MDPI

Date 2023 Jul 29

PMID 37508964

Authors

Maria E Rivera-Castro

Cesar F Pastelin

Juan Bravo-Benitez

Carolina Moran

Affiliations

Soon will be listed here.

Abstract

Communication between the ovaries and the central nervous system occurs by peripheral innervation through the celiac plexus, superior ovarian nerve, and ovarian plexus nerve. The vagus nerve is involved in regulating the ovaries, but the neuroanatomical pathway that links them is not clear. Adult female rats were used for gross anatomy, acetylcholinesterase histochemistry, and the immunofluorescence analysis of tyrosine hydroxylase (TH), choline acetyltransferase (ChAT), and tryptophan hydroxylase 2 (TPH). The results obtained indicate that the right vagus nerve (RVN) travels parallel and caudal to the esophagus, where three nerve branches were identified. Also, a right vagal plexus (RVP) formed by microganglia was described, establishing communication with the celiac plexus, and was mainly reactive to tyrosine hydroxylase (TH); some serotoninergic and cholinergic neurons were also found. The left vagus nerve (LVN) travels over the esophagus, bifurcates before its insertion into the stomach and enters the RCG. This neuroanatomical and biochemical description of the RVN and LVN in the rat suggests the RVP is formed by presynaptic catecholaminergic terminals and cholinergic neurons. This information could support detailed studies of communication between the vagus nerve and the ovaries and identify the type of neural signaling involved in abdominal control of the vagus nerve.

Citing Articles

Can a Sacrococcygeal Epidural of 0.25% Bupivacaine Prevent the Activation of the Sympathetic Nervous System during Feline Ovariectomy?.

Martins J, Eliseu A, Campos S, Ribeiro L, Otero P, Cabral P Animals (Basel). 2024; 14(12).

PMID: 38929350 PMC: 11200459. DOI: 10.3390/ani14121732.

The role of the autonomic nervous system in polycystic ovary syndrome.

Yu Y, Chen T, Zheng Z, Jia F, Liao Y, Ren Y Front Endocrinol (Lausanne). 2024; 14:1295061.

PMID: 38313837 PMC: 10834786. DOI: 10.3389/fendo.2023.1295061.

References

Pastelin C, Rosas N, Morales-Ledesma L, Linares R, Dominguez R, Moran C . Anatomical organization and neural pathways of the ovarian plexus nerve in rats. J Ovarian Res. 2017; 10(1):18. PMC: 5351206. DOI: 10.1186/s13048-017-0311-x. View

Browning K, Verheijden S, Boeckxstaens G . The Vagus Nerve in Appetite Regulation, Mood, and Intestinal Inflammation. Gastroenterology. 2016; 152(4):730-744. PMC: 5337130. DOI: 10.1053/j.gastro.2016.10.046. View

ABERCROMBIE M . Estimation of nuclear population from microtome sections. Anat Rec. 2010; 94:239-47. DOI: 10.1002/ar.1090940210. View

Ojeda S, White S, Aguado L, Advis J, Andersen J . Abdominal vagotomy delays the onset of puberty and inhibits ovarian function in the female rat. Neuroendocrinology. 1983; 36(4):261-7. DOI: 10.1159/000123465. View

Baljet B, DRUKKER J . The extrinsic innervation of the abdominal organs in the female rat. Acta Anat (Basel). 1979; 104(3):243-67. DOI: 10.1159/000145073. View

Lawrence Jr I, Burden H . The origin of the extrinsic adrenergic innervation to the rat ovary. Anat Rec. 1980; 196(1):51-9. DOI: 10.1002/ar.1091960106. View

Morales L, Ricardo B, Bolanos A, Chavira R, Dominguez R . Ipsilateral vagotomy to unilaterally ovariectomized pre-pubertal rats modifies compensatory ovarian responses. Reprod Biol Endocrinol. 2007; 5:24. PMC: 1920514. DOI: 10.1186/1477-7827-5-24. View

Burden H, Leonard M, Smith C, Lawrence Jr I . The sensory innervation of the ovary: a horseradish peroxidase study in the rat. Anat Rec. 1983; 207(4):623-7. DOI: 10.1002/ar.1092070410. View

Gerendai I, Toth I, Boldogkoi Z, Medveczky I, Halasz B . CNS structures presumably involved in vagal control of ovarian function. J Auton Nerv Syst. 2000; 80(1-2):40-5. DOI: 10.1016/s0165-1838(00)00071-0. View

10.

Linares R, Hernandez D, Moran C, Chavira R, Cardenas M, Dominguez R . Unilateral or bilateral vagotomy induces ovulation in both ovaries of rats with polycystic ovarian syndrome. Reprod Biol Endocrinol. 2013; 11:68. PMC: 3722028. DOI: 10.1186/1477-7827-11-68. View

11.

Lara H, Dissen G, Leyton V, Paredes A, Fuenzalida H, Fiedler J . An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat. Endocrinology. 2000; 141(3):1059-72. DOI: 10.1210/endo.141.3.7395. View

12.

Burden H, Leonard M, Hodson C, Louis T, Lawrence Jr I . Effect of abdominal vagotomy at proestrus on ovarian weight, ovarian antral follicles, and serum levels of gonadotropins, estradiol, and testosterone in the rat. Neuroendocrinology. 1986; 42(6):449-55. DOI: 10.1159/000124486. View

13.

Morales L, Chavez R, Ayala M, Dominguez R . Effects of unilateral or bilateral superior ovarian nerve section in prepubertal rats on the ovulatory response to gonadotrophin administration. J Endocrinol. 1998; 158(2):213-9. DOI: 10.1677/joe.0.1580213. View

14.

Agrawal R, Kakkar N, Vasishta R, Kumari V, Samujh R, Rao K . Acetylcholinesterase histochemistry (AChE)--A helpful technique in the diagnosis and in aiding the operative procedures of Hirschsprung disease. Diagn Pathol. 2015; 10:208. PMC: 4668621. DOI: 10.1186/s13000-015-0443-5. View

15.

Deitch A, MOSES M . The Nissl substance of living and fixed spinal ganglion cells. II. An ultraviolet absorption study. J Biophys Biochem Cytol. 1957; 3(3):449-56. PMC: 2224041. DOI: 10.1083/jcb.3.3.449. View

16.

JACKSON R . Anatomy of the vagus nerves in the region of the lower esophagus and the stomach. Anat Rec. 1949; 103(1):1-18. DOI: 10.1002/ar.1091030102. View

17.

Fox E . Vagal afferent controls of feeding: a possible role for gastrointestinal BDNF. Clin Auton Res. 2012; 23(1):15-31. DOI: 10.1007/s10286-012-0170-x. View

18.

de Lartigue G . Role of the vagus nerve in the development and treatment of diet-induced obesity. J Physiol. 2016; 594(20):5791-5815. PMC: 5063945. DOI: 10.1113/JP271538. View

19.

Murray K, Rude K, Sladek J, Reardon C . Divergence of neuroimmune circuits activated by afferent and efferent vagal nerve stimulation in the regulation of inflammation. J Physiol. 2021; 599(7):2075-2084. PMC: 8016722. DOI: 10.1113/JP281189. View

20.

Vieyra E, Garcia J, Zarco H, Linares R, Rosas G, Ramirez D . Suprachiasmatic nucleus and vagus nerve trigger preovulatory LH and ovulation. Reproduction. 2022; 165(2):147-157. DOI: 10.1530/REP-22-0119. View