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Neural interrelationships of autonomic ganglia from the pelvic region of male rats

Published:December 28, 2018DOI:https://doi.org/10.1016/j.autneu.2018.12.005

      Highlights

      • The pelvic plexus of the male rat is made of two major ganglia and three pairs of accessory ganglia.
      • The components of the pelvic plexus are anatomically interrelated through ipsilateral and contralateral commissural nerves.
      • The accessory ganglia represent around 25% of the postganglionic pelvic innervation.
      • Efferent nerves of the MPG present a topographical organization.

      Abstract

      The aims of the present study were to describe, in male rats, the anatomical organization of the major and accessory pelvic ganglia (MPG, AG; respectively), the interrelationship of the pelvic plexus components, and the morphometry of the pelvic postganglionic neurons. Anatomical, histochemical and histological studies were performed in anesthetized adult Wistar male rats. We found that the pelvic plexus consists of intricate neural circuits composed of two MPG, and three pairs of AG (AGI, AGII, AGIII) anatomically interrelated through ipsilateral and contralateral commissural nerves. Around 30 nerves emerge from each MPG and 17 from AGI and AGII. The MPG efferent nerves spread out preganglionic information to several pelvic organs controlling urinary, bowel, reproductive and sexual functions, while AG innervation is more regional, and it is confined to reproductive organs located in the rostral region of the urogenital tract. Both MPG and AG contain nerve fascicles, blood vessels, small intensely fluorescent cells, satellite cells and oval neuronal somata with one to three nucleoli. The soma area of AG neurons is larger than those of MPG neurons (p < 0.005). The MPG contains about 75% of the total pelvic postganglionic neurons. Our findings corroborated previous reports about MPG inputs, and add new information regarding pelvic ganglia efferent branches, AG neurons (number and morphometry), and neural interrelationship between the pelvic plexus components. This information will be useful in designing future studies about the role of pelvic innervation in the physiology and pathophysiology of pelvic functions.

      Graphical abstract

      Keywords

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      References

        • Carlstedt A.
        • Nordgren S.
        • Fasth S.
        • Appelgren L.
        • Hulten L.
        Sympathetic nervous influence on the internal anal sphincter and rectum in man.
        Int. J. Color. Dis. 1988; 3: 90-95
        • Carlstedt A.
        • Nordgren S.
        • Fasth S.
        • Hulten L.
        The influence of the pelvic nerves on anorectal motility in the cat.
        Acta Physiol. Scand. 1989; 135: 57-64
        • Coggeshall R.E.
        A consideration of neural counting methods.
        Trends Neurosci. 1992; 15: 9-13
        • Cruz Y.
        • Hernández-Plata I.
        • Lucio R.A.
        • Zempoalteca R.
        • Castelán F.
        • Martínez-Gómez M.
        Anatomical organization and somatic axonal components of the lumbosacral nerves in female rabbits.
        Neurourol. Urodyn. 2017; 36: 1749-1756
        • Dail W.G.
        • Trujillo D.
        • de la Rosa D.
        • Walton G.
        Autonomic innervation of reproductive organs: analysis of the neurons whose axons project in the main penile nerve in the pelvic plexus of the rat.
        Anat. Rec. 1989; 224: 94-101
        • Dail W.G.
        • Harji F.
        • Gonzales J.
        • Galindo R.
        Multiple vasodilator pathways from the pelvic plexus to the penis of the rat.
        Int. J. Impot. Res. 1999; 11: 277-285
        • de Groat W.C.
        • Griffiths D.
        • Yoshimura N.
        Neural control of the lower urinary tract.
        Compr. Physiol. 2015; 5: 327-396
        • Galindo R.
        • Barba V.
        • Dail W.G.
        The sensory branch of the pudendal nerve is the major route for adrenergic innervation of the penis in the rat.
        Anat. Rec. 1997; 247: 479-485
        • Greenwood D.
        • Coggeshall R.E.
        • Hulsebosch C.E.
        Sexual dimorphism in the numbers of neurons in the pelvic ganglia of adult rats.
        Brain Res. 1985; 340: 160-162
        • Hehemann M.
        • Choe S.
        • Kalmanek E.
        • Harrington D.
        • Stupp S.I.
        • McVary K.T.
        • Podlasek C.A.
        Pelvic and hypogastric nerves are injured in a rat prostatectomy model, contributing to development of stress urinary incontinence.
        Sci. Rep. 2018; 816432
        • Kaplan S.
        • Odacı E.
        • Canan S.
        • Önger M.E.
        • Aslan H.
        • Ünal B.
        The disector counting technique.
        Neuroquantology. 2012; 10: 44-53
        • Karnovsky M.J.
        • Roots L.
        A “direct-coloring” thiocholine method for cholinesterases.
        J. Histochem. Cytochem. 1964; 12: 219-221
        • Keast J.R.
        Location and peptide content of pelvic neurons supplying the muscle and lamina propria of the rat vas deferens.
        J. Auton. Nerv. Syst. 1992; 40: 1-11
        • Keast J.R.
        Visualization and immunohistochemical characterization of sympathetic and parasympathetic neurons in the male rat major pelvic ganglion.
        Neuroscience. 1995; 66: 655-662
        • Keast J.R.
        The autonomic nerve supply of male sex organs–an important target of circulating androgens.
        Behav. Brain Res. 1999; 105: 81-92
        • Keast J.R.
        Plasticity of pelvic autonomic ganglia and urogenital innervation.
        Int. Rev. Cytol. 2006; 248: 141-208
        • Keast J.R.
        • de Groat W.C.
        Immunohistochemical characterization of pelvic neurons which project to the bladder, colon, or penis in rats.
        J. Comp. Neurol. 1989; 288 (15): 387-400
        • Keast J.R.
        • Booth A.M.
        • de Groat W.C.
        Distribution of neurons in the major pelvic ganglion of the rat which supply the bladder, colon or penis.
        Cell Tissue Res. 1989; 256: 105-112
        • Kepper M.
        • Keast J.
        Immunohistochemical properties and spinal connections of pelvic autonomic neurons that innervate the rat prostate gland.
        Cell Tissue Res. 1995; 281: 533-542
        • Kepper M.E.
        • Keast J.R.
        Location, immunohistochemical features, and spinal connections of autonomic neurons innervating the rat seminal vesicles.
        Biol. Reprod. 1997; 57: 1164-1174
        • Kihara K.
        • de Groat W.C.
        Sympathetic efferent pathways projecting bilaterally to the vas deferens in the rat.
        Anat. Rec. 1997; 248: 291-299
        • Kihara K.
        • de Groat W.C.
        Sympathetic efferent pathways projecting to the bladder neck and proximal urethra in the rat.
        J. Auton. Nerv. Syst. 1997; 62: 134-142
        • Kolbeck S.C.
        • Steers W.D.
        Origin of neurons supplying the vas deferens of the rat.
        J. Urol. 1993; 149: 918-921
        • Langley J.N.
        • Anderson H.K.
        The innervation of the pelvic and adjoining viscera: part VII. Anatomical observations.
        J. Physiol. 1896; 20: 372-406
        • Langworthy O.R.
        Innervation of the pelvic organs of the rat.
        Investig. Urol. 1965; 2: 491-511
        • Li M.Z.
        • Masuko S.
        Target specific organization and neuron types of the dog pelvic ganglia: a retrograde-tracing and immunohistochemical study.
        Arch. Histol. Cytol. 2001; 64: 267-280
        • Lucio R.A.
        • Manzo J.
        • Martínez-Gómez M.
        • Sachs B.D.
        • Pacheco P.
        Participation of pelvic nerve branches in male rat copulatory behavior.
        Physiol. Behav. 1994; 55: 241-246
        • Luckensmeyer G.B.
        • Keast J.R.
        Projections from the prevertebral and major pelvic ganglia to the ileum and large intestine of the male rat.
        J. Auton. Nerv. Syst. 1994; 49: 247-259
        • Luckensmeyer G.B.
        • Keast J.R.
        Immunohistochemical characterisation of sympathetic and parasympathetic pelvic neurons projecting to the distal colon in the male rat.
        Cell Tissue Res. 1995; 281: 551-559
        • Luckensmeyer G.B.
        • Keast J.R.
        Projections of pelvic autonomic neurons within the lower bowel of the male rat: an anterograde labelling study.
        Neuroscience. 1998; 84: 263-280
        • Magnon C.
        • Hall S.J.
        • Lin J.
        • Xue X.
        • Gerber L.
        • Freedland S.J.
        • Frenette P.S.
        Autonomic nerve development contributes to prostate cancer progression.
        Science. 2013; 3411236361
        • Melvin J.E.
        • Hamill R.W.
        Gonadal hormone regulation of neurotransmitter synthesizing enzymes in the developing hypogastric ganglion.
        Brain Res. 1986; 383: 38-46
        • Melvin J.E.
        • McNeill T.H.
        • Hamill R.W.
        Biochemical and morphological effects of castration on the postorganizational development of the hypogastric ganglion.
        Brain Res. 1988; 466: 131-139
        • Pacheco P.
        • Martinez-Gomez M.
        • Whipple B.
        • Beyer C.
        • Komisaruk B.R.
        Somato-motor components of the pelvic and pudendal nerves of the female rat.
        Brain Res. 1989; 490: 85-94
        • Pastelín C.F.
        • Zempoalteca R.
        • Pacheco P.
        • Downie J.W.
        • Cruz Y.
        Sensory and somatomotor components of the “sensory branch” of the pudendal nerve in the male rat.
        Brain Res. 2008; 1222: 149-155
        • Pastelín C.F.
        • Pacheco P.
        • Camacho M.
        • Cruz Y.
        Another component of the pelvic plexus that innervates the penis in the rat.
        Urology. 2011; 78: e7-13
        • Purinton P.T.
        • Fletcher T.F.
        • Bradley W.E.
        Gross and light microscopic features of the pelvic plexus in the rat.
        Anat. Rec. 1973; 175: 697-705
        • Rauchenwald M.
        • Steers W.D.
        • Desjardins C.
        Efferent innervation of the rat testis.
        Biol. Reprod. 1995; 52: 1136-1143
        • Steers W.D.
        • Mallory B.
        • de Groat W.C.
        Electrophysiological study of neural activity in penile nerve of the rat.
        Am. J. Phys. 1988; 254: R989-1000
        • Sterio D.C.
        The unbiased estimation of number and sizes of arbitrary particles using the disector.
        J. Microsc. 1984; 134: 127-136
        • Taguchi K.
        • Tsukamoto T.
        • Murakami G.
        Anatomical studies of the autonomic nervous system in the human pelvis by the whole-mount staining method: left-right communicating nerves between bilateral pelvic plexuses.
        J. Urol. 1999; 161: 320-325