Autonomic-somatic communications in the human pelvis: computer-assisted anatomic dissection in male and female fetuses

Bayan Alsaid, David Moszkowicz, Frédérique Peschaud, Thomas Bessede, Mazen Zaitouna, Ibrahim Karam, Stéphane Droupy, Gérard Benoit, Bayan Alsaid, David Moszkowicz, Frédérique Peschaud, Thomas Bessede, Mazen Zaitouna, Ibrahim Karam, Stéphane Droupy, Gérard Benoit

Abstract

Sphincter continence and sexual function require co-ordinated activity of autonomic and somatic neural pathways, which communicate at several levels in the human pelvis. However, classical dissection approaches are only of limited value for the determination and examination of thin nerve fibres belonging to autonomic supralevator and somatic infralevator pathways. In this study, we aimed to identify the location and nature of communications between these two pathways by combining specific neuronal immunohistochemical staining and three-dimensional reconstruction imaging. We studied 14 normal human fetal pelvic specimens (seven male and seven female, 15-31 weeks' gestation) by three-dimensional computer-assisted anatomic dissection (CAAD) with neural, nitrergic and myelin sheath markers. We determined the precise location and distribution of both the supra- and infralevator neural pathways, for which we provide a three-dimensional presentation. We found that the two pathways crossed each other distally in an X-shaped area in two spatial planes. They yielded dual innervation to five targets: the anal sphincter, levator ani muscles, urethral sphincter, corpus spongiosum and perineal muscles, and corpora cavernosa. The two pathways communicated at three levels: proximal supralevator, intermediary intralevator and distal infralevator. The dorsal penis/clitoris nerve (DN) had segmental nitrergic activity. The proximal DN was nNOS-negative, whereas the distal DN was nNOS-positive. Distal communication was found to involve interaction of the autonomic nitrergic cavernous nerves with somatic nitrergic branches of the DN, with nitrergic activity carried in the distal part of the nerve. In conclusion, the pelvic structures responsible for sphincter continence and sexual function receive dual innervation from the autonomic supralevator and the somatic infralevator pathways. These two pathways displayed proximal, intermediate and distal communication. The distal communication between the CN and branches of the DN extended nitrergic activity to the distal part of the cavernous bodies in fetuses of both sexes. These structures are important for erectile function, and care should therefore be taken to conserve this communication during reconstructive surgery.

© 2011 The Authors. Journal of Anatomy © 2011 Anatomical Society of Great Britain and Ireland.

Figures

Fig. 1
Fig. 1
(A,B) Three-dimensional computer-assisted anatomic dissection from transverse immunolabelled histological sections of a 15-week-old male fetus. (A) Lateral view of intrapelvic organs showing the infralevator neural pathways of the pudendal nerve (PN) behind the levator ani muscles (LAM) and its terminal branch [dorsal nerve of the penis (DNP)]. (B) Same view with transparency of the LAM, showing the distal distribution of the inferior hypogastric (pelvic) plexus (IHP), in three directions: postero-inferior for the anal sphincter, lateral for the LAM, and anterior-inferior for the neurovascular bundles (NVB), which travel posterolaterally to the prostate (P), nerve fibres from the NVB forming three projections: anterior for the urethral sphincter (US), antero-lateral cavernous nerve (CN) for the corpora cavernosa (CC) and postero-lateral spongious nerves (SN) for the corpus spongiosum (CS). (C) Same lateral view with the two pathways, (D) Schematic diagram of the supra- and infralevator pathways. These two pathways ensure the dual innervation of five targets: (1) anal sphincter (AS); (2) LAM; (3) urethral sphincter (US); (4) CS and perineal muscles; and (5) CC. Communications between the two pathways occurred at three levels (blue arrow in D): proximal communication, intralevator communication (IC) and distal communication (DC). The two pathways crossed distally in an X-shaped area in two spatial planes (cycle in C,D).
Fig. 2
Fig. 2
Serial transverse sections of 21-week-old female (A,B) and 20-week-old male (C,D) fetuses, at 150-μm intervals, immuno-stained with antibody against S100 and scanned at an optical resolution of 4800 dpi, showing the microscopic (×4) appearance of the nerve fibres (frame in A,B). (E) Three-dimensional computer-assisted anatomic dissection from transverse immuno-labelled histological sections of the male fetus showing the two levels of section in (C,D). Nerve fibres leave the pudendal nerve (PN) (A,C arrowhead) to reach the inferior hypogastric (pelvic) plexus (IHP) via the lateral face of its posterior portion (B,D arrowhead) (SN, sciatic nerve).
Fig. 3
Fig. 3
(A,B) Microscopic appearance (×4) of serial transverse sections of 15-week-old male fetus (50-μm intervals) at the level of membranous urethra, immuno-stained with antibody against S100. (C) Three-dimensional computer-assisted anatomic dissection showing the two levels of section in (A,B). Nerve fibres from the inferior hypogastric (pelvic) plexus (IHP) travelled distally in the levator ani muscles; some fibres (arrowhead in A) cross the lower border of the muscle in the direction of the pudendal pedicle (Pud. Ped.) (arrowhead in B).
Fig. 4
Fig. 4
(A,E) Transverse sections at the level of ischiopubic root (IPR), showing the clitoris and the penile hilum in 26-week-old female and 20-week-old-male fetuses, respectively. Sections immunostained with antibody against S100 and scanned at an optical resolution of 4800 dpi. Microscopic appearance of the dorsal nerve of the clitoris (DNC) in B (from inset in A) and dorsal nerve of the penis (DNP) in (F) (from inset in E) and their surrounding nerve fibres, treated with an antibody against nitrergic fibres (anti-nNOS) (in C and G) and an antibody against the myelin sheath (anti-PMP22) (in D and H). At the proximal part of the corpora cavernosa (CC) in both sexes, nerve fibres branching from the DN (back arrow in B, F) had strong nitrergic activity (white arrowhead in C, G) in both sexes. The proximal portion of the DN had no nitrergic activity at this level (white star in C, G). These branches were somatic (PMP22+, black arrow in D,H) and had the same somatic nature as DN (PMP22+, black star in D,H). The cavernous nerves (CN) directed to the corpora cavernosa (CC) were strongly nitrergic (black bold arrow in C,G) and autonomic and non-myelinated in nature (PMP22−, white bold arrow in D,H).
Fig. 5
Fig. 5
(A,D) Schematic diagrams of pelvic transverse sections at the ischio-pubic root (IPR) in female and male fetuses, (B,C) Serial transverse sections of 26-week-old female fetuses at the level of the clitoris hilum (frame in A) immuno-stained with antibody against S100 in (B) and antibody against nNOS in (C) and scanned at an optical resolution of 4800 dpi. (E–H) Microscopic appearance (×10) of the dorsal nerve of the penis (DNP) in 20-week-old-male fetuses; proximal portion near the penile hilum (black frame in D) and distal portion in the penis (grey frame in D), immuno-stained with antibody against S100 in (E,G) and antibody against nNOS in (F,H). The cavernous nerves (CN) travel antero-lateral to the urethra (U) and reach the corpora cavernosa (CC). CN gave a positive signal with anti-nNOS antibodies in both sexes (black arrow in C,F), The somatic dorsal nerve of the clitoris (DNC) and the DNP had segmental nitrergic activity and their proximal portions were negative for nNOS (white arrowhead in C,F), with parietal anti-nNOS staining observed in the distal portions (black arrowhead in C,H).
Fig. 6
Fig. 6
(A) Computer-assisted anatomical dissection (CAAD) of the pelvic structure with pubis transparency in a 26-week-old female fetus, shown in antero-lateral view. (B) Zoomed view (frame in A) without the bone. (C) Same view with nerve fibre transparency, with nitrergic nerve fibres shown in pink. The distal branches from the inferior hypogastric (pelvic) plexus (IHP) formed the neurovascular bundles (NVB). Some nerve fibres converged in an anterior position to innervate the urethral sphincter (US). The NVB continued its postero-lateral course to the vagina, to reach the corpus spongiosum vestibular bulb via the spongious nerves (SN). The cavernous nerves (CN) travelled anterolaterally to the vagina (V) and reached the corpora cavernosa of the clitoris (C). All the CN fibres were nitrergic. The pudendal nerve (PN) became the dorsal nerve of the clitoris (DNC), which had segmental nitrergic activity, with a non-nitrergic proximal portion (white arrowhead in C) and a nitrergic distal portion (black arrowhead in C). The change in the nitrergic nature of the DN related to the DNC branches (black arrow in B,C), which interacted with the nitrergic CN and carried the nitrergic activity to the DN. This interaction occurred in the X-shaped region of communication between the infra- and supralevator pathways.

References

    1. Acimi S. Clitoroplasty: a variant of the technique. Urology. 2008;72:669–671.
    1. Alsaid B, Bessede T, Karam I, et al. Coexistence of adrenergic and cholinergic nerves in the inferior hypogastric plexus: anatomical and immunohistochemical study with 3D reconstruction in human male fetus. J Anat. 2009;214:645–654.
    1. Alsaid B, Bessede T, Diallo D, et al. Division of autonomic nerves within the neurovascular bundles distally into corpora cavernosa and corpus spongiosum components: immunohistochemical confirmation with three-dimensional reconstruction. Eur Urol. 2011;59:902–909.
    1. Arango-Toro O, Domenech-Mateu JM. Development of the pelvic plexus in human embryos and fetuses and its relationship with the pelvic viscera. Eur J Morphol. 1993;31:193–208.
    1. Baader B, Herrmann M. Topography of the pelvic autonomic nervous system and its potential impact on surgical intervention in the pelvis. Clin Anat. 2003;16:119–130.
    1. Baizer JS, Broussard DM. Expression of calcium-binding proteins and nNOS in the human vestibular and precerebellar brainstem. J Comp Neurol. 2010;518:872–895.
    1. Barber MD, Bremer RE, Thor KB, et al. Innervation of the female levator ani muscles. Am J Obstet Gynecol. 2002;187:64–71.
    1. Benoit G, Droupy S, Quillard J, et al. Supra and infralevator neurovascular pathways to the penile corpora cavernosa. J Anat. 1999;195(Pt 4):605–615.
    1. Bernstein AJ, Peters KM. Expanding indications for neuromodulation. Urol Clin North Am. 2005;32:59–63.
    1. Bremer J, Baumann F, Tiberi C, et al. Axonal prion protein is required for peripheral myelin maintenance. Nat Neurosci. 2010;13:310–318.
    1. Burnett AL, Lowenstein CJ, Bredt DS, et al. Nitric oxide: a physiologic mediator of penile erection. Science. 1992;257:401–403.
    1. Colleselli K, Stenzl A, Eder R, et al. The female urethral sphincter: a morphological and topographical study. J Urol. 1998;160:49–54.
    1. Colombel M, Droupy S, Paradis V, et al. Caverno-pudendal nervous communicating branches in the penile hilum. Surg Radiol Anat. 1999;21:273–276.
    1. Costello AJ, Brooks M, Cole OJ. Anatomical studies of the neurovascular bundle and cavernosal nerves. Br J Urol Int. 2004;94:1071–1076.
    1. Fritsch H. Topography of the pelvic autonomic nerves in human fetuses between 21-29 weeks of gestation. Anat Embryol (Berl) 1989;180:57–64.
    1. Hern WM. Correlation of fetal age and measurements between 10 and 26 weeks of gestation. Obstet Gynecol. 1984;63:26–32.
    1. Hoyle CH, Stones RW, Robson T, et al. Innervation of vasculature and microvasculature of the human vagina by NOS and neuropeptide-containing nerves. J Anat. 1996;188(Pt 3):633–644.
    1. Junemann KP, Schmidt RA, Melchior H, et al. Neuroanatomy and clinical significance of the external urethral sphincter. Urol Int. 1987;42:132–136.
    1. Karam I, Moudouni S, Droupy S, et al. The structure and innervation of the male urethra: histological and immunohistochemical studies with three-dimensional reconstruction. J Anat. 2005;206:395–403.
    1. Leng WW, Chancellor MB. How sacral nerve stimulation neuromodulation works. Urol Clin North Am. 2005;32:11–18.
    1. Lombardi G, Mondaini N, Giubilei G, et al. Sacral neuromodulation for lower urinary tract dysfunction and impact on erectile function. J Sex Med. 2008;5:2135–2140.
    1. Martin-Alguacil N, Pfaff DW, Shelley DN, et al. Clitoral sexual arousal: an immunocytochemical and innervation study of the clitoris. BJU Int. 2008a;101:1407–1413.
    1. Martin-Alguacil N, Schober J, Kow LM, et al. Oestrogen receptor expression and neuronal nitric oxide synthase in the clitoris and preputial gland structures of mice. Br J Urol Int. 2008b;102:1719–1723.
    1. Mauroy B, Bizet B, Bonnal JL, et al. Systematization of the vesical and uterovaginal efferences of the female inferior hypogastric plexus (pelvic): applications to pelvic surgery on women patients. Surg Radiol Anat. 2007a;29:209–217.
    1. Mauroy B, Demondion X, Bizet B, et al. The female inferior hypogastric ( = pelvic) plexus: anatomical and radiological description of the plexus and its afferences – applications to pelvic surgery. Surg Radiol Anat. 2007b;29:55–66.
    1. Moszkowicz D, Alsaid B, Bessede T, et al. Female pelvic autonomic neuroanatomy based on conventional macroscopic and computer-assisted anatomic dissections. Surg Radiol Anat. 2011a;33:397–404.
    1. Moszkowicz D, Alsaid B, Bessede T, et al. Neural supply to the clitoris: immunohistochemical study with three-dimensional reconstruction of cavernous nerve, spongious nerve, and dorsal clitoris nerve in human fetus. J Sex Med. 2011b;8:1112–1122.
    1. Narayan P, Konety B, Aslam K, et al. Neuroanatomy of the external urethral sphincter: implications for urinary continence preservation during radical prostate surgery. J Urol. 1995;153:337–341.
    1. Paick JS, Donatucci CF, Lue TF. Anatomy of cavernous nerves distal to prostate: microdissection study in adult male cadavers. Urology. 1993;42:145–149.
    1. Pauls RN, Marinkovic SP, Silva WA, et al. Effects of sacral neuromodulation on female sexual function. Int Urogynecol J Pelvic Floor Dysfunct. 2007;18:391–395.
    1. Roberts WH, Harrison CWS, Mitchell DAJ, et al. The levator ani muscle and the nerve supply of its puborectalis component. Clin Anat. 1988;1:267–283.
    1. Shafik A, el-Sherif M, Youssef A, et al. Surgical anatomy of the pudendal nerve and its clinical implications. Clin Anat. 1995;8:110–115.
    1. Snipes GJ, Suter U, Welcher AA, et al. Characterization of a novel peripheral nervous system myelin protein (PMP-22/SR13) J Cell Biol. 1992;117:225–238.
    1. Wallner C, van Wissen J, Maas CP, et al. The contribution of the levator ani nerve and the pudendal nerve to the innervation of the levator ani muscles; a study in human fetuses. Eur Urol. 2008;54:1136–1142.
    1. Yucel S, Baskin LS. Identification of communicating branches among the dorsal, perineal and cavernous nerves of the penis. J Urol. 2003;170:153–158.
    1. Yucel S, De Souza A, Jr, Baskin LS. Neuroanatomy of the human female lower urogenital tract. J Urol. 2004;172:191–195.

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