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

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.

Levator ani muscle innervation: Anatomical study in human fetus

“…We used polyclonal antibodies against PS100, TH, VACHT, PMP22, and nNOS because of their validity. Indeed, we already demonstrated the internal validity with a high reproducibility . Moreover, external validity of these antibodies has been also demonstrated by others teams .…”

“…We have recently described dual autonomic (IHP) and somatic control (PN) of pelvic viscera with a communicating loop within the LAM . In the present study, we observed that lateral distal branches of the IHP innervated the medial part of the LAM.…”

“…These authors also showed a communicating branch between the PN and LAN . The PN is located below the LAM and is thought to supply only somatic impulses toward the perineum and external genital structures . But no PN function was assessed with immunolabeling.…”

“…Nevertheless, controversies exist on nerve distribution, nerve nature (somatic or autonomic), and participation of the PN) in LAM innervation. As previously described by our team, a dual somatic and autonomic innervation in rectum, urethra, and erectile bodies involving communicating neural loops within the LAM, autonomic contribution from the inferior hypogastric plexus in LAM innervation cannot be excluded. So far, no functional analysis of LAM innervation has been conducted.…”

Applied Anatomy of the Male Pelvis

“…Given the fi ne nature of these nerve branches however, traditional anatomical dissections are extremely challenging. An alternative technique using immunohistochemistry of serial sections with three-dimensional reconstruction identifi ed autonomic-somatic communications at three levels: proximal supralevator, intermediary intralevator and distal infralevator [ 59 ]. However, other studies have been unable to fi nd any such communications between pudendal and cavernosal nerves [ 60 ].…”