Sensory and Autonomic Neurons Project Both to the Smooth Retractor Penis and to the Striated Bulbospongiosus Muscles. Neurochemical Features of the Sympathetic Subset

Abstract

Aim of the present study was to verify, by means of double retrograde neuronal tracers technique, the hypothesis that a subpopulation of sensory and autonomic neurons send collateral axons to both smooth and striated genital muscles. We also wanted to define the neurochemical content of the eventually retrogradelly double labeled (RDL) neurons in the sympathetic trunk ganglia (STG). We used six intact pigs and we injected the tracer Diamidino Yellow (DY) in the smooth left retractor penis muscle (RPM) and the tracer Fast Blue (FB) in the striated left bulbospongiosus muscle (BSM). Rare (2 6 0.6) RDL neurons were found in the ipsilateral S2 spinal ganglion (SG), 220 6 42 in the ipsilateral STGs, from L3 to S3, 19 6 15 in the contralateral S1-S2 ones and 22 6 5 in the bilateral caudal mesenteric ganglia (CMG). The RDL neurons of the STG were IR for TH (85 6 13%), DbH (69 6 17%), NPY (69 6 23%), nNOS (60 6 11%), LENK (54 6 19%), VIP (53626%), SOM (40 6 8%), CGRP (34 6 12%), SP (31 6 16%), and VAChT (28 6 3%). Our research highlights the presence of sensory and sympathetic neurons with qualitatively different neurochemical content sending axons both to the smooth RPM and to the striated BSM of the pig. These RDL neurons are likely to project to the smooth vasal musculature to create the ideal physiological conditions in which these muscles can optimize the erectile function.

Clarification of the Innervation of the Bladder, External Urethral Sphincter and Clitoris: A Neuronal Tracing Study in Female Mongrel Hound Dogs

“…In all cases, the fascia of the end organs represented a barrier capable of preventing the spread of the tracers into the surrounding tissues. Histological examination of the end organs/structures confirmed this absence of dye outside of the injected tissues (data not shown), a finding that matches a previous report (Botti et al, ).…”

“…A preserved filling sensation in human subjects with complete cauda equina or lower conus lesions (Reitz, ) may also be the consequence of intact afferents traveling centrally on hypogastric, thoracic or lumbar splanchnic nerves (Kanai and Andersson, ). Postganglionic autonomic efferent projections to the penis, the homolog of the clitoris, have been reported in pigs extending from sympathetic trunk ganglia at L2‐S3 levels, with peak frequencies at L7 and S1 (Panu et al, ; Botti et al, ), and in caudal mesenteric ganglia after dye injections into retractor smooth muscles of the penis and striated bulbospongiosus muscles (Botti et al, ). This is the first study to report autonomic efferent innervation of the clitoris directly from intermediolateral lamina in S1‐S3 segments of the spinal cord.…”

“…We are hesitant to term these sacral autonomics as parasympathetic based on a recent study showing that sacral autonomic outflow had 15 phenotypic and ontogenetic features of thoracolumbar autonomic outflow, and may be best characterized as sympathetic (Espinosa‐Medina et al, ). Even if a new framework of autonomic function has to be considered in future studies, autonomic efferents to the clitoris are likely involved in the vasomotor regulation of muscle metabolism in pigs (Botti et al, ). The possibility of somatic innervation of bulbospongiosus striated muscles has also been reported in rat and pig penises (Schroder, ; Botti et al, ).…”

“…There are also thoracic and lumbar splanchnic nerves, that typically refer to preganglionic nerves extending from thoracic and lumbar spinal cord segments, respectively, to abdominal sympathetic ganglia, for example, caudal mesenteric ganglia. Sympathetic trunk ganglia are also known as sympathetic chain and paravertebral ganglia, while spinal ganglia (SG) have also been termed dorsal root ganglia in the literature (Panu et al, ; Botti et al, ). Some studies describe post‐ganglionic neurons of the bladder as located both in ganglia of the pelvic plexus and the bladder wall, yet name them together as pelvic plexus ganglia.…”

Immunohistochemical Properties of the Peripheral Neurons Projecting to the Pig Bulbospongiosus Muscle

“…Moreover, we used the pig as experimental animal because of its often use in biomedical investigations (Bossowska, ), including neuroanatomical studies (Kaleczyc et al, ; Majewski et al, ; Botti et al, ,b, , ; Ragionieri et al, ; Lepiarczyc et al, ,).…”