Preganglionic fibers in the rat hypogastric nerve project bilaterally to pelvic ganglia

Abstract

Stimulation of the hypogastric nerve (HGN) often evokes bilateral responses in some pelvic organs. Retrograde labeling studies indicate that axons of postganglionic neurons often cross to the opposite side. However, there is little information available as to whether preganglionic fibers in the HGN have a contralateral projection to pelvic ganglia. A retrograde tracer was injected into the left major pelvic ganglion (MPG) in rats receiving various lesions of preganglionic nerves (HGN and pelvic nerve, PN). The lumbar spinal cord was then examined for location and number of dye-filled neurons. In a second approach, the incidence of synapto-physin immunoreactivity (SN-IR) perineuronal profiles (baskets) was examined in the MPG and in the accessory pelvic ganglia (APG) after nerve lesions. Labeled neuronal profiles were found in spinal cord nuclei (Lumbar 1-2) after dye injection of the MPG in animals with an intact contralateral HGN. Cutting both HGNs virtually eliminated dye labeling in the lumbar cord, as did severing commissural branches (CB) between pelvic ganglia (leaving the contralateral HGN intact). Some SN-IR baskets were found in the left APG when only the contralateral HGN was intact, but baskets were rare when all four preganglionic nerves were cut. It could not be determined whether the HGN projects to the contralateral MPG, since SN-IR baskets were numerous in the MPG even when all four nerves were cut. This study has shown that some preganglionic fibers in the HGN synapse on neurons in contralateral pelvic ganglia. Both the APG and MPG receive contralateral innervation, but it is likely that neurons in the APG are the primary target of this input. Thus, in addition to crossing postganglionic fibers, a portion of the bilateral control of pelvic tissues is accomplished by preganglionic fibers which target autonomic neurons in contralateral ganglia.

The soma and proximal dendrites of sympathetic preganglionic neurons innervating the major pelvic ganglion in female rats receive predominantly inhibitory inputs

“…Whole transverse sections were cut on a vibrating tissue slicer (Electron Microscopy Sciences, Fort Washington, PA, USA) at a thickness of 250 μm in ice-cold PBS. These sections were briefly analyzed in a Nikon E600 light microscope equipped for epifluorescent detection of FG through a UV filter, where we confirmed that the pattern of FG fluorescence in SPNs was consistent with previously published studies (Harji et al, 1998) of MPG injection, with no evidence of systemic tracer leakage. Sections were cut to isolate the IML and DCN nuclei for embedding, and then cryo-protected through a graded series of glycerol in PBS, and stored overnight at 4°C in a solution of 30% glycerol.…”

“…It is known that some of these neurons, contrary to the standard paradigm of sympathetic projections, actually extend their axons through the spinal chain ganglia and the inferior mesenteric ganglion without synapsing, as they are identifiable through application of retrograde tracers, such as horseradish peroxidase, to the transected stump of the hypogastric nerve (Nadelhaft and McKenna, 1987, Baron and Jänig, 1991). More recently, these neurons have also been traced through the injection of retrograde tracers such as cholera toxin subunit B (Hosoya et al, 1994, Llewellyn-Smith et al, 2005, Ranson et al, 2006) or Fluorogold (Harji et al, 1998, Chang and Havton, 2010) directly into the major pelvic ganglion (MPG) itself, where the parasympathetic preganglionic neurons (PPNs) in the lumbosacral spinal cord also project their axons via the pelvic nerve (Keast, 1995). …”

“…Likewise, SPNs that innervate pelvic ganglia are found principally in segments L1-L2, the caudal end of the spinal distribution of SPNs (Strack et al, 1988, Harji et al, 1998, Llewellyn-Smith et al, 2005), resulting in some overlap of innervation that would necessitate retrograde tracing studies in order to distinguish, in the spinal nuclei, the subpopulations innervating the inferior mesenteric ganglion from those innervating the MPG.…”

Neural Control of the Lower Urinary Tract

“…Ganglia on one side are interconnected by numerous fiber tracts and the majority of inputs from the spinal cord occur ipsilaterally. In addition in some species fiber connections between the right and left pelvic plexuses and the IMGs occur (220, 327, 622) and synaptic interactions between the right and left plexuses have been reported (257). The striated muscle of the external urethral sphincter (EUS) is directly innervated by axons originating from motoneurons in the spinal cord.…”

Physiological and pharmacological aspects of the vas deferens—an update

“…The vas is innervated by autonomic postganglionic nerve fibers originating primarily from neurons in pelvic ganglia, and to a lesser extent, from neurons in the caudal mesenteric ganglion and sympathetic chain ganglia, and also by sensory nerve fibers arising from dorsal root ganglia (Kaleczyc, 1998; Kihara et al, 1998; Burnstock and Verkhratsky, 2010). In rodents the hypogastric nerve provides bilateral innervation to the vas, and contractile responses can be elicited with hypogastric stimulation from either side (Kihara et al, 1996; Harji et al, 1998). …”