A study on preganglionic connections and possible viscerofugal projections from urinary bladder intramural ganglia to the caudal mesenteric ganglion in the pig

Abstract

The present study was designed to (1) ascertain the distribution and immunohistochemical characteristics of sympathetic preganglionic neurons supplying the caudal mesenteric ganglion (CaMG) and (2) verify the existence of viscerofugal projections from the urinary bladder trigone intramural ganglia (UBT‐IG) to the CaMG in female pigs (n = 6). Combined retrograde tracing and immunofluorescence methods were used. Injections of the neuronal tracer Fast Blue (FB) into the right CaMG revealed no retrogradely labelled (FB‐positive; FB+) nerve cells in the intramural ganglia; however, many FB+ neurons were found in the spinal cord sympathetic nuclei. Double‐labelling immunohistochemistry revealed that nearly all (99.4 ± 0.6%) retrogradely labelled neurons were cholinergic (choline acetyltransferase‐positive; ChAT+) in nature. Many FB+/ChAT+ perikarya stained positive for vesicular acetylcholine transporter (63.11 ± 5.34%), neuronal nitric oxide synthase (53.48 ± 9.62%) or cocaine‐ and amphetamine‐regulated transcript peptide (41.13 ± 4.77%). A small number of the retrogradely labelled cells revealed immunoreactivity for calcitonin gene‐related peptide (7.60 ± 1.34%) or pituitary adenylate cyclase‐activating polypeptide (4.57 ± 1.43%). The present study provides the first detailed information on the arrangement and chemical features of preganglionic neurons projecting to the porcine CaMG and, importantly, strong evidence suggesting the absence of viscerofugal projections from the UBT‐IG.

The distribution and chemical coding of urinary bladder trigone-projecting neurons in testicular and aorticorenal ganglia in male pigs

“…It has been well recognized so far that the innervation of the urinary bladder is supplied by three sets of peripheral nerves: sacral parasympathetic, thoracolumbar sympathetic [hypogastric nerves and prevertebral ganglia, including testicular (TG) and aorticorenal (ARG) ganglia] and sacral sensory ones. These pathways are a structural basis for reflexes, which either keep the bladder in a relaxed state, enabling urine storage at low intravesical pressure, or initiate bladder emptying by relaxing the outflow region and contracting the detrusor muscle (Pidsudko 2013, 2014, Lepiarczyk et al 2019.…”

The influence of castration on intramural neurons of the urinary bladder trigone in male pigs

“…The number of intramural neurons or ganglia in the UB also differs significantly among species; they are numerous in humans, domestic pigs, guinea pigs, cats, rabbits, and ferrets (Dixon et al, 1983; Fehér et al, 1979; Gabella, 1990; Gilpin et al, 1983; Lincoln & Burnstock, 1993; Pirker et al, 2005; Sann et al, 1998) but are absent in rats and mice (Gabella & Uvelius, 1990). Although the morpho‐functional organization of the intramural nerve circuits of UB does not seem to be as complex as that of the alimentary tract (e.g., at least in the pig, intramural ganglia in the bladder trigone do not send viscerofugal projections to the prevertebral ganglia; Lepiarczyk et al, 2019), an increasing body of evidence suggests that UB intramural ganglia (UBIG) should not be considered as simple relay stations for preganglionic impulses to the local target tissues. The presence of many adrenergic and cholinergic ganglion cells (also called “short neurons”) in the bladder wall allows the development of dense sympathetic and parasympathetic neuroterminal networks, respectively, and enables these neurons to establish local synaptic contacts, which implies that the sympathetic and parasympathetic pathways are closely interrelated and are mutually coordinated at this peripheral level (Elbadawi & Shenk, 1968; Elbadawi & Schenk, 1971a, 1971b; Fehér & Vajda, 1979; Gillespie et al, 2006; Rahnama'i et al, 2015).…”

“…Furthermore, UBIG are thought to be an important element of local circuits associated with micturition, and they also contribute to the unique triple sympathetic‐parasympathetic‐somatic innervation of the urethral rhabdosphincter (Alsaid et al, 2011; Elbadawi & Schenk, 1974; for review, see Bessede et al, 2017. In this context, it should be noted that the morpho‐functional arrangement of extramural postganglionic autonomic pathways to the UB, especially to the trigone area, is also relatively complex (Ragionieri et al, 2013; Russo et al, 2013; for review, see de Groat et al, 2015; Lepiarczyk et al, 2019).…”

Polish Journal of Veterinary Sciences

“…It has been well recognized so far that the innervation of the urinary bladder is supplied by three sets of peripheral nerves: sacral parasympathetic, thoracolumbar sympathetic (hypogastric nerves and prevertebral ganglia-, including testicular (TG) and aorticorenal (ARG) ganglia ) and sacral sensory nerves. These pathways are a structural basis for reflexes which either keep the bladder in a relaxed state, enabling urine storage at low intravesical pressure, or initiate bladder emptying by relaxing the outflow region and contracting the detrusor muscle (Pidsudko 2013, 2014, Lepiarczyk et al 2019).…”