Innervation of the gallbladder: structure, neurochemical coding, and physiological properties of guinea pig gallbladder ganglia

Microsc Res Tech. 1997 Oct 1;39(1):1-13. doi: 10.1002/(SICI)1097-0029(19971001)39:1<1::AID-JEMT1>3.0.CO;2-R.

Abstract

The muscle and epithelial tissues of the gallbladder are regulated by a ganglionated plexus that lies within the wall of the organ. Although these ganglia are derived from the same set of precursor neural crest cells that colonize the gut, they exhibit structural, neurochemical and physiological characteristics that are distinct from the myenteric and submucous plexuses of the enteric nervous system. Structurally, the ganglionated plexus of the guinea pig gallbladder is comprised of small clusters of neurons that are located in the outer wall of the organ, between the serosa and underlying smooth muscle. The ganglia are encapsulated by a shell of fibroblasts and a basal lamina, and are devoid of collagen. Gallbladder neurons are rather simple in structure, consisting of a soma, a few short dendritic processes and one or two long axons. Results reported here indicate that all gallbladder neurons are probably cholinergic since they all express immunoreactivity for choline acetyltransferase. The majority of these neurons also express substance P, neuropeptide Y, and somatostatin, and a small remaining population of neurons express vasoactive intestinal peptide (VIP) immunoreactivity and NADPH-diaphorase enzymatic activity. We report here that NADPH-diaphorase activity, nitric oxide synthase immunoreactivity, and VIP immunoreactivity are expressed by the same neurons in the gallbladder. Physiological studies indicate that the ganglia of the gallbladder are the site of action of the following neurohumoral inputs: 1) all neurons receive nicotinic input from vagal preganglionic fibers; 2) norepinephrine released from sympathetic postganglionic fibers acts presynaptically on vagal terminals within gallbladder ganglia to decrease the release of acetylcholine from vagal terminals; 3) substance P and calcitonin gene-related peptide, which are co-expressed in sensory fibers, cause prolonged depolarizations of gallbladder neurons that resemble slow EPSPs; and 4) cholecystokinin (CCK) acts presynaptically within gallbladder ganglia to increase the release of acetylcholine from vagal terminals. Results reported here indicate that hormonal CCK can readily access gallbladder ganglia, since there is no evidence for a blood-ganglionic barrier in the gallbladder. Taken together, these results indicate that gallbladder ganglia are not simple relay stations, but rather sites of complex modulatory interactions that ultimately influence the functions of muscle and epithelial cells in the organ.

Publication types

  • Research Support, U.S. Gov't, P.H.S.
  • Review

MeSH terms

  • Acetylcholine / metabolism
  • Animals
  • Catecholamines / metabolism
  • Cholecystokinin / metabolism
  • Gallbladder / anatomy & histology
  • Gallbladder / innervation*
  • Gallbladder / ultrastructure
  • Ganglia / anatomy & histology*
  • Ganglia / metabolism
  • Ganglia / physiology*
  • Guinea Pigs
  • Immunohistochemistry
  • Microscopy, Electron
  • Neurons / physiology
  • Neuropeptides / metabolism
  • Nitric Oxide Synthase / metabolism

Substances

  • Catecholamines
  • Neuropeptides
  • Cholecystokinin
  • Nitric Oxide Synthase
  • Acetylcholine