Effects of Autonomic Nerve Stimulation on Colorectal Motility in Rats

Overview

Journal Neurogastroenterol Motil

Specialties Gastroenterology
Neurology

Date 2010 Jan 14

PMID 20067587

Citations 27

Authors

W D Tong

T J Ridolfi

L Kosinski

K Ludwig

T Takahashi

Affiliations

Soon will be listed here.

Abstract

Background: Several disease processes of the colon and rectum, including constipation and incontinence, have been associated with abnormalities of the autonomic nervous system. However, the autonomic innervation to the colon and rectum are not fully understood. The aims of this study were to investigate the effect of stimulation of vagus nerves, pelvic nerves (PN) and hypogastric nerves (HGN) on colorectal motility in rats.

Methods: Four strain gauge transducers were implanted on the proximal colon, mid colon, distal colon and rectum to record circular muscle contractions in rats. Electrical stimulation was administered to the efferent distal ends of the cervical vagus nerve, PN and HGN. Motility index (MI) was evaluated before and during stimulation.

Key Results: Electrical stimulation (5-20 Hz) of the cervical vagus elicited significant contractions in the mid colon and distal colon, whereas less pronounced contractions were observed in the proximal colon. Pelvic nerves stimulation elicited significant contractions in the rectum as well as the mid colon and distal colon. Atropine treatment almost completely abolished the contractions induced by vagus nerve and PN stimulation. Hypogastric nerves stimulation caused relaxations in the rectum, mid colon and distal colon. The relaxations in response to HGN stimulation were abolished by propranolol.

Conclusions & Inferences: Vagal innervation extends to the distal colon, while the PN has projections in the distribution of the rectum through the mid colon. This suggests a pattern of dual parasympathetic innervation in the left colon. Parasympathetic fibers regulate colorectal contractions via muscarinic receptors. The HGN mainly regulates colorectal relaxations via beta-adrenoceptors.

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References

Garrett J, Howard E, Jones W . The internal anal sphincter in the cat: a study of nervous mechanisms affecting tone and reflex activity. J Physiol. 1974; 243(1):153-66. PMC: 1330694. DOI: 10.1113/jphysiol.1974.sp010747. View

Hulten L . Extrinsic nervous control of colonic motility and blood flow. An experimental study in the cat. Acta Physiol Scand Suppl. 1969; 335:1-116. View

Hedlund H, Fasth S, Hulten L . Efferent sympathetic nervous control of rectal motility in the cat. Acta Physiol Scand. 1984; 121(4):317-24. DOI: 10.1111/j.1748-1716.1984.tb07462.x. View

Hedlund H, Fandriks L, Delbro D, Fasth S . On the transmission of sacral parasympathetic nervous influence on distal colonic and rectal motility in the cat. Acta Physiol Scand. 1985; 125(2):225-34. DOI: 10.1111/j.1748-1716.1985.tb07711.x. View

Hirabayashi T, Matsufuji H, Yokoyama J, Hagane K, Hoshino K, Morikawa Y . Colorectal motility induction by sacral nerve electrostimulation in a canine model: implications for colonic pacing. Dis Colon Rectum. 2003; 46(6):809-17. DOI: 10.1007/s10350-004-6661-7. View

Carlstedt A, Fasth S, Hulten L, Nordgren S . The sympathetic innervation of the internal anal sphincter and rectum in the cat. Acta Physiol Scand. 1988; 133(3):423-31. DOI: 10.1111/j.1748-1716.1988.tb08425.x. View

Olsson C, Holmberg A, Holmgren S . Development of enteric and vagal innervation of the zebrafish (Danio rerio) gut. J Comp Neurol. 2008; 508(5):756-70. DOI: 10.1002/cne.21705. View

Bennett M . Rebound excitation of the smooth muscle cells of the guinea-pig taenia coli after stimulation of intramural inhibitory nerves. J Physiol. 1966; 185(1):124-31. PMC: 1395873. DOI: 10.1113/jphysiol.1966.sp007975. View

Maruyama S, Okabe S, Endo M, Sato K, Iwai T . The role of the rectal branches of pelvic plexus in defecation and colonic motility in a canine model. J Med Dent Sci. 2004; 50(4):275-84. View

10.

Altschuler S, Escardo J, Lynn R, Miselis R . The central organization of the vagus nerve innervating the colon of the rat. Gastroenterology. 1993; 104(2):502-9. DOI: 10.1016/0016-5085(93)90419-d. View

11.

GILLIS R, Dias Souza J, Hicks K, Mangel A, Pagani F, HAMILTON B . Inhibitory control of proximal colonic motility by the sympathetic nervous system. Am J Physiol. 1987; 253(4 Pt 1):G531-9. DOI: 10.1152/ajpgi.1987.253.4.G531. View

12.

Fasth S, Hulten L, Nordgren S . Evidence for a dual pelvic nerve influence on large bowel motility in the cat. J Physiol. 1980; 298:159-69. PMC: 1279108. DOI: 10.1113/jphysiol.1980.sp013073. View

13.

Ariga H, Imai K, Chen C, Mantyh C, Pappas T, Takahashi T . Fixed feeding potentiates interdigestive gastric motor activity in rats: importance of eating habits for maintaining interdigestive MMC. Am J Physiol Gastrointest Liver Physiol. 2008; 294(3):G655-9. DOI: 10.1152/ajpgi.00484.2007. View

14.

Dorofeeva A, Panteleev S, Makarov F . Involvement of the sacral parasympathetic nucleus in the innervation of the descending colon and rectum in cats. Neurosci Behav Physiol. 2009; 39(2):207-10. DOI: 10.1007/s11055-009-9104-z. View

15.

Takahashi T, Owyang C . Regional differences in the nitrergic innervation between the proximal and the distal colon in rats. Gastroenterology. 1998; 115(6):1504-12. DOI: 10.1016/s0016-5085(98)70029-0. View

16.

Dapoigny M, Cowles V, Zhu Y, Condon R . Vagal influence on colonic motor activity in conscious nonhuman primates. Am J Physiol. 1992; 262(2 Pt 1):G231-6. DOI: 10.1152/ajpgi.1992.262.2.G231. View

17.

Takaki M, Neya T, Nakayama S . Sympathetic activity in the recto-rectal reflex of the guinea pig. Pflugers Arch. 1980; 388(1):45-52. DOI: 10.1007/BF00582627. View

18.

Neya T, Takaki M, Nakayama S . Mechanism of rectal contraction mediated by sympathetic efferents from rectoanal pelvic afferents in guinea pigs. Acta Med Okayama. 1984; 38(1):21-7. DOI: 10.18926/AMO/30367. View

19.

Venkova K, Krier J . Stimulation of lumbar sympathetic nerves evokes contractions of cat colon circular muscle mediated by ATP and noradrenaline. Br J Pharmacol. 1993; 110(3):1260-70. PMC: 2175786. DOI: 10.1111/j.1476-5381.1993.tb13951.x. View

20.

Devroede G, Lamarche J . Functional importance of extrinsic parasympathetic innervation to the distal colon and rectum in man. Gastroenterology. 1974; 66(2):273-80. View