Digestive Diseases and Sciences

, Volume 49, Issue 5, pp 729–737 | Cite as

Vagal Afferent Is Involved in Short-Pulse Gastric Electrical Stimulation in Rats

  • Jinsong Liu
  • Xian Qiao
  • J. D. Z Chen

Abstract

This study investigated the effect of gastric electrical stimulation (GES) on vagal activity and its possible vagal afferent-mediated mechanisms. Sixty rats implanted with gastric serosal electrodes were divided into six groups (control, vehicle, local capsaicin, perivagal capsaicin, systemic capsaicin, and vagotomy). GES with six sets of parameters was performed in the control group; and GES with one set of effective parameters was performed in the other five groups. Spectral analysis of heart rate variability was used to assess vagal activity. Regular gastric slow waves were recorded in the control rats with a frequency of 4.8 cycles/min. Vagotomy significantly reduced the frequency of the gastric slow wave but did not induce dysrhythmia. Capsaicin did not alter the gastric slow wave. Short-pulse (300-μsec) GES significantly increased vagal activity at a frequency four times the intrinsic slow-wave frequency. Stimulation at a lower frequency or with a long pulse (300 msec) had no effect on vagal activity. Vagotomy or capsaicin administered perivagally, systemically, or locally abolished the effect of GES on the vagal activity. GES with short but not long pulses is capable of altering vagal activity. This effect is mediated by capsaicin-sensitive vagal afferent fibers.

gastric electrical stimulation vagal activity afferent pathway 

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REFERENCES

  1. 1.
    Bellahsene BE, Lind CD, Schirmer BD, Updike OL, McCallum RW: Acceleration of gastric emptying with electrical stimulation in a canine model of gastroparesis. Am J Physiol 265(5, pt 1):G826–G834, 1992Google Scholar
  2. 2.
    Chen JD, Qian L, Ouyang H, Yin J: Gastric electrical stimulation with short pulses reduces vomiting but not dysrhythmias in dogs. Gastroenterology 124(2):401–409, 2003Google Scholar
  3. 3.
    McCallum RW, Chen JDZ, Lin ZY, Schirmer BD, Williams RD, Ross RA: Gastric pacing improves emptying and symptoms in patients with gastroparesis. Gastroenterology 114(3):456–461, 1998Google Scholar
  4. 4.
    Kelly KA: Pacing the gut. Gastroenterology 103(6):1967–1969, 1992Google Scholar
  5. 5.
    Abell T, McCallum R, Hicking M, Koch, K, Abrahamsson H, LeBlanc I, Lindberg G, Konturek J, Nowak T, Quigley EMM, Tougas G, Starkebaum W: Gastric electrical stimulation for medically refractory gastroparesis. Gastroenterology 125:421–428, 2003Google Scholar
  6. 6.
    Familoni BO, Abell TL, Nemoto D, Voeller G, Johnson B: Efficacy of electrical stimulation at frequencies higher than basal rate in canine stomach. Dig Dis Sci 42(5):892–897, 1997Google Scholar
  7. 7.
    Forster J, Sarosiek I, Delcore R, Lin Z, Raju GS, McCallum RW: Gastric pacing is a new surgical treatment for gastroparesis. Am J Surg 182(6):676–681, 2001Google Scholar
  8. 8.
    Qian LW, Lin XM, Chen JDZ: Normalization of atropine-induced postprandial dysrhythmias with gastric pacing. Am J Physiol 276(2, pt 1):G387–G392, 1999Google Scholar
  9. 9.
    Wang ZS, Qian LW, Ueno T, Chen JDZ: Mechanisms of various gastric electrical stimulations. Gastroenterology 118(Suppl 2):A669, 2000Google Scholar
  10. 10.
    De Boer RW, Karemaker JM, Strackee J: Relationships between short-term blood pressure fluctations and heart rate variability in resting subjects. I. Aspectral analysis approach. Med Biol Eng Comput 23(4):352–358, 1985Google Scholar
  11. 11.
    Pagani MF, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell'Orto S, Piccaluga E, Turiel M, Baselli G, Cerutti S, Malliani A: Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympathovagal interaction in man and conscious dog. Circ Res 59(2):178–193, 1986Google Scholar
  12. 12.
    Akselrod S, Gordon D, Madwed JB, Snidman NC, Shannon DC, Cohen RJ: Hemodynamic regulation: investigation by spectral analysis. Am J Physiol 249(4, pt 2):H867–H875, 1985Google Scholar
  13. 13.
    Rimoldi O, Pierini S, Ferrari A, Cerutti S, Pagani M, Malliani A: Analysis of short-term oscillations of R-R and arterial pressure in conscious dogs. Am J Physiol 258(4, pt 2):H967–H976, 1990Google Scholar
  14. 14.
    Holzer P. Capsaicin: Cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev 43(2):143–201, 1991Google Scholar
  15. 15.
    Chen JDZ, McCallum RW: Clinical applications of electrogastrography. Am J Gastroenterol 88(9):1324–1336, 1993Google Scholar
  16. 16.
    Hou XH, Yin JY, Pasricha PJ, Chen JD: Role of enteric nerves in the regulation and propagation of spontaneous and electrically “paced” gastric slow waves in rats. Gastroenterology 120(5):1479, 2001Google Scholar
  17. 17.
    Wang ZS, Chen JDZ: Robust ECG R-R wave detection using evolutionary-programming-based fuzzy inference system (EPFIS) and application to assessing brain-gut interaction. IEE Proc Sci Meas Technol 147(6):351–356, 2000Google Scholar
  18. 18.
    Lu CL, Zou XP, Orr WC, Chen JDZ: Postprandial changes of sympathovagal balance measured by heart rate variability. Dig Dis Sci 44(4):857–861, 1999Google Scholar
  19. 19.
    Kruger C, Kalenka A, Haunstetter A, Schweizer M, Maier C, Ruhle U, Ehmke H, Kubler W, Haass M: Baroreflex sensitivity and heart rate variability in conscious rats with myocardial infartion. Am J Physiol 273(5, pt 2):H2240–H2247, 1997Google Scholar
  20. 20.
    Gori T, Floras JS, Parker JD: Effects of nitroglycerin treatment on baroreflex sensitivity and short-term heart rate variability in humans. J Am Coll Cardiol 40(11):2000–2005, 2002Google Scholar
  21. 21.
    Matsunaga T, Harada T, Mitsui T, Inokuma M, Hashimoto M, Miyauchi M, Murano H, Shibutani Y: Spectral analysis of circadian rhythms in heart rate variability of dogs. Am J Vet Res 62(1):37–42, 2001Google Scholar
  22. 22.
    Tougas G, Spaziani R, Hollerbach S, Djuric V, Pang C, Upton AR, Fallen EL, Kamath MV: Cardiac autonomic function and oesophageal acid sensitivity in patients with non-cardiac chest pain. Gut 49(5):706–712, 2001Google Scholar
  23. 23.
    Ouyang H, Yin J, Wang Z, Pasricha PJ, Chen JD: Electroacupuncture accelerates gastric emptying in association with changes in vagal activity. Am J Physiol 282(2):G390–G396, 2002Google Scholar
  24. 24.
    Lu CL, Shidler N, Chen JD: Enhanced postprandial gastric myoelectrical activity after moderate-intensity exercise. Am J Gastroenterol 95(2):425–431, 2000Google Scholar
  25. 25.
    Cerutti C, Gustin MP, Paultre CZ, Lo M, Julien MLC, Vincent M, Sassard J: Autonomic nervous system and cardiovascular variability in rats: a spectral analysis approach. Am J Physiol 261(4, pt 2):H1292–H1299, 1991Google Scholar
  26. 26.
    Kuwahara M, Yayou K, Ishii K, Hashimoto S, Tsubone H, Sugano S: Power spectral analysis of heart rate variability as a new method for assessing autonomic activity in the rat. J Electrocardiol 27(4):333–337, 1994Google Scholar
  27. 27.
    Bielefeldt K, Bass P: Sodium channel blockers alter slow-wave frequency of the rat stomach in vivo. Digestion 48(1):43–50, 1991Google Scholar
  28. 28.
    De Lavernhe-Lemaire MC, Decaud-Laroche J, Boiron M, Thouvenot J: Gastroduodenal electric activity, in situ, during anesthesia and recovery. Study in chronic electrode-carrying rats. Arch Int Physiol Biochim 94(1):19–28, 1986Google Scholar
  29. 29.
    Chen JD, McCallum RW: Electrogastrography: Principles and applications. New York, Raven Press, 1993Google Scholar
  30. 30.
    Geldof H, van der Schee EJ, van Blankenstein M, Smout AJ, Akkermans LM: Effects of highly selective vagotomy on gastric myoelectrical activity. An electrogastrographic study. Dig Dis Sci 35(8):969–975, 1990Google Scholar
  31. 31.
    Stoddard CJ, Smalhwood RH, Duthie HL: Electrical arrhythmias in the human stomach. Gut 22(9):705–712, 1981Google Scholar
  32. 32.
    Aeberhard P, Bedi BS: Effects of proximal gastric vagotomy (PGV) followed by total vagotomy (TV) on postprandial and fasting myoelectrical activity of the canine stomach and duodenum. Gut 18(7):515–523, 1997Google Scholar
  33. 33.
    Shibata C, Sasaki I, Naito H, Ueno T, Matsuno S: Intragastric capsaicin stimulates motility of upper gut and proximal colon via diatinct pathways in conscious dogs. Dig Dis Sci 44(6):1083–1089, 1999Google Scholar
  34. 34.
    Gonzalez R, Dunkel R, Koletzko B, Schusdziarra V, Allescher HD: Effect of capsaicin-containing red pepper sauce suspension on upper gastrointestinal motility in healthy volunteers. Dig Dis Sci 43(6):1165–1171, 1998Google Scholar
  35. 35.
    Holzer HH, Raybould HE: Vagal and splanchnic sensory pathways mediate inhibition of gastric motility induced by duodenal distension. Am J Physiol 262(4, pt 1):G603–G608, 1992Google Scholar
  36. 36.
    Abell TL, Hocking M, McCallum RW, Koch K, Abrahamsson H, Blanc IL, Linderberg G, Konturek J, Novak T, Tougas GH: Gastric electrical stimulation for gastroparesis: A multicenter double blind cross over study, by the waves study group. Gastroenterology 118(Suppl 2):A393, 2000 (abstr)Google Scholar
  37. 37.
    Tack J, Coulie B, Van Cutsem E: The influence of gastric electrical stimulation on proximal gastric motor and sensory function in severe idiopathic gastroparesis. Gastroenterology 116(4):G4733, 1999Google Scholar
  38. 38.
    Dinh TT, Ritter S: Capsaicin induces neuronal degeneration in the brain and spinal cord of adult rats. Soc Neurosci Abstr 11:349, 1985Google Scholar
  39. 39.
    Helke CJ, Eskay RL: Capsaicin reduces substance P immunoreactivity in the lateral nucleus of the solitary tract and nodose ganglion. Peptides 6(Suppl 1):121–126, 1985Google Scholar
  40. 40.
    South EH, Ritter RC: Capsaicin application to central or peripheral vagal fibers attenuates CCK satiety. Peptides 9(3):601–612, 1988Google Scholar
  41. 41.
    Tougas G, Wang L: Pseudoaffective cardioautonomic responses to gastric distension in rats. Am J Physiol 227(1, pt 2):R272–R278, 1999Google Scholar
  42. 42.
    Erin N, Ercan F, Yegen BC, Arbak S, Okar I, Oktay S: Role of capsaicin-sensitive nerves in gastric and hepatic injury induced by cold-restraint stress. Dig Dis Sci 45(9):1889–1899, 2000Google Scholar
  43. 43.
    Bozkurt A, Oktar BK, Kurtel H, Alican I, Coskun T, Yegen BC: Capsaicin-sensitive vagal fibers and 5-HT-, gastrin releasing peptide-and cholecystokinin A-receptors are involved in distensioninduced inhibition of gastric emptying in the rat. Regulatory Pept 83(2-3):81–86, 1999Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Jinsong Liu
    • 1
  • Xian Qiao
    • 1
  • J. D. Z Chen
    • 1
  1. 1.The Division of GastroenterologyUniversity of Texas Medical BranchGalvestonUSA

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