Skip to main content
Gut logoLink to Gut
. 1995 Nov;37(5):603–609. doi: 10.1136/gut.37.5.603

Oesophageal sensation assessed by electrical stimuli and brain evoked potentials--a new model for visceral nociception.

O Frøbert 1, L Arendt-Nielsen 1, P Bak 1, P Funch-Jensen 1, J P Bagger 1
PMCID: PMC1382861  PMID: 8549932

Abstract

Sensory thresholds and brain evoked potentials were determined in 12 healthy volunteers using electrical stimulation of the oesophagus 28 and 38 cm from the nares. The peaks of the evoked potentials were designated N for negative deflections and P for positive. Continuous electrical stimulation (40 Hz) at the 38 cm position resembled heartburn (five of 12 subjects) while non-specific ('electrical') sensations were provoked at 28 cm (10 of 12). Thresholds of sensation and of pain were lower at the initial than the second determination, but did not differ with respect to stimulation site. The pain summation threshold to repeated stimuli (2 Hz, 5 stimuli) was determined for the first time in a viscus. This threshold was lower than the pain threshold to single stimuli at 38 cm (p < 0.02). Evoked potential latencies did not change significantly over a six month period while the N1/P2 amplitude was higher at the first measurement (p < 0.05). P1 and N1 latencies were significantly shorter 38 cm (medians 100 and 141 ms) than 28 cm from the nares (102 and 148 ms) (p = 0.04 and p = 0.008). Electrical stimulation of the oesophagus may serve as a human experimental model for visceral pain. Longer evoked potential latencies from the proximal compared with distal stimulations provide new information about the sensory pathways of the oesophagus.

Full text

PDF
605

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andrews P. L. Vagal afferent innervation of the gastrointestinal tract. Prog Brain Res. 1986;67:65–86. doi: 10.1016/s0079-6123(08)62757-0. [DOI] [PubMed] [Google Scholar]
  2. Arendt-Nielsen L., Bjerring P. Selective averaging of argon laser induced pre-pain and pain related cortical responses. J Neurosci Methods. 1988 Jun;24(2):117–123. doi: 10.1016/0165-0270(88)90054-4. [DOI] [PubMed] [Google Scholar]
  3. Arendt-Nielsen L. First pain event related potentials to argon laser stimuli: recording and quantification. J Neurol Neurosurg Psychiatry. 1990 May;53(5):398–404. doi: 10.1136/jnnp.53.5.398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barish C. F., Castell D. O., Richter J. E. Graded esophageal balloon distention. A new provocative test for noncardiac chest pain. Dig Dis Sci. 1986 Dec;31(12):1292–1298. doi: 10.1007/BF01299805. [DOI] [PubMed] [Google Scholar]
  5. Bland J. M., Altman D. G. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986 Feb 8;1(8476):307–310. [PubMed] [Google Scholar]
  6. Breumelhof R., Nadorp J. H., Akkermans L. M., Smout A. J. Analysis of 24-hour esophageal pressure and pH data in unselected patients with noncardiac chest pain. Gastroenterology. 1990 Nov;99(5):1257–1264. doi: 10.1016/0016-5085(90)91147-x. [DOI] [PubMed] [Google Scholar]
  7. Buchsbaum M. S., Davis G. C., Bunney W. E., Jr Naloxone alters pain perception and somatosensory evoked potentials in normal subjects. Nature. 1977 Dec 15;270(5638):620–622. doi: 10.1038/270620a0. [DOI] [PubMed] [Google Scholar]
  8. Burack B., Furman S. Transesophageal cardiac pacing. Am J Cardiol. 1969 Mar;23(3):469–472. doi: 10.1016/0002-9149(69)90530-x. [DOI] [PubMed] [Google Scholar]
  9. Cannon R. O., 3rd, Cattau E. L., Jr, Yakshe P. N., Maher K., Schenke W. H., Benjamin S. B., Epstein S. E. Coronary flow reserve, esophageal motility, and chest pain in patients with angiographically normal coronary arteries. Am J Med. 1990 Mar;88(3):217–222. doi: 10.1016/0002-9343(90)90145-4. [DOI] [PubMed] [Google Scholar]
  10. Castell D. O., Wood J. D., Frieling T., Wright F. S., Vieth R. F. Cerebral electrical potentials evoked by balloon distention of the human esophagus. Gastroenterology. 1990 Mar;98(3):662–666. doi: 10.1016/0016-5085(90)90286-a. [DOI] [PubMed] [Google Scholar]
  11. Chapman W. P., Jones C. M. VARIATIONS IN CUTANEOUS AND VISCERAL PAIN SENSITIVITY IN NORMAL SUBJECTS. J Clin Invest. 1944 Jan;23(1):81–91. doi: 10.1172/JCI101475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chauhan A., Petch M. C., Schofield P. M. Effect of oesophageal acid instillation on coronary blood flow. Lancet. 1993 May 22;341(8856):1309–1310. doi: 10.1016/0140-6736(93)90817-z. [DOI] [PubMed] [Google Scholar]
  13. Clouse R. E., McCord G. S., Lustman P. J., Edmundowicz S. A. Clinical correlates of abnormal sensitivity to intraesophageal balloon distension. Dig Dis Sci. 1991 Aug;36(8):1040–1045. doi: 10.1007/BF01297444. [DOI] [PubMed] [Google Scholar]
  14. DEBECKER J., DESMEDT J. E. LES POTENTIELS 'EVOQU'ES C'ER'EBRAUX ET LES POTENTIELS DE NERF SENSIBLE CHEZ L'HOMME. UTILISATION DE L'ORDINATEUR NUM'ERIQUE MNEMOTRON. Acta Neurol Psychiatr Belg. 1964 Dec;64:1212–1248. [PubMed] [Google Scholar]
  15. Davies H. A. Anginal pain of esophageal origin: clinical presentation, prevalence, and prognosis. Am J Med. 1992 May 27;92(5A):5S–10S. doi: 10.1016/0002-9343(92)80050-a. [DOI] [PubMed] [Google Scholar]
  16. De Caestecker J. S., Pryde A., Heading R. C. Comparison of intravenous edrophonium and oesophageal acid perfusion during oesophageal manometry in patients with non-cardiac chest pain. Gut. 1988 Aug;29(8):1029–1034. doi: 10.1136/gut.29.8.1029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. DeVault K. R., Beacham S., Streletz L. J., Castell D. O. Cerebral evoked potentials. A method of quantification of central nervous system response to esophageal pain. Dig Dis Sci. 1993 Dec;38(12):2241–2246. doi: 10.1007/BF01299903. [DOI] [PubMed] [Google Scholar]
  18. Deschner W. K., Maher K. A., Cattau E. L., Jr, Benjamin S. B. Prospective evaluation of high-dose bethanechol in investigation of esophageal chest pain. Dig Dis Sci. 1989 Nov;34(11):1656–1661. doi: 10.1007/BF01540040. [DOI] [PubMed] [Google Scholar]
  19. Eypasch E. P., DeMeester T. R., Klingman R. R., Stein H. J. Physiologic assessment and surgical management of diffuse esophageal spasm. J Thorac Cardiovasc Surg. 1992 Oct;104(4):859–869. [PubMed] [Google Scholar]
  20. Frieling T., Enck P., Wienbeck M. Cerebral responses evoked by electrical stimulation of the esophagus in normal subjects. Gastroenterology. 1989 Aug;97(2):475–478. doi: 10.1016/0016-5085(89)90087-5. [DOI] [PubMed] [Google Scholar]
  21. Frøbert O., Arendt-Nielsen L., Bak P., Andersen O. K., Funch-Jensen P., Bagger J. P. Electric stimulation of the esophageal mucosa. Perception and brain-evoked potentials. Scand J Gastroenterol. 1994 Sep;29(9):776–781. doi: 10.3109/00365529409092509. [DOI] [PubMed] [Google Scholar]
  22. Gayheart P. A., Gwirtz P. A., Bravenec J. S., Longlet N., Jones C. E. An alpha-adrenergic coronary constriction during esophageal distention in the dog. J Cardiovasc Pharmacol. 1991 May;17(5):747–753. doi: 10.1097/00005344-199105000-00009. [DOI] [PubMed] [Google Scholar]
  23. Hewson E. G., Dalton C. B., Richter J. E. Comparison of esophageal manometry, provocative testing, and ambulatory monitoring in patients with unexplained chest pain. Dig Dis Sci. 1990 Mar;35(3):302–309. doi: 10.1007/BF01537406. [DOI] [PubMed] [Google Scholar]
  24. London R. L., Ouyang A., Snape W. J., Jr, Goldberg S., Hirshfeld J. W., Jr, Cohen S. Provocation of esophageal pain by ergonovine or edrophonium. Gastroenterology. 1981 Jul;81(1):10–14. [PubMed] [Google Scholar]
  25. McNally E. M., Meyer E. C., Langendorf R. Elective countershock in unanesthetized patients with use of an esophageal electrode. Circulation. 1966 Jan;33(1):124–127. doi: 10.1161/01.cir.33.1.124. [DOI] [PubMed] [Google Scholar]
  26. Mellow M. H., Simpson A. G., Watt L., Schoolmeester L., Haye O. L. Esophageal acid perfusion in coronary artery disease. Induction of myocardial ischemia. Gastroenterology. 1983 Aug;85(2):306–312. [PubMed] [Google Scholar]
  27. Ness T. J., Gebhart G. F. Visceral pain: a review of experimental studies. Pain. 1990 May;41(2):167–234. doi: 10.1016/0304-3959(90)90021-5. [DOI] [PubMed] [Google Scholar]
  28. Polland W. S., Bloomfield A. L. EXPERIMENTAL REFERRED PAIN FROM THE GASTRO-INTESTINAL TRACT. PART I. THE ESOPHAGUS. J Clin Invest. 1931 Aug;10(3):435–452. doi: 10.1172/JCI100363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Price D. D., Hu J. W., Dubner R., Gracely R. H. Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. Pain. 1977 Feb;3(1):57–68. doi: 10.1016/0304-3959(77)90035-5. [DOI] [PubMed] [Google Scholar]
  30. Price D. D., McHaffie J. G., Larson M. A. Spatial summation of heat-induced pain: influence of stimulus area and spatial separation of stimuli on perceived pain sensation intensity and unpleasantness. J Neurophysiol. 1989 Dec;62(6):1270–1279. doi: 10.1152/jn.1989.62.6.1270. [DOI] [PubMed] [Google Scholar]
  31. Richter J. E., Barish C. F., Castell D. O. Abnormal sensory perception in patients with esophageal chest pain. Gastroenterology. 1986 Oct;91(4):845–852. doi: 10.1016/0016-5085(86)90685-2. [DOI] [PubMed] [Google Scholar]
  32. Rodrigo J., Hernández J., Vidal M. A., Pedrosa J. A. Vegetative innervation of the esophagus. II. Intraganglionic laminar endings. Acta Anat (Basel) 1975;92(1):79–100. doi: 10.1159/000144431. [DOI] [PubMed] [Google Scholar]
  33. SHAFIROFF B. G., LINDER J. Effects of external electrical pacemaker stimuli on the human heart. J Thorac Surg. 1957 Apr;33(4):544–550. [PubMed] [Google Scholar]
  34. Sengupta J. N., Saha J. K., Goyal R. K. Stimulus-response function studies of esophageal mechanosensitive nociceptors in sympathetic afferents of opossum. J Neurophysiol. 1990 Sep;64(3):796–812. doi: 10.1152/jn.1990.64.3.796. [DOI] [PubMed] [Google Scholar]
  35. Smout A. J., DeVore M. S., Castell D. O. Cerebral potentials evoked by esophageal distension in human. Am J Physiol. 1990 Dec;259(6 Pt 1):G955–G959. doi: 10.1152/ajpgi.1990.259.6.G955. [DOI] [PubMed] [Google Scholar]
  36. Smout A. J., DeVore M. S., Dalton C. B., Castell D. O. Cerebral potentials evoked by oesophageal distension in patients with non-cardiac chest pain. Gut. 1992 Mar;33(3):298–302. doi: 10.1136/gut.33.3.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stein H. J., DeMeester T. R., Eypasch E. P., Klingman R. R. Ambulatory 24-hour esophageal manometry in the evaluation of esophageal motor disorders and noncardiac chest pain. Surgery. 1991 Oct;110(4):753–763. [PubMed] [Google Scholar]
  38. Svensson P., Arendt-Nielsen L., Kaaber S., Bjerring P. Vertex potentials evoked by nociceptive laser stimulation of oral mucosa: a comparison of four stimulation paradigms. Anesth Pain Control Dent. 1992 Fall;1(4):222–228. [PubMed] [Google Scholar]
  39. Tougas G., Hudoba P., Fitzpatrick D., Hunt R. H., Upton A. R. Cerebral-evoked potential responses following direct vagal and esophageal electrical stimulation in humans. Am J Physiol. 1993 Mar;264(3 Pt 1):G486–G491. doi: 10.1152/ajpgi.1993.264.3.G486. [DOI] [PubMed] [Google Scholar]
  40. Valori R. M. Nutcracker, neurosis, or sampling bias? Gut. 1990 Jul;31(7):736–737. doi: 10.1136/gut.31.7.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wall P. D., Woolf C. J. Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat. J Physiol. 1984 Nov;356:443–458. doi: 10.1113/jphysiol.1984.sp015475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ward B. W., Wu W. C., Richter J. E., Hackshaw B. T., Castell D. O. Long-term follow-up of symptomatic status of patients with noncardiac chest pain: is diagnosis of esophageal etiology helpful? Am J Gastroenterol. 1987 Mar;82(3):215–218. [PubMed] [Google Scholar]
  43. Willer J. C. Influence de l'anticipation de la douleur sur les fréquences cardiaque et respiratoire et sur le réflexe nociceptif chez l'homme. Physiol Behav. 1975 Oct;15(5):411–415. doi: 10.1016/0031-9384(75)90206-1. [DOI] [PubMed] [Google Scholar]
  44. de Caestecker J. S., Pryde A., Heading R. C. Site and mechanism of pain perception with oesophageal balloon distension and intravenous edrophonium in patients with oesophageal chest pain. Gut. 1992 May;33(5):580–586. doi: 10.1136/gut.33.5.580. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Gut are provided here courtesy of BMJ Publishing Group

RESOURCES