Digestive Diseases and Sciences

, Volume 43, Issue 11, pp 2558–2566 | Cite as

Cortical Evoked Responses Following Esophageal Balloon Distension and Electrical Stimulation in Healthy Volunteers

  • Stephan Hollerbach
  • Peter Hudoba
  • Debbie Fitzpatrick
  • Richard Hunt
  • Adrian R.M. Upton
  • Gervais Tougas


Recording of evoked potential responsesrepresents an objective and quantifiable method to studyvisceral afferent sensory pathways in humans. Weexamined the evoked responses to mechanical distension(balloon) and electrical stimulation of the proximal anddistal esophagus. A standard manometric catheter with alatex balloon and an additional electrode attached toits body was placed in the lower esophagus in 15 healthy young volunteers. Repeatednonpainful balloon distension stimuli above theindividual sensation threshold (0.17 Hz, 12-20 ml) orshort electrical impulses (0.2 Hz, 12-16 mA) weredelivered in an alternate fashion at 23 and 33 cm from thenares. Evoked potential responses (EP) were recordedthrough 22 scalp surface electrodes using the standard10/20 International EEG system of electrode placement. Balloon distension produced a reproducibletriphasic response at both sites. Peak latencies ofthree negative EP peaks were 92 ± 17, 229± 40, and 339 ± 36 msec with proximalstimulation versus 154 ± 24, 275 ± 24, and384 ± 30 msec obtained with distal stimulation (P< 0.001). Electrical stimulation produced a triphasicresponse with significantly shorter peak latencies atboth sites when compared to mechanical stimulation (P <0.001). Peak latencies were 74 ± 12, 137 ±11, and 245 ± 27 msec proximal versus 83 ±12, 148 ± 32, and 247 ± 51 msec withdistal stimulation (P < 0.01). The calculated conduction velocities forboth modes of stimulation (balloon: 1.73 ± 0.9m/sec vs electrical: 10.1 ± 3.4 m/sec) arecompatible with conduction through C fibers and Adeltafibers, respectively. Both modes of stimulation producecharacteristic brain responses that are conveyed throughdifferent types of afferent fibers. The respectivecontributions of both types of fibers to esophageal function and symptomatology can be specificallyaddressed using this approach in both normal andpathologic conditions.



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  1. 1.
    Mayer EA, Gebhart GF: Basic and clinical aspe cts of visceral hype ralge sia. Gastroenterology 107:271–293, 1994PubMedGoogle Scholar
  2. 2.
    Spaziani R, Djuric V, Kamath MV, Sridhar S, Armstrong D, Fallen ED, Upton ARM, Tougas G: Autonomic response to esophage al acid perfusion in patients with esophageal symptoms. Gastroenterology 110:A762, 1996Google Scholar
  3. 3.
    Badr G, Carlsson CA, Fall M, Friberg S, Lindstrom L, Ohlsson B: Cortical evoked potentials following stimulation of the urinary bladder in man. Electroencephalogr Clin Neurophysiol 54:494–498, 1982CrossRefPubMedGoogle Scholar
  4. 4.
    Hanse n MV, Ertekin L, Larsson LE: Cere bral evoked potentials after stimulation of the posterior urethra in man. Electroencephalogr Clin Neurophysiol 52:517–530, 1990Google Scholar
  5. 5.
    Sarica Y, Karacan I: Cerebral response s evoked by stimulation of the vesico-urethral junction in normal subjects. Electroencephalogr Clin Neurophysiol 65:440–446, 1986PubMedGoogle Scholar
  6. 6.
    Frie ling T, Enck P, Wienbeck M: Cerebral re sponses by e lectrical stimulation of the re ctosigmoid in normal subjects. Dig Dis Sci 34:202–205, 1989PubMedGoogle Scholar
  7. 7.
    Loening-Baucke V, Read NW, Yamada T: Further evaluation of the afferent nervous pathways from the re ctum. Am J Physiol (Gastrointest Liver Physiol) 262:G927–G933, 1992Google Scholar
  8. 8.
    Aziz Q, Furlong PQ, Barlow J, Hobson A, Alani S, Bance wicz J, Ribbands M, Harding GFA, Thompson DG: Topographic mapping of cortical potentials evoked by distension of the human proximal and distal oesophagus. Electroencephalogr Clin Neurophysiol Evoked Potentials 96:219–228, 1995Google Scholar
  9. 9.
    Castell DO, Wood JD, Frieling T, Wright F, Vieth RF: Cerebral electrical potentials evoked by balloon distension of the human esophagus. Gastroenterology 98:662–666, 1990PubMedGoogle Scholar
  10. 10.
    Frie ling T, Enck P, Wienbeck M: Cerebral responses evoked by ele ctrical stimulation of the esophagus in normal subjects. Gastroente rology 97:475–478, 1989Google Scholar
  11. 11.
    Hollerbach S, Kamath MV, Chen Y, Fitzpatrick D, Upton ARM, Tougas G: The magnitude of the central response to esophageal electrical stimulation is intensity dependent. Gastroenterology 112:1137–1146, 1997PubMedGoogle Scholar
  12. 12.
    Hollerbach S, Kamath MV, Fitzpatrick D, Shine G, Fallen EL, Upton ARM, Tougas G: The cerebral response to electrical stimuli in the oesophagus is altered by increasing stimulus frequencies. Neurogastroenterol Motil 9:129–139, 1997CrossRefPubMedGoogle Scholar
  13. 13.
    Hollerbach S, Tougas G, Frieling T, Enck P, Fitzpatrick D, Upton ARM, Kamath MV: Cerebral evoked responses to gastrointestinal stimulation in humans. Crit Rev Biomed Eng 25:22–57, 1997Google Scholar
  14. 14.
    Tougas G, Hudoba P, Fitzpatrick D, Hunt RH, Upton ARM: Cerebral-evoke d potential responses following direct vagal and esophageal electrical stimulation in humans. Am J Physiol (Gastrointest Liver Physiol) 264:G486–G491, 1993Google Scholar
  15. 15.
    Rathmann W, Enck P, Frie ling T, Gries FA: Visceral afferent neuropathy in diabetic gastroparesis. Diabete s Care 14:1086–1089, 1991Google Scholar
  16. 16.
    Smout AJPM, DeVore MS, Dalton CB, Castell DO: Cere bral potentials evoked by oesophageal distension in patients with non-cardiac chest pain. Gut 33:298–302, 1992PubMedGoogle Scholar
  17. 17.
    Tougas G, Hunt RH, Fitzpatrick D, Upton ARM: Evidence of impaired afferent vagal function in patients with diabete s gastroparesis. PACE. 15:1597–1602, 1992PubMedGoogle Scholar
  18. 18.
    Smout AJP M, DeVore MS, Castell DO: Cerebral potentials evoked by esophage al distension in humans. Am J Physiol (Gastrointest Liver Physiol) 259:G955–G959, 1990Google Scholar
  19. 19.
    Upton ARM, Tougas G, Tallalla A, White AM, Hudoba P, Fitzpatrick D, Clarke B, Hunt RH: Neurophysiological effects of left vagal stimulation in man. PACE 14:70–76, 1991PubMedGoogle Scholar
  20. 20.
    Jasper HH: The 10/20 e lectrode system of the International Fede ration. Electroencephalogr Clin Neurophysiol 10:371–375, 1958Google Scholar
  21. 21.
    Tougas G, Fitzpatrick D, Upton ARM, Hunt RH: The cortical evoked response s produced by balloon distension and e lectrical stimulation of the esophagus involve different afferent vagal fibers. Gastroente rology 104:A592, 1993Google Scholar
  22. 22.
    Frobe rt O, Arendt-Nielsen L, Bak P, Funch-Jense n P, Bagge r JP: Oesophage al sensation assessed by e lectrical stimuli and brain evoked potentials—a new mode l for visceral nociception. Gut 37:603–609, 1995PubMedGoogle Scholar
  23. 23.
    Tougas G, Hudoba P, Upton ARM, Fitzpatrick D, Shine G, Hunt RH: Evoked potential re sponses (EPRs) and brain topography using balloon distension and e lectrical stimulation in man. Am J Gastroenterol 86:1305, 1991Google Scholar
  24. 24.
    Mei N: Inte stinal chemosensitivity. Physiol Rev 65:211–237, 1985PubMedGoogle Scholar
  25. 25.
    Sengupta JN, Kauvar D, Goyal RK: Characteristics of vagal esophage al tension-sensitive afferent fibers in the opossum. J Neurophysiol 61:1001–1010, 1989PubMedGoogle Scholar
  26. 26.
    Greenbe rg GR, Chan B, McDonald TJ, Alleyne J: The role of vagal integrity in gastrin rele asing peptide stimulated gastroente ropancre atic hormone re lease and gastric acid secretion. Regul Pept 10:179–187, 1985CrossRefPubMedGoogle Scholar
  27. 27.
    Collman PI, Tremblay L, Diamant NE: The distribution of spinal and vagal sensory neurons that innervate the esophagus of the cat. Gastroenterology 103:817–822, 1992PubMedGoogle Scholar
  28. 28.
    Theis R, Foreman RD: Inhibition and excitation of thoracic spinoreticular neurons by e lectrical stimulation of vagal afferent nerve s. Brain Res 207:178–183, 1981PubMedGoogle Scholar
  29. 29.
    DeVault KR, Beacham S, Castell DO, Streletz LJ, Ditunno JF: Esophage al sensation in spinal cord-injured patients: Balloon distension and ce rebral evoked potential recording. Am J Physiol (Gastrointest Liver Physiol) 271:G937–G941, 1996Google Scholar
  30. 30.
    Taylor DCM, Pierau FK: Painful sensations. InNociceptive afferent neurons. DCM Taylor, FK Pierau (eds). Manche ster, UK, Manche ste r University Pre ss, 1991, pp 18–36Google Scholar
  31. 31.
    Woodbury JW, Woodbury DM: Vagal stimulation reduce s the seve rity of maximal ele ctroshock seizures in intact rats. Use of a cuff for the stimulation and recording. PACE 14:94–106, 1991PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • Stephan Hollerbach
  • Peter Hudoba
  • Debbie Fitzpatrick
  • Richard Hunt
  • Adrian R.M. Upton
  • Gervais Tougas

There are no affiliations available

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