Neurobiological and psychophysical mechanisms underlying the oral sensation produced by carbonated water

C. T. Simons, J. M. Dessirier, M. Iodi Carstens, M. O'Mahony, Earl Carstens

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Abstract

Carbonated drinks elicit a sensation that is highly sought after, yet the underlying neural mechanisms are ill-defined. We hypothesize that CO2 is converted via carbonic anhydrase into carbonic acid, which excites lingual nociceptors that project to the trigeminal nuclei. We investigated this hypothesis using three methodological approaches. Electrophysiological methods were used to record responses of single units located in superficial laminae of the dorsomedial aspect of trigeminal subnucleus caudalis (Vc) evoked by lingual application of carbonated water in anesthetized rats. After pretreatment of the tongue with the carbonic anhydrase inhibitor dorzolamide, neuronal responses to carbonated water were significantly attenuated, followed by recovery. Using c-Fos immunohistochemistry, we investigated the distribution of brainstem neurons activated by intraoral carbonated water. Fos-like immunoreactivity (FLI) was significantly higher in the superficial laminae of dorsomedial and ventrolateral Vc in animals treated with carbonated water versus controls. Dorzolamide pretreatment significantly reduced FLI in dorsomedial Vc. We also examined the sensation elicited by carbonated water in human psychophysical studies. When one side of the tongue was pretreated with dorzolamide, followed by bilateral application of carbonated water, a significant majority of subjects chose the untreated side as having a stronger sensation and assigned significantly higher intensity ratings to that side. Dorzolamide did not reduce irritation elicited by pentanoic acid. The present data support the hypothesis that carbonated water excites lingual nociceptors via a carbonic anhydrase-dependent process, in turn exciting neurons in Vc that are presumably involved in signaling oral irritant sensations.

Original languageEnglish (US)
Pages (from-to)8134-8144
Number of pages11
JournalJournal of Neuroscience
Volume19
Issue number18
StatePublished - Sep 15 1999

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Keywords

  • C-Fos
  • Carbonated water
  • Carbonic anhydrase
  • Oral irritation
  • Psychophysics
  • Rat
  • Single-unit recording
  • Trigeminal nucleus caudalis
  • Two-alternative forced-choice

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Simons, C. T., Dessirier, J. M., Carstens, M. I., O'Mahony, M., & Carstens, E. (1999). Neurobiological and psychophysical mechanisms underlying the oral sensation produced by carbonated water. Journal of Neuroscience, 19(18), 8134-8144.