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The Journal of Neuroscience, September 15, 1999, 19(18):8134-8144
Neurobiological and Psychophysical Mechanisms Underlying the Oral
Sensation Produced by Carbonated Water
C. T.
Simons1, 2,
J. -M.
Dessirier1, 2,
M. Iodi
Carstens1,
M.
O'Mahony2, and
E.
Carstens1
1 Section of Neurobiology, Physiology, and Behavior,
and 2 Department of Food Science and Technology, University
of California, Davis, California 95616
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.
Key words:
trigeminal nucleus caudalis; c-Fos; single-unit
recording; rat; carbonated water; carbonic anhydrase; oral irritation; psychophysics; two-alternative forced-choice
Copyright © 1999 Society for Neuroscience 0270-6474/99/19188134-11$05.00/0
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