Neurobiological and psychophysical mechanisms underlying the oral sensation produced by carbonated water.
Carbonated drinks elicit a sensation that is highly sought after, yet the underlying neural mechanisms are ill-defined. We hypothesize that CO(2) 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.
Simons
C T
CT
Section of Neurobiology, Physiology, and Behavior, University of California, Davis, California 95616, USA.
Dessirier
J M
JM
Carstens
M I
MI
O'Mahony
M
M
Carstens
E
E
D000200:Action Potentials / Q000187:drug effects; D000328:Adult; D000818:Animals; D001933:Brain Stem / Q000502:physiology*; D002253:Carbonated Beverages; D002257:Carbonic Anhydrase Inhibitors / Q000494:pharmacology*; D004594:Electrophysiology / Q000379:methods; D005260:Female; D007839:Functional Laterality; D006801:Humans; D008297:Male; D009474:Neurons / Q000502:physiology*; D016760:Proto-Oncogene Proteins c-fos / Q000032:analysis / Q000235:genetics; D051381:Rats; D017207:Rats, Sprague-Dawley; D012677:Sensation / Q000502:physiology*; D013449:Sulfonamides / Q000494:pharmacology*; D013876:Thiophenes / Q000494:pharmacology*; D014059:Tongue / Q000294:innervation*; D014278:Trigeminal Nuclei / Q000502:physiology*
D002257:Carbonic Anhydrase Inhibitors; D016760:Proto-Oncogene Proteins c-fos; D013449:Sulfonamides; D013876:Thiophenes; C062765:dorzolamide