The Physiological Role of Serotonergic Transmission in Adult Rat Taste Buds

The role of the neurotransmitter serotonin (5-HT) in the taste bud is not well understood. Serotonin was long thought to be the neurotransmitter of taste signals from taste receptor cells (TRCs) to the gustatory afferent nerves, but the surprising discovery that this transmission is actually purinergic has left the actual role of serotonin in the taste bud enigmatic. Across mammalian species, 5-HT is highly conserved in type III cells of the bud, the only cells that form classic synaptic contacts with afferent nerve fibers. Previous work has documented that taste cells respond to serotonergic stimulation, and that of the many serotonin receptors, taste buds express only the 5-HT1A and 5-HT3 subtypes. The 5-HT1A subtype was found to be expressed in TRCs, while the 5-HT3 subtype is presumed to be expressed in postsynaptic neural elements. Further, 5-HT and the 5-HT1A receptor have been shown to localize in non-overlapping subpopulations of TRCs, signifying that serotonin functions in a paracrine manner among cells within the bud. Recent reports suggest that 5-HT may play a modulatory role in signal processing prior to the afferent output. The present study explored the role of serotonin in the rat taste bud by (1) determining the identity of TRCs and taste qualities affected by serotonin release, and (2) by examining the net outcome from this release at the gustatory neural level. Phenotyping the 5-HT1A-expressing cells through double label immunocytochemistry and single cell reverse transcriptase PCR revealed that 5-HT1A is localized only in a subset of type II taste cells that partially co-expressed type II TRC-specific markers, including taste receptor molecules T1R3 and T2R9, involved in detecting bitter, sweet, and umami tastes. 5-HT1A did not co-express with type III TRC-specific markers PKD2L1 and NCAM, confirming the paracrine nature of 5-HT signaling in the taste bud. To examine the functional role of serotonin in the taste bud, whole nerve recordings from the chorda tympani (CT) nerve were performed before and after jugular injections of serotonin receptor antagonists. Injection of the 5-HT1A receptor antagonists WAY-100635 or NAD-299 at various concentrations produced inhibitions in the integrated neural responses to lingually applied sweet, sour, salty, and bitter stimuli. On the other hand, injection of ondansetron, a 5-HT3 receptor antagonist, or saline, failed to produce any significant change in the chorda tympani responses to these lingually applied stimuli. These data provide solid evidence for a significant 5-HT1A-mediated role for serotonin in the modulation of taste information within the taste bud. Overall, findings from this study suggest that serotonin’s action, measured at the level of the chorda tympani, is mediated through its 5-HT1A receptor, found expressed paracrine to 5-HT in type II TRCs, including those that respond to bitter, sweet, and umami tastes. The study concludes that serotonin plays a facilitatory role in the transmission of taste signals from the taste bud by regulating ATP release from type II taste receptor cells following gustatory stimulation, and hence preventing the too-rapid desensitization of P2 purinoceptors on gustatory afferent nerve endings.

Name thesis:degree_name

Doctor of Philosophy

Level thesis:degree_level

doctoral

Discipline thesis:degree_discipline

Oral Biology

Grantor dc:publisher

The Ohio State University

Year dc:date

2013

Author dc:creator

• Jaber, Fadi Luc

Contributors dc:contributor

• HERNESS, SCOTT

• Neurosciences
• Serotonin
• 5-HT
• 5-HT1A
• 5-HT3
• taste bud
• gustation
• chorda tympani
• electrophysiological whole nerve recording
• immunocytochemistry
• single cell RT-PCR
• ATP
• P2X
• P2Y
• purinergic receptors
• T2R
• T1R

Statement dc:rights

• unrestricted
• This thesis or dissertation is protected by copyright: all rights reserved. It may not be copied or redistributed beyond the terms of applicable copyright laws.

Language dc:language

English

Repository record dc:identifier

http://rave.ohiolink.edu/etdc/view?acc_num=osu1357250524

OAI identifier oai:identifier

oai:etd.ohiolink.edu:osu1357250524