Gustatory modulation of the responses of trigeminal subnucleus caudalis neurons to noxious stimulation of the tongue in rats

Yves Boucher, Rufino Felizardo, Amanda H. Klein, Mirela I. Carstens, Earl Carstens

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Certain tastants inhibit oral irritation by capsaicin, whereas anesthesia of the chorda tympani (CT) enhances oral capsaicin burn. We tested the hypothesis that tastants activate the CT to suppress responses of trigeminal subnucleus caudalis (Vc) neurons to noxious oral stimuli. In anesthetized rats, we recorded Vc unit responses to noxious electrical, chemical (pentanoic acid, 200 μm) and thermal (55 °C) stimulation of the tongue. Electrically evoked responses were significantly reduced by a tastant mix and individually applied NaCl, monosodium glutamate (MSG), and monopotassium glutamate. Sucrose, citric acid, quinine and water (control) had no effect. Pentanoic acid-evoked responses were similarly attenuated by NaCl and MSG, but not by other tastants. Responses to noxious heat were not affected by any tastant. Transection and/or anesthesia of the CT bilaterally affected neither Vc neuronal responses to electrical or pentanoic acid stimulation, nor the depressant effect of NaCl and MSG on electrically evoked responses. Calcium imaging showed that neither NaCl nor MSG directly excited any trigeminal ganglion cells or affected their responses to pentanoic acid. GABA also had no effect, arguing against peripheral effects of GABA, NaCl or MSG on lingual nocicepive nerve endings. The data also rule out a central mechanism, as the effects of NaCl and MSG were intact following CT transection. We speculate that the effect is mediated peripherally by the release from taste receptor cells (type III) of some mediator(s) other than GABA to indirectly inhibit trigeminal nociceptors. The results also indicate that the CT does not exert a tonic inhibitory effect on nociceptive Vc neurons.

Original languageEnglish (US)
Pages (from-to)2812-2822
Number of pages11
JournalEuropean Journal of Neuroscience
Volume38
Issue number6
DOIs
StatePublished - Sep 2013

Fingerprint

Sodium Glutamate
Pentanoic Acids
Tongue
Neurons
gamma-Aminobutyric Acid
Nociceptors
Capsaicin
Anesthesia
Hot Temperature
Lingual Nerve
Trigeminal Ganglion
Quinine
Nerve Endings
Citric Acid
Sucrose
Glutamic Acid
Calcium
Water

Keywords

  • Calcium imaging
  • Chorda tympani
  • Tastant
  • Trigeminal ganglion cell

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Gustatory modulation of the responses of trigeminal subnucleus caudalis neurons to noxious stimulation of the tongue in rats. / Boucher, Yves; Felizardo, Rufino; Klein, Amanda H.; Carstens, Mirela I.; Carstens, Earl.

In: European Journal of Neuroscience, Vol. 38, No. 6, 09.2013, p. 2812-2822.

Research output: Contribution to journalArticle

Boucher, Yves ; Felizardo, Rufino ; Klein, Amanda H. ; Carstens, Mirela I. ; Carstens, Earl. / Gustatory modulation of the responses of trigeminal subnucleus caudalis neurons to noxious stimulation of the tongue in rats. In: European Journal of Neuroscience. 2013 ; Vol. 38, No. 6. pp. 2812-2822.
@article{8c9121d612c840d082a977230e4c1a85,
title = "Gustatory modulation of the responses of trigeminal subnucleus caudalis neurons to noxious stimulation of the tongue in rats",
abstract = "Certain tastants inhibit oral irritation by capsaicin, whereas anesthesia of the chorda tympani (CT) enhances oral capsaicin burn. We tested the hypothesis that tastants activate the CT to suppress responses of trigeminal subnucleus caudalis (Vc) neurons to noxious oral stimuli. In anesthetized rats, we recorded Vc unit responses to noxious electrical, chemical (pentanoic acid, 200 μm) and thermal (55 °C) stimulation of the tongue. Electrically evoked responses were significantly reduced by a tastant mix and individually applied NaCl, monosodium glutamate (MSG), and monopotassium glutamate. Sucrose, citric acid, quinine and water (control) had no effect. Pentanoic acid-evoked responses were similarly attenuated by NaCl and MSG, but not by other tastants. Responses to noxious heat were not affected by any tastant. Transection and/or anesthesia of the CT bilaterally affected neither Vc neuronal responses to electrical or pentanoic acid stimulation, nor the depressant effect of NaCl and MSG on electrically evoked responses. Calcium imaging showed that neither NaCl nor MSG directly excited any trigeminal ganglion cells or affected their responses to pentanoic acid. GABA also had no effect, arguing against peripheral effects of GABA, NaCl or MSG on lingual nocicepive nerve endings. The data also rule out a central mechanism, as the effects of NaCl and MSG were intact following CT transection. We speculate that the effect is mediated peripherally by the release from taste receptor cells (type III) of some mediator(s) other than GABA to indirectly inhibit trigeminal nociceptors. The results also indicate that the CT does not exert a tonic inhibitory effect on nociceptive Vc neurons.",
keywords = "Calcium imaging, Chorda tympani, Tastant, Trigeminal ganglion cell",
author = "Yves Boucher and Rufino Felizardo and Klein, {Amanda H.} and Carstens, {Mirela I.} and Earl Carstens",
year = "2013",
month = "9",
doi = "10.1111/ejn.12282",
language = "English (US)",
volume = "38",
pages = "2812--2822",
journal = "European Journal of Neuroscience",
issn = "0953-816X",
publisher = "Wiley-Blackwell",
number = "6",

}

TY - JOUR

T1 - Gustatory modulation of the responses of trigeminal subnucleus caudalis neurons to noxious stimulation of the tongue in rats

AU - Boucher, Yves

AU - Felizardo, Rufino

AU - Klein, Amanda H.

AU - Carstens, Mirela I.

AU - Carstens, Earl

PY - 2013/9

Y1 - 2013/9

N2 - Certain tastants inhibit oral irritation by capsaicin, whereas anesthesia of the chorda tympani (CT) enhances oral capsaicin burn. We tested the hypothesis that tastants activate the CT to suppress responses of trigeminal subnucleus caudalis (Vc) neurons to noxious oral stimuli. In anesthetized rats, we recorded Vc unit responses to noxious electrical, chemical (pentanoic acid, 200 μm) and thermal (55 °C) stimulation of the tongue. Electrically evoked responses were significantly reduced by a tastant mix and individually applied NaCl, monosodium glutamate (MSG), and monopotassium glutamate. Sucrose, citric acid, quinine and water (control) had no effect. Pentanoic acid-evoked responses were similarly attenuated by NaCl and MSG, but not by other tastants. Responses to noxious heat were not affected by any tastant. Transection and/or anesthesia of the CT bilaterally affected neither Vc neuronal responses to electrical or pentanoic acid stimulation, nor the depressant effect of NaCl and MSG on electrically evoked responses. Calcium imaging showed that neither NaCl nor MSG directly excited any trigeminal ganglion cells or affected their responses to pentanoic acid. GABA also had no effect, arguing against peripheral effects of GABA, NaCl or MSG on lingual nocicepive nerve endings. The data also rule out a central mechanism, as the effects of NaCl and MSG were intact following CT transection. We speculate that the effect is mediated peripherally by the release from taste receptor cells (type III) of some mediator(s) other than GABA to indirectly inhibit trigeminal nociceptors. The results also indicate that the CT does not exert a tonic inhibitory effect on nociceptive Vc neurons.

AB - Certain tastants inhibit oral irritation by capsaicin, whereas anesthesia of the chorda tympani (CT) enhances oral capsaicin burn. We tested the hypothesis that tastants activate the CT to suppress responses of trigeminal subnucleus caudalis (Vc) neurons to noxious oral stimuli. In anesthetized rats, we recorded Vc unit responses to noxious electrical, chemical (pentanoic acid, 200 μm) and thermal (55 °C) stimulation of the tongue. Electrically evoked responses were significantly reduced by a tastant mix and individually applied NaCl, monosodium glutamate (MSG), and monopotassium glutamate. Sucrose, citric acid, quinine and water (control) had no effect. Pentanoic acid-evoked responses were similarly attenuated by NaCl and MSG, but not by other tastants. Responses to noxious heat were not affected by any tastant. Transection and/or anesthesia of the CT bilaterally affected neither Vc neuronal responses to electrical or pentanoic acid stimulation, nor the depressant effect of NaCl and MSG on electrically evoked responses. Calcium imaging showed that neither NaCl nor MSG directly excited any trigeminal ganglion cells or affected their responses to pentanoic acid. GABA also had no effect, arguing against peripheral effects of GABA, NaCl or MSG on lingual nocicepive nerve endings. The data also rule out a central mechanism, as the effects of NaCl and MSG were intact following CT transection. We speculate that the effect is mediated peripherally by the release from taste receptor cells (type III) of some mediator(s) other than GABA to indirectly inhibit trigeminal nociceptors. The results also indicate that the CT does not exert a tonic inhibitory effect on nociceptive Vc neurons.

KW - Calcium imaging

KW - Chorda tympani

KW - Tastant

KW - Trigeminal ganglion cell

UR - http://www.scopus.com/inward/record.url?scp=84884704219&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84884704219&partnerID=8YFLogxK

U2 - 10.1111/ejn.12282

DO - 10.1111/ejn.12282

M3 - Article

C2 - 23802589

AN - SCOPUS:84884704219

VL - 38

SP - 2812

EP - 2822

JO - European Journal of Neuroscience

JF - European Journal of Neuroscience

SN - 0953-816X

IS - 6

ER -