Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli

Karen L. Zanotto, Austin W. Merrill, Mirela Iodi Carstens, Earl Carstens

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

The recent discoveries of cold-sensitive transient receptor potential (TRP) channels prompted us to investigate the responses of neurons in trigeminal subnucleus caudalis (Vc) to intraoral cooling and agonists of TRPM8 and TRPA1. Single units responsive to lingual cooling were recorded in superficial laminae of Vc in thiopental-anesthetized rats. All units responded to noxious heat and 88% responded to menthol. Responses increased with menthol concentration from 0.1 to 1% (6.4-64 mM) and plateaued at 10% (640 mM). Noxious coldevoked responses were significantly enhanced after menthol in a concentration-dependent manner. Constant-flow application of 1% menthol elicited a phasic discharge that adapted over 2-8 min and significantly enhanced subsequent cold-evoked but not heat-evoked responses; vehicle (10% ethanol) was ineffective. Reapplication of menthol 15 min later elicited a significantly reduced response (self-desensitization). Vc units were similarly excited phasically by 1% menthol dissolved in 40% ethanol. The 40% ethanol briefly excited Vc units during the first minute and reduced subsequent responses to noxious heat and cold while exhibiting neither self-desensitization nor cross-desensitization to menthol. Menthol cross-desensitized Vc responses to 40% ethanol. Most menthol-responsive units also responded to the TRPA1 agonists cinnamaldehyde and mustard oil, and the TRPV1 agonist capsaicin. Units in superficial Vc receive convergent input from primary afferents that express TRPM8, TRPA1, and/or TRPV1 channels, either directly or indirectly via intersub-nuclear pathways. The convergent nature of these units suggests a general role in signaling noxious stimuli.

Original languageEnglish (US)
Pages (from-to)966-978
Number of pages13
JournalJournal of Neurophysiology
Volume97
Issue number2
DOIs
StatePublished - Feb 2007

Fingerprint

Menthol
Irritants
Neurons
Ethanol
Hot Temperature
Transient Receptor Potential Channels
Thiopental
Capsaicin
Tongue

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli. / Zanotto, Karen L.; Merrill, Austin W.; Carstens, Mirela Iodi; Carstens, Earl.

In: Journal of Neurophysiology, Vol. 97, No. 2, 02.2007, p. 966-978.

Research output: Contribution to journalArticle

Zanotto, Karen L. ; Merrill, Austin W. ; Carstens, Mirela Iodi ; Carstens, Earl. / Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli. In: Journal of Neurophysiology. 2007 ; Vol. 97, No. 2. pp. 966-978.
@article{13e10cea594c4f62815dd757b76cb15c,
title = "Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli",
abstract = "The recent discoveries of cold-sensitive transient receptor potential (TRP) channels prompted us to investigate the responses of neurons in trigeminal subnucleus caudalis (Vc) to intraoral cooling and agonists of TRPM8 and TRPA1. Single units responsive to lingual cooling were recorded in superficial laminae of Vc in thiopental-anesthetized rats. All units responded to noxious heat and 88{\%} responded to menthol. Responses increased with menthol concentration from 0.1 to 1{\%} (6.4-64 mM) and plateaued at 10{\%} (640 mM). Noxious coldevoked responses were significantly enhanced after menthol in a concentration-dependent manner. Constant-flow application of 1{\%} menthol elicited a phasic discharge that adapted over 2-8 min and significantly enhanced subsequent cold-evoked but not heat-evoked responses; vehicle (10{\%} ethanol) was ineffective. Reapplication of menthol 15 min later elicited a significantly reduced response (self-desensitization). Vc units were similarly excited phasically by 1{\%} menthol dissolved in 40{\%} ethanol. The 40{\%} ethanol briefly excited Vc units during the first minute and reduced subsequent responses to noxious heat and cold while exhibiting neither self-desensitization nor cross-desensitization to menthol. Menthol cross-desensitized Vc responses to 40{\%} ethanol. Most menthol-responsive units also responded to the TRPA1 agonists cinnamaldehyde and mustard oil, and the TRPV1 agonist capsaicin. Units in superficial Vc receive convergent input from primary afferents that express TRPM8, TRPA1, and/or TRPV1 channels, either directly or indirectly via intersub-nuclear pathways. The convergent nature of these units suggests a general role in signaling noxious stimuli.",
author = "Zanotto, {Karen L.} and Merrill, {Austin W.} and Carstens, {Mirela Iodi} and Earl Carstens",
year = "2007",
month = "2",
doi = "10.1152/jn.00996.2006",
language = "English (US)",
volume = "97",
pages = "966--978",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "2",

}

TY - JOUR

T1 - Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli

AU - Zanotto, Karen L.

AU - Merrill, Austin W.

AU - Carstens, Mirela Iodi

AU - Carstens, Earl

PY - 2007/2

Y1 - 2007/2

N2 - The recent discoveries of cold-sensitive transient receptor potential (TRP) channels prompted us to investigate the responses of neurons in trigeminal subnucleus caudalis (Vc) to intraoral cooling and agonists of TRPM8 and TRPA1. Single units responsive to lingual cooling were recorded in superficial laminae of Vc in thiopental-anesthetized rats. All units responded to noxious heat and 88% responded to menthol. Responses increased with menthol concentration from 0.1 to 1% (6.4-64 mM) and plateaued at 10% (640 mM). Noxious coldevoked responses were significantly enhanced after menthol in a concentration-dependent manner. Constant-flow application of 1% menthol elicited a phasic discharge that adapted over 2-8 min and significantly enhanced subsequent cold-evoked but not heat-evoked responses; vehicle (10% ethanol) was ineffective. Reapplication of menthol 15 min later elicited a significantly reduced response (self-desensitization). Vc units were similarly excited phasically by 1% menthol dissolved in 40% ethanol. The 40% ethanol briefly excited Vc units during the first minute and reduced subsequent responses to noxious heat and cold while exhibiting neither self-desensitization nor cross-desensitization to menthol. Menthol cross-desensitized Vc responses to 40% ethanol. Most menthol-responsive units also responded to the TRPA1 agonists cinnamaldehyde and mustard oil, and the TRPV1 agonist capsaicin. Units in superficial Vc receive convergent input from primary afferents that express TRPM8, TRPA1, and/or TRPV1 channels, either directly or indirectly via intersub-nuclear pathways. The convergent nature of these units suggests a general role in signaling noxious stimuli.

AB - The recent discoveries of cold-sensitive transient receptor potential (TRP) channels prompted us to investigate the responses of neurons in trigeminal subnucleus caudalis (Vc) to intraoral cooling and agonists of TRPM8 and TRPA1. Single units responsive to lingual cooling were recorded in superficial laminae of Vc in thiopental-anesthetized rats. All units responded to noxious heat and 88% responded to menthol. Responses increased with menthol concentration from 0.1 to 1% (6.4-64 mM) and plateaued at 10% (640 mM). Noxious coldevoked responses were significantly enhanced after menthol in a concentration-dependent manner. Constant-flow application of 1% menthol elicited a phasic discharge that adapted over 2-8 min and significantly enhanced subsequent cold-evoked but not heat-evoked responses; vehicle (10% ethanol) was ineffective. Reapplication of menthol 15 min later elicited a significantly reduced response (self-desensitization). Vc units were similarly excited phasically by 1% menthol dissolved in 40% ethanol. The 40% ethanol briefly excited Vc units during the first minute and reduced subsequent responses to noxious heat and cold while exhibiting neither self-desensitization nor cross-desensitization to menthol. Menthol cross-desensitized Vc responses to 40% ethanol. Most menthol-responsive units also responded to the TRPA1 agonists cinnamaldehyde and mustard oil, and the TRPV1 agonist capsaicin. Units in superficial Vc receive convergent input from primary afferents that express TRPM8, TRPA1, and/or TRPV1 channels, either directly or indirectly via intersub-nuclear pathways. The convergent nature of these units suggests a general role in signaling noxious stimuli.

UR - http://www.scopus.com/inward/record.url?scp=33846911018&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33846911018&partnerID=8YFLogxK

U2 - 10.1152/jn.00996.2006

DO - 10.1152/jn.00996.2006

M3 - Article

C2 - 17151223

AN - SCOPUS:33846911018

VL - 97

SP - 966

EP - 978

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 2

ER -