Sensitization of trigeminal caudalis neuronal responses to intraoral acid and salt stimuli and desensitization by nicotine

Satoko Sudo, Makoto Sudo, Christopher T. Simons, Jean Marc Dessirier, Earl Carstens

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

In human studies, repeated intraoral application of strong acidic or salt stimuli induces irritation that progressively increases across trials (sensitization), whereas irritation elicited by nicotine progressively decreases (desensitization). We investigated whether nociceptive neurons in trigeminal subnucleus caudalis (Vc) exhibit increasing or decreasing patterns of firing to the intraoral application of these irritants. In rats anesthetized with halothane and thiopental, single-unit recordings were made from nociceptive neurons in superficial layers of dorsomedial Vc that responded to mechanical and noxious thermal and chemical stimulation of the tongue. NaCl (5M), citric acid (300mM), pentanoic acid (300mM) or nicotine (600mM) were separately delivered to the tongue by constant flow (0.32ml/min) for 15 or 25min. NaCl, citric acid and pentanoic acid each elicited a progressive, significant increase in Vc neuronal firing over the initial 10min to a plateau level that was maintained for the stimulus duration. Nicotine induced a significant increase in firing rate of Vc neurons within 6min, followed by a decline back to the baseline level over the ensuing 10min. Following a rest period, reapplication of nicotine no longer activated Vc neurons, indicative of self-desensitization. We additionally tested for nicotine cross-desensitization to acid. After recording the responses of Vc neurons to pentanoic acid and noxious heat, nicotine was then applied for 15min. Post-nicotine responses to pentanoic acid were markedly reduced (to 13% of control), indicative of cross-desensitization; responses to noxious heat were also reduced to a lesser degree (to 71% of control). The progressive increase in Vc neuronal firing elicited by NaCl and acid, and the decline in firing after initial nicotinic excitation, resemble psychophysical patterns of sensitization and desensitization, respectively, and support the involvement of Vc neurons in the signaling of oral irritant sensations.

Original languageEnglish (US)
Pages (from-to)277-286
Number of pages10
JournalPain
Volume98
Issue number3
DOIs
StatePublished - 2002

Fingerprint

Nicotine
Pentanoic Acids
Salts
Acids
Neurons
Nociceptors
Hot Temperature
Irritants
Tongue
Citric Acid
Chemical Stimulation
Thiopental
Halothane
Psychologic Desensitization

Keywords

  • Acid
  • Desensitization
  • Nicotine
  • Oral irritation
  • Salt
  • Sensitization
  • Trigeminal subnucleus caudalis

ASJC Scopus subject areas

  • Clinical Neurology
  • Psychiatry and Mental health
  • Neurology
  • Neuroscience(all)
  • Pharmacology
  • Clinical Psychology

Cite this

Sensitization of trigeminal caudalis neuronal responses to intraoral acid and salt stimuli and desensitization by nicotine. / Sudo, Satoko; Sudo, Makoto; Simons, Christopher T.; Dessirier, Jean Marc; Carstens, Earl.

In: Pain, Vol. 98, No. 3, 2002, p. 277-286.

Research output: Contribution to journalArticle

Sudo, Satoko ; Sudo, Makoto ; Simons, Christopher T. ; Dessirier, Jean Marc ; Carstens, Earl. / Sensitization of trigeminal caudalis neuronal responses to intraoral acid and salt stimuli and desensitization by nicotine. In: Pain. 2002 ; Vol. 98, No. 3. pp. 277-286.
@article{7aaac239d10642e1bba56ceb49bef07d,
title = "Sensitization of trigeminal caudalis neuronal responses to intraoral acid and salt stimuli and desensitization by nicotine",
abstract = "In human studies, repeated intraoral application of strong acidic or salt stimuli induces irritation that progressively increases across trials (sensitization), whereas irritation elicited by nicotine progressively decreases (desensitization). We investigated whether nociceptive neurons in trigeminal subnucleus caudalis (Vc) exhibit increasing or decreasing patterns of firing to the intraoral application of these irritants. In rats anesthetized with halothane and thiopental, single-unit recordings were made from nociceptive neurons in superficial layers of dorsomedial Vc that responded to mechanical and noxious thermal and chemical stimulation of the tongue. NaCl (5M), citric acid (300mM), pentanoic acid (300mM) or nicotine (600mM) were separately delivered to the tongue by constant flow (0.32ml/min) for 15 or 25min. NaCl, citric acid and pentanoic acid each elicited a progressive, significant increase in Vc neuronal firing over the initial 10min to a plateau level that was maintained for the stimulus duration. Nicotine induced a significant increase in firing rate of Vc neurons within 6min, followed by a decline back to the baseline level over the ensuing 10min. Following a rest period, reapplication of nicotine no longer activated Vc neurons, indicative of self-desensitization. We additionally tested for nicotine cross-desensitization to acid. After recording the responses of Vc neurons to pentanoic acid and noxious heat, nicotine was then applied for 15min. Post-nicotine responses to pentanoic acid were markedly reduced (to 13{\%} of control), indicative of cross-desensitization; responses to noxious heat were also reduced to a lesser degree (to 71{\%} of control). The progressive increase in Vc neuronal firing elicited by NaCl and acid, and the decline in firing after initial nicotinic excitation, resemble psychophysical patterns of sensitization and desensitization, respectively, and support the involvement of Vc neurons in the signaling of oral irritant sensations.",
keywords = "Acid, Desensitization, Nicotine, Oral irritation, Salt, Sensitization, Trigeminal subnucleus caudalis",
author = "Satoko Sudo and Makoto Sudo and Simons, {Christopher T.} and Dessirier, {Jean Marc} and Earl Carstens",
year = "2002",
doi = "10.1016/S0304-3959(02)00025-8",
language = "English (US)",
volume = "98",
pages = "277--286",
journal = "Pain",
issn = "0304-3959",
publisher = "Elsevier",
number = "3",

}

TY - JOUR

T1 - Sensitization of trigeminal caudalis neuronal responses to intraoral acid and salt stimuli and desensitization by nicotine

AU - Sudo, Satoko

AU - Sudo, Makoto

AU - Simons, Christopher T.

AU - Dessirier, Jean Marc

AU - Carstens, Earl

PY - 2002

Y1 - 2002

N2 - In human studies, repeated intraoral application of strong acidic or salt stimuli induces irritation that progressively increases across trials (sensitization), whereas irritation elicited by nicotine progressively decreases (desensitization). We investigated whether nociceptive neurons in trigeminal subnucleus caudalis (Vc) exhibit increasing or decreasing patterns of firing to the intraoral application of these irritants. In rats anesthetized with halothane and thiopental, single-unit recordings were made from nociceptive neurons in superficial layers of dorsomedial Vc that responded to mechanical and noxious thermal and chemical stimulation of the tongue. NaCl (5M), citric acid (300mM), pentanoic acid (300mM) or nicotine (600mM) were separately delivered to the tongue by constant flow (0.32ml/min) for 15 or 25min. NaCl, citric acid and pentanoic acid each elicited a progressive, significant increase in Vc neuronal firing over the initial 10min to a plateau level that was maintained for the stimulus duration. Nicotine induced a significant increase in firing rate of Vc neurons within 6min, followed by a decline back to the baseline level over the ensuing 10min. Following a rest period, reapplication of nicotine no longer activated Vc neurons, indicative of self-desensitization. We additionally tested for nicotine cross-desensitization to acid. After recording the responses of Vc neurons to pentanoic acid and noxious heat, nicotine was then applied for 15min. Post-nicotine responses to pentanoic acid were markedly reduced (to 13% of control), indicative of cross-desensitization; responses to noxious heat were also reduced to a lesser degree (to 71% of control). The progressive increase in Vc neuronal firing elicited by NaCl and acid, and the decline in firing after initial nicotinic excitation, resemble psychophysical patterns of sensitization and desensitization, respectively, and support the involvement of Vc neurons in the signaling of oral irritant sensations.

AB - In human studies, repeated intraoral application of strong acidic or salt stimuli induces irritation that progressively increases across trials (sensitization), whereas irritation elicited by nicotine progressively decreases (desensitization). We investigated whether nociceptive neurons in trigeminal subnucleus caudalis (Vc) exhibit increasing or decreasing patterns of firing to the intraoral application of these irritants. In rats anesthetized with halothane and thiopental, single-unit recordings were made from nociceptive neurons in superficial layers of dorsomedial Vc that responded to mechanical and noxious thermal and chemical stimulation of the tongue. NaCl (5M), citric acid (300mM), pentanoic acid (300mM) or nicotine (600mM) were separately delivered to the tongue by constant flow (0.32ml/min) for 15 or 25min. NaCl, citric acid and pentanoic acid each elicited a progressive, significant increase in Vc neuronal firing over the initial 10min to a plateau level that was maintained for the stimulus duration. Nicotine induced a significant increase in firing rate of Vc neurons within 6min, followed by a decline back to the baseline level over the ensuing 10min. Following a rest period, reapplication of nicotine no longer activated Vc neurons, indicative of self-desensitization. We additionally tested for nicotine cross-desensitization to acid. After recording the responses of Vc neurons to pentanoic acid and noxious heat, nicotine was then applied for 15min. Post-nicotine responses to pentanoic acid were markedly reduced (to 13% of control), indicative of cross-desensitization; responses to noxious heat were also reduced to a lesser degree (to 71% of control). The progressive increase in Vc neuronal firing elicited by NaCl and acid, and the decline in firing after initial nicotinic excitation, resemble psychophysical patterns of sensitization and desensitization, respectively, and support the involvement of Vc neurons in the signaling of oral irritant sensations.

KW - Acid

KW - Desensitization

KW - Nicotine

KW - Oral irritation

KW - Salt

KW - Sensitization

KW - Trigeminal subnucleus caudalis

UR - http://www.scopus.com/inward/record.url?scp=0036068540&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0036068540&partnerID=8YFLogxK

U2 - 10.1016/S0304-3959(02)00025-8

DO - 10.1016/S0304-3959(02)00025-8

M3 - Article

C2 - 12127029

AN - SCOPUS:0036068540

VL - 98

SP - 277

EP - 286

JO - Pain

JF - Pain

SN - 0304-3959

IS - 3

ER -