Oral thermosensing by murine trigeminal neurons: modulation by capsaicin, menthol and mustard oil

Sara C.M. Leijon, Amanda F. Neves, Joseph M. Breza, Sidney A. Simon, Nirupa Chaudhari, Stephen D Roper

Research output: Contribution to journalArticle

Abstract

Key points: Orosensory thermal trigeminal afferent neurons respond to cool, warm, and nociceptive hot temperatures with the majority activated in the cool range. Many of these thermosensitive trigeminal orosensory afferent neurons also respond to capsaicin, menthol, and/or mustard oil (allyl isothiocyanate) at concentrations found in foods and spices. There is significant but incomplete overlap between afferent trigeminal neurons that respond to oral thermal stimulation and to the above chemesthetic compounds. Capsaicin sensitizes warm trigeminal thermoreceptors and orosensory nociceptors; menthol attenuates cool thermoresponses. Abstract: When consumed with foods, mint, mustard, and chili peppers generate pronounced oral thermosensations. Here we recorded responses in mouse trigeminal ganglion neurons to investigate interactions between thermal sensing and the active ingredients of these plants – menthol, allyl isothiocyanate (AITC), and capsaicin, respectively – at concentrations found in foods and commercial hygiene products. We carried out in vivo confocal calcium imaging of trigeminal ganglia in which neurons express GCaMP3 or GCAMP6s and recorded their responses to oral stimulation with thermal and the above chemesthetic stimuli. In the V3 (oral sensory) region of the ganglion, thermoreceptive neurons accounted for ∼10% of imaged neurons. We categorized them into three distinct classes: cool-responsive and warm-responsive thermosensors, and nociceptors (responsive only to temperatures ≥43–45 °C). Menthol, AITC, and capsaicin also elicited robust calcium responses that differed markedly in their latencies and durations. Most of the neurons that responded to these chemesthetic stimuli were also thermosensitive. Capsaicin and AITC increased the numbers of warm-responding neurons and shifted the nociceptor threshold to lower temperatures. Menthol attenuated the responses in all classes of thermoreceptors. Our data show that while individual neurons may respond to a narrow temperature range (or even bimodally), taken collectively, the population is able to report on graded changes of temperature. Our findings also substantiate an explanation for the thermal sensations experienced when one consumes pungent spices or mint.

Original languageEnglish (US)
JournalJournal of Physiology
DOIs
StatePublished - Jan 1 2019

Fingerprint

Thermosensing
Menthol
Capsaicin
Hot Temperature
Neurons
Afferent Neurons
Nociceptors
Thermoreceptors
Mentha
Trigeminal Ganglion
Spices
Temperature
Food
Sensory Ganglia
Calcium
Capsicum
Mustard Plant
mustard oil
Hygiene

Keywords

  • calcium imaging
  • chemesthesis
  • sensory neurons
  • thermosensation
  • Trigeminal ganglion

ASJC Scopus subject areas

  • Physiology

Cite this

Oral thermosensing by murine trigeminal neurons : modulation by capsaicin, menthol and mustard oil. / Leijon, Sara C.M.; Neves, Amanda F.; Breza, Joseph M.; Simon, Sidney A.; Chaudhari, Nirupa; Roper, Stephen D.

In: Journal of Physiology, 01.01.2019.

Research output: Contribution to journalArticle

@article{681f3796ff6f42c6a9c8bc385fd52e8d,
title = "Oral thermosensing by murine trigeminal neurons: modulation by capsaicin, menthol and mustard oil",
abstract = "Key points: Orosensory thermal trigeminal afferent neurons respond to cool, warm, and nociceptive hot temperatures with the majority activated in the cool range. Many of these thermosensitive trigeminal orosensory afferent neurons also respond to capsaicin, menthol, and/or mustard oil (allyl isothiocyanate) at concentrations found in foods and spices. There is significant but incomplete overlap between afferent trigeminal neurons that respond to oral thermal stimulation and to the above chemesthetic compounds. Capsaicin sensitizes warm trigeminal thermoreceptors and orosensory nociceptors; menthol attenuates cool thermoresponses. Abstract: When consumed with foods, mint, mustard, and chili peppers generate pronounced oral thermosensations. Here we recorded responses in mouse trigeminal ganglion neurons to investigate interactions between thermal sensing and the active ingredients of these plants – menthol, allyl isothiocyanate (AITC), and capsaicin, respectively – at concentrations found in foods and commercial hygiene products. We carried out in vivo confocal calcium imaging of trigeminal ganglia in which neurons express GCaMP3 or GCAMP6s and recorded their responses to oral stimulation with thermal and the above chemesthetic stimuli. In the V3 (oral sensory) region of the ganglion, thermoreceptive neurons accounted for ∼10{\%} of imaged neurons. We categorized them into three distinct classes: cool-responsive and warm-responsive thermosensors, and nociceptors (responsive only to temperatures ≥43–45 °C). Menthol, AITC, and capsaicin also elicited robust calcium responses that differed markedly in their latencies and durations. Most of the neurons that responded to these chemesthetic stimuli were also thermosensitive. Capsaicin and AITC increased the numbers of warm-responding neurons and shifted the nociceptor threshold to lower temperatures. Menthol attenuated the responses in all classes of thermoreceptors. Our data show that while individual neurons may respond to a narrow temperature range (or even bimodally), taken collectively, the population is able to report on graded changes of temperature. Our findings also substantiate an explanation for the thermal sensations experienced when one consumes pungent spices or mint.",
keywords = "calcium imaging, chemesthesis, sensory neurons, thermosensation, Trigeminal ganglion",
author = "Leijon, {Sara C.M.} and Neves, {Amanda F.} and Breza, {Joseph M.} and Simon, {Sidney A.} and Nirupa Chaudhari and Roper, {Stephen D}",
year = "2019",
month = "1",
day = "1",
doi = "10.1113/JP277385",
language = "English (US)",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",

}

TY - JOUR

T1 - Oral thermosensing by murine trigeminal neurons

T2 - modulation by capsaicin, menthol and mustard oil

AU - Leijon, Sara C.M.

AU - Neves, Amanda F.

AU - Breza, Joseph M.

AU - Simon, Sidney A.

AU - Chaudhari, Nirupa

AU - Roper, Stephen D

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Key points: Orosensory thermal trigeminal afferent neurons respond to cool, warm, and nociceptive hot temperatures with the majority activated in the cool range. Many of these thermosensitive trigeminal orosensory afferent neurons also respond to capsaicin, menthol, and/or mustard oil (allyl isothiocyanate) at concentrations found in foods and spices. There is significant but incomplete overlap between afferent trigeminal neurons that respond to oral thermal stimulation and to the above chemesthetic compounds. Capsaicin sensitizes warm trigeminal thermoreceptors and orosensory nociceptors; menthol attenuates cool thermoresponses. Abstract: When consumed with foods, mint, mustard, and chili peppers generate pronounced oral thermosensations. Here we recorded responses in mouse trigeminal ganglion neurons to investigate interactions between thermal sensing and the active ingredients of these plants – menthol, allyl isothiocyanate (AITC), and capsaicin, respectively – at concentrations found in foods and commercial hygiene products. We carried out in vivo confocal calcium imaging of trigeminal ganglia in which neurons express GCaMP3 or GCAMP6s and recorded their responses to oral stimulation with thermal and the above chemesthetic stimuli. In the V3 (oral sensory) region of the ganglion, thermoreceptive neurons accounted for ∼10% of imaged neurons. We categorized them into three distinct classes: cool-responsive and warm-responsive thermosensors, and nociceptors (responsive only to temperatures ≥43–45 °C). Menthol, AITC, and capsaicin also elicited robust calcium responses that differed markedly in their latencies and durations. Most of the neurons that responded to these chemesthetic stimuli were also thermosensitive. Capsaicin and AITC increased the numbers of warm-responding neurons and shifted the nociceptor threshold to lower temperatures. Menthol attenuated the responses in all classes of thermoreceptors. Our data show that while individual neurons may respond to a narrow temperature range (or even bimodally), taken collectively, the population is able to report on graded changes of temperature. Our findings also substantiate an explanation for the thermal sensations experienced when one consumes pungent spices or mint.

AB - Key points: Orosensory thermal trigeminal afferent neurons respond to cool, warm, and nociceptive hot temperatures with the majority activated in the cool range. Many of these thermosensitive trigeminal orosensory afferent neurons also respond to capsaicin, menthol, and/or mustard oil (allyl isothiocyanate) at concentrations found in foods and spices. There is significant but incomplete overlap between afferent trigeminal neurons that respond to oral thermal stimulation and to the above chemesthetic compounds. Capsaicin sensitizes warm trigeminal thermoreceptors and orosensory nociceptors; menthol attenuates cool thermoresponses. Abstract: When consumed with foods, mint, mustard, and chili peppers generate pronounced oral thermosensations. Here we recorded responses in mouse trigeminal ganglion neurons to investigate interactions between thermal sensing and the active ingredients of these plants – menthol, allyl isothiocyanate (AITC), and capsaicin, respectively – at concentrations found in foods and commercial hygiene products. We carried out in vivo confocal calcium imaging of trigeminal ganglia in which neurons express GCaMP3 or GCAMP6s and recorded their responses to oral stimulation with thermal and the above chemesthetic stimuli. In the V3 (oral sensory) region of the ganglion, thermoreceptive neurons accounted for ∼10% of imaged neurons. We categorized them into three distinct classes: cool-responsive and warm-responsive thermosensors, and nociceptors (responsive only to temperatures ≥43–45 °C). Menthol, AITC, and capsaicin also elicited robust calcium responses that differed markedly in their latencies and durations. Most of the neurons that responded to these chemesthetic stimuli were also thermosensitive. Capsaicin and AITC increased the numbers of warm-responding neurons and shifted the nociceptor threshold to lower temperatures. Menthol attenuated the responses in all classes of thermoreceptors. Our data show that while individual neurons may respond to a narrow temperature range (or even bimodally), taken collectively, the population is able to report on graded changes of temperature. Our findings also substantiate an explanation for the thermal sensations experienced when one consumes pungent spices or mint.

KW - calcium imaging

KW - chemesthesis

KW - sensory neurons

KW - thermosensation

KW - Trigeminal ganglion

UR - http://www.scopus.com/inward/record.url?scp=85061449622&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85061449622&partnerID=8YFLogxK

U2 - 10.1113/JP277385

DO - 10.1113/JP277385

M3 - Article

C2 - 30656684

AN - SCOPUS:85061449622

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

ER -