Transcriptomes and neurotransmitter profiles of classes of gustatory and somatosensory neurons in the geniculate ganglion

Dvoryanchikov, Gennady; Hernández, Damián; Roebber, Jennifer K.; Hill, David L.; Roper, Stephen D.; Chaudhari, Nirupa

doi:10.1038/s41467-017-01095-1

Cited by 69 publications

(104 citation statements)

References 66 publications

(99 reference statements)

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“…) and elicits inward Na + currents in ∼1/4 of geniculate ganglion neurons (Nakamura & Bradley, ) despite the absence of TRPV1 expression in that ganglion (Dvoryanchikov et al . ). Further, topical capsaicin (and mustard oil) is well known to produce vasodilatation and increased blood flow (Jancso, ; Jancso et al .…”

Section: Discussionmentioning

confidence: 97%

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

Leijon

Neves

Breza

et al. 2019

The Journal of Physiology

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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.

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Section: Discussionmentioning

confidence: 97%

“…; Dvoryanchikov et al . ). In addition, we used GCaMP6s‐expressing mice generated by crossing floxed GCaMP6s mice (stock no.…”

Section: Methodsmentioning

confidence: 97%

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

Leijon

Neves

Breza

et al. 2019

The Journal of Physiology

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“…We used mice that express GCaMP3 as a knock-in/ knockout at the Pirt locus (obtained from X. Dong, Johns Hopkins). These mice have previously been reported to express GCaMP in all sensory neurons of the dorsal root, trigeminal, and geniculate ganglia (Kim et al 2014;Wu et al 2015;Dvoryanchikov et al 2017). In addition, we used GCaMP6s-expressing mice generated by crossing floxed GCaMP6s mice (stock no.…”

Section: Animalsmentioning

confidence: 97%

“…For instance, capsaicin, acting through TRPV1, increases intracellular cAMP, activates cGMP-protein kinase G and Ca 2+ /calmodulin-dependent protein kinase II pathways, and inhibits voltage-gated sodium and potassium channels (Liu et al 2001;Liu & Simon, 2003). Capsaicin also modulates potassium channels and inhibits neuronal action potentials via TRPV1-independent pathways (Pezzoli et al 2014;Yang et al 2014) and elicits inward Na + currents in ß1/4 of geniculate ganglion neurons (Nakamura & Bradley, 2011) despite the absence of TRPV1 expression in that ganglion (Dvoryanchikov et al 2017). Further, topical capsaicin (and mustard oil) is well known to produce vasodilatation and increased blood flow (Jancso, 1960;Jancso et al 1967;Helme & McKernan, 1985;Roberts et al 1992), which itself will alter the mucosal temperature and thus indirectly influence thermosensory responses (Wang et al 1995).…”

Section: Pretreatment With Menthol Affects Oral Thermosensory Respomentioning

confidence: 99%

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

Leijon

Neves

Simon

et al. 2018

Preprint

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Key pointsr Orosensory thermal trigeminal afferent neurons respond to cool, warm, and nociceptive hot temperatures with the majority activated in the cool range.r 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.r There is significant but incomplete overlap between afferent trigeminal neurons that respond to oral thermal stimulation and to the above chemesthetic compounds.r 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 plantsmenthol, 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 ß10% 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 Sara Leijon received her PhD degree at Karolinska Institutet in Stockholm in 2016. During her doctoral studies she used in vitro whole-cell patch-clamp electrophysiology to study the audio-vestibular brainstem. Currently she works as a postdoctoral research associate at the University of Miami. Her career is focused on sensory neurophysiology. She is currently using in vivo functional imaging to study the two sensory ganglia, geniculate and trigeminal, that innervate the orofacial region. Amanda Neves has a MSc degree in Biomedical Engineering and, in 2018, she obtained her PhD at the University of Campinas, Brazil, investigating neuron-glia communication in dorsal root ganglia in relation to inflammatory pain.S. C. M. Leijon and others J Physiol 597.7 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.

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“…Since PLCβ3 and IP 3 R3 are not expressed in the NTS (Figure S6) or the geniculate ganglia (Dvoryanchikov, Hernandez et al, 2017), our data suggest that input from both of these signaling molecules in taste cells is required for normal taste behavior. Moreover, if Type II and BR taste cells independently signal to the central taste system, then the loss of input from either cell population would be predicted to reduce the NTS activity proportionally to their contribution in taste processing.…”

Section: Discussionmentioning

confidence: 87%

A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli

Banik

Benfey

[]

et al. 2019

Preprint

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1Taste receptor cells use multiple signaling pathways to detect chemicals in 2 potential food items. These cells are functionally grouped into different types: Type I 3 cells act as support cells and have glial-like properties; Type II cells detect bitter, sweet, 4 and umami taste stimuli; and Type III cells detect sour and salty stimuli. We have 5 identified a new population of taste cells that are broadly tuned to multiple taste stimuli 6 including bitter, sweet, sour and umami. The goal of this study was to characterize 7 these broadly tuned (BR) taste cells. We used an IP3R3-KO mouse (does not release 8 calcium (Ca 2+ ) from Type II cells when stimulated with bitter, sweet or umami stimuli) to 9 characterize the BR cells without any potentially confounding input from Type II cells.

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Transcriptomes and neurotransmitter profiles of classes of gustatory and somatosensory neurons in the geniculate ganglion

Cited by 69 publications

References 66 publications

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

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

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

A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli

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