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Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats

Nociceptive information from the orofacial area projects to the trigeminal spinal subnucleus caudalis (Sp5C) and is then conveyed to several nuclei, including the parabrachial nucleus (PBN). The insular cortex (IC) receives orofacial nociceptive information and sends corticofugal projections to the...

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Autores principales: Nakaya, Yuka, Yamamoto, Kiyofumi, Kobayashi, Masayuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Wolters Kluwer 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9916064/
https://www.ncbi.nlm.nih.gov/pubmed/35969237
http://dx.doi.org/10.1097/j.pain.0000000000002755
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author Nakaya, Yuka
Yamamoto, Kiyofumi
Kobayashi, Masayuki
author_facet Nakaya, Yuka
Yamamoto, Kiyofumi
Kobayashi, Masayuki
author_sort Nakaya, Yuka
collection PubMed
description Nociceptive information from the orofacial area projects to the trigeminal spinal subnucleus caudalis (Sp5C) and is then conveyed to several nuclei, including the parabrachial nucleus (PBN). The insular cortex (IC) receives orofacial nociceptive information and sends corticofugal projections to the Sp5C. The Sp5C consists of glutamatergic and GABAergic/glycinergic interneurons that induce excitatory postsynaptic currents and inhibitory postsynaptic currents, respectively, in projection neurons. Therefore, quantification of glutamatergic IC inputs in combination with identifying postsynaptic neuronal subtypes is critical to elucidate IC roles in the regulation of Sp5C activities. We investigated features of synaptic transmission from the IC to glutamatergic and GABAergic/glycinergic Sp5C neurons of laminae I/II using vesicular GABA transporter-Venus transgenic rats that received an injection of adeno-associated virus-channelrhodopsin-2-mCherry into the IC. Selective stimulation of IC axon terminals in Sp5C slice preparations induced monosynaptic excitatory postsynaptic currents in both excitatory glutamatergic and inhibitory GABAergic/glycinergic Sp5C neurons with a comparable amplitude. Paired whole-cell patch-clamp recordings showed that unitary inhibitory postsynaptic currents from inhibitory neurons influencing excitatory neurons, including neurons projecting to the PBN, exhibited a high failure rate and were suppressed by both bicuculline and strychnine, suggesting that excitatory neurons in the Sp5C receive both GABAergic and glycinergic inhibition with low impact. Moreover, selective stimulation of IC axons increased the firing rate at the threshold responses. Finally, we demonstrated that selective stimulation of IC axons in the Sp5C by a chemogenetic approach decreased the thresholds of both mechanical and thermal nociception. Thus, IC projection to the Sp5C is likely to facilitate rather than suppress excitatory outputs from the Sp5C.
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spelling pubmed-99160642023-02-14 Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats Nakaya, Yuka Yamamoto, Kiyofumi Kobayashi, Masayuki Pain Research Paper Nociceptive information from the orofacial area projects to the trigeminal spinal subnucleus caudalis (Sp5C) and is then conveyed to several nuclei, including the parabrachial nucleus (PBN). The insular cortex (IC) receives orofacial nociceptive information and sends corticofugal projections to the Sp5C. The Sp5C consists of glutamatergic and GABAergic/glycinergic interneurons that induce excitatory postsynaptic currents and inhibitory postsynaptic currents, respectively, in projection neurons. Therefore, quantification of glutamatergic IC inputs in combination with identifying postsynaptic neuronal subtypes is critical to elucidate IC roles in the regulation of Sp5C activities. We investigated features of synaptic transmission from the IC to glutamatergic and GABAergic/glycinergic Sp5C neurons of laminae I/II using vesicular GABA transporter-Venus transgenic rats that received an injection of adeno-associated virus-channelrhodopsin-2-mCherry into the IC. Selective stimulation of IC axon terminals in Sp5C slice preparations induced monosynaptic excitatory postsynaptic currents in both excitatory glutamatergic and inhibitory GABAergic/glycinergic Sp5C neurons with a comparable amplitude. Paired whole-cell patch-clamp recordings showed that unitary inhibitory postsynaptic currents from inhibitory neurons influencing excitatory neurons, including neurons projecting to the PBN, exhibited a high failure rate and were suppressed by both bicuculline and strychnine, suggesting that excitatory neurons in the Sp5C receive both GABAergic and glycinergic inhibition with low impact. Moreover, selective stimulation of IC axons increased the firing rate at the threshold responses. Finally, we demonstrated that selective stimulation of IC axons in the Sp5C by a chemogenetic approach decreased the thresholds of both mechanical and thermal nociception. Thus, IC projection to the Sp5C is likely to facilitate rather than suppress excitatory outputs from the Sp5C. Wolters Kluwer 2023-03 2022-08-15 /pmc/articles/PMC9916064/ /pubmed/35969237 http://dx.doi.org/10.1097/j.pain.0000000000002755 Text en Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the International Association for the Study of Pain. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) , where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.
spellingShingle Research Paper
Nakaya, Yuka
Yamamoto, Kiyofumi
Kobayashi, Masayuki
Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
title Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
title_full Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
title_fullStr Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
title_full_unstemmed Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
title_short Descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
title_sort descending projections from the insular cortex to the trigeminal spinal subnucleus caudalis facilitate excitatory outputs to the parabrachial nucleus in rats
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9916064/
https://www.ncbi.nlm.nih.gov/pubmed/35969237
http://dx.doi.org/10.1097/j.pain.0000000000002755
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