Cargando…
A direct spino-cortical circuit bypassing the thalamus modulates nociception
Nociceptive signals are usually transmitted to layer 4 neurons in somatosensory cortex via the spinothalamic-thalamocortical pathway. The layer 5 corticospinal neurons in sensorimotor cortex are reported to receive the output of neurons in superficial layers; and their descending axons innervate the...
Autores principales: | , , , , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer Nature Singapore
2023
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10542357/ https://www.ncbi.nlm.nih.gov/pubmed/37311832 http://dx.doi.org/10.1038/s41422-023-00832-0 |
_version_ | 1785114078489870336 |
---|---|
author | Cai, Bing Wu, Dan Xie, Hong Chen, Yan Wang, Huadong Jin, Sen Song, Yuran Li, Anan Huang, Shiqi Wang, Sashuang Lu, Yingjin Bao, Lan Xu, Fuqiang Gong, Hui Li, Changlin Zhang, Xu |
author_facet | Cai, Bing Wu, Dan Xie, Hong Chen, Yan Wang, Huadong Jin, Sen Song, Yuran Li, Anan Huang, Shiqi Wang, Sashuang Lu, Yingjin Bao, Lan Xu, Fuqiang Gong, Hui Li, Changlin Zhang, Xu |
author_sort | Cai, Bing |
collection | PubMed |
description | Nociceptive signals are usually transmitted to layer 4 neurons in somatosensory cortex via the spinothalamic-thalamocortical pathway. The layer 5 corticospinal neurons in sensorimotor cortex are reported to receive the output of neurons in superficial layers; and their descending axons innervate the spinal cord to regulate basic sensorimotor functions. Here, we show that a subset of layer 5 neurons receives spinal inputs through a direct spino-cortical circuit bypassing the thalamus, and thus define these neurons as spino-cortical recipient neurons (SCRNs). Morphological studies revealed that the branches from spinal ascending axons formed a kind of disciform structure with the descending axons from SCRNs in the basilar pontine nucleus (BPN). Electron microscopy and calcium imaging further confirmed that the axon terminals from spinal ascending neurons and SCRNs made functional synaptic contacts in the BPN, linking the ascending sensory pathway to the descending motor control pathway. Furthermore, behavioral tests indicated that the spino-cortical connection in the BPN was involved in nociceptive responses. In vivo calcium imaging showed that SCRNs responded to peripheral noxious stimuli faster than neighboring layer 4 cortical neurons in awake mice. Manipulating activities of SCRNs could modulate nociceptive behaviors. Therefore, this direct spino-cortical circuit represents a noncanonical pathway, allowing a fast sensory-motor transition of the brain in response to noxious stimuli. |
format | Online Article Text |
id | pubmed-10542357 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Springer Nature Singapore |
record_format | MEDLINE/PubMed |
spelling | pubmed-105423572023-10-03 A direct spino-cortical circuit bypassing the thalamus modulates nociception Cai, Bing Wu, Dan Xie, Hong Chen, Yan Wang, Huadong Jin, Sen Song, Yuran Li, Anan Huang, Shiqi Wang, Sashuang Lu, Yingjin Bao, Lan Xu, Fuqiang Gong, Hui Li, Changlin Zhang, Xu Cell Res Article Nociceptive signals are usually transmitted to layer 4 neurons in somatosensory cortex via the spinothalamic-thalamocortical pathway. The layer 5 corticospinal neurons in sensorimotor cortex are reported to receive the output of neurons in superficial layers; and their descending axons innervate the spinal cord to regulate basic sensorimotor functions. Here, we show that a subset of layer 5 neurons receives spinal inputs through a direct spino-cortical circuit bypassing the thalamus, and thus define these neurons as spino-cortical recipient neurons (SCRNs). Morphological studies revealed that the branches from spinal ascending axons formed a kind of disciform structure with the descending axons from SCRNs in the basilar pontine nucleus (BPN). Electron microscopy and calcium imaging further confirmed that the axon terminals from spinal ascending neurons and SCRNs made functional synaptic contacts in the BPN, linking the ascending sensory pathway to the descending motor control pathway. Furthermore, behavioral tests indicated that the spino-cortical connection in the BPN was involved in nociceptive responses. In vivo calcium imaging showed that SCRNs responded to peripheral noxious stimuli faster than neighboring layer 4 cortical neurons in awake mice. Manipulating activities of SCRNs could modulate nociceptive behaviors. Therefore, this direct spino-cortical circuit represents a noncanonical pathway, allowing a fast sensory-motor transition of the brain in response to noxious stimuli. Springer Nature Singapore 2023-06-13 2023-10 /pmc/articles/PMC10542357/ /pubmed/37311832 http://dx.doi.org/10.1038/s41422-023-00832-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Cai, Bing Wu, Dan Xie, Hong Chen, Yan Wang, Huadong Jin, Sen Song, Yuran Li, Anan Huang, Shiqi Wang, Sashuang Lu, Yingjin Bao, Lan Xu, Fuqiang Gong, Hui Li, Changlin Zhang, Xu A direct spino-cortical circuit bypassing the thalamus modulates nociception |
title | A direct spino-cortical circuit bypassing the thalamus modulates nociception |
title_full | A direct spino-cortical circuit bypassing the thalamus modulates nociception |
title_fullStr | A direct spino-cortical circuit bypassing the thalamus modulates nociception |
title_full_unstemmed | A direct spino-cortical circuit bypassing the thalamus modulates nociception |
title_short | A direct spino-cortical circuit bypassing the thalamus modulates nociception |
title_sort | direct spino-cortical circuit bypassing the thalamus modulates nociception |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10542357/ https://www.ncbi.nlm.nih.gov/pubmed/37311832 http://dx.doi.org/10.1038/s41422-023-00832-0 |
work_keys_str_mv | AT caibing adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT wudan adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT xiehong adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT chenyan adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT wanghuadong adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT jinsen adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT songyuran adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT lianan adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT huangshiqi adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT wangsashuang adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT luyingjin adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT baolan adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT xufuqiang adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT gonghui adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT lichanglin adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT zhangxu adirectspinocorticalcircuitbypassingthethalamusmodulatesnociception AT caibing directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT wudan directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT xiehong directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT chenyan directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT wanghuadong directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT jinsen directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT songyuran directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT lianan directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT huangshiqi directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT wangsashuang directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT luyingjin directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT baolan directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT xufuqiang directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT gonghui directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT lichanglin directspinocorticalcircuitbypassingthethalamusmodulatesnociception AT zhangxu directspinocorticalcircuitbypassingthethalamusmodulatesnociception |