Cargando…
Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex
Pain is a complex multidimensional experience encompassing sensory-discriminative, affective-motivational and cognitive-emotional components mediated by different neural mechanisms. Investigations of neurophysiological signals from simultaneous recordings of two or more cortical circuits may reveal...
Autores principales: | , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2019
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6492531/ https://www.ncbi.nlm.nih.gov/pubmed/31105532 http://dx.doi.org/10.3389/fncel.2019.00165 |
_version_ | 1783415158137159680 |
---|---|
author | Xiao, Zhengdong Martinez, Erik Kulkarni, Prathamesh M. Zhang, Qiaosheng Hou, Qianning Rosenberg, David Talay, Robert Shalot, Leor Zhou, Haocheng Wang, Jing Chen, Zhe Sage |
author_facet | Xiao, Zhengdong Martinez, Erik Kulkarni, Prathamesh M. Zhang, Qiaosheng Hou, Qianning Rosenberg, David Talay, Robert Shalot, Leor Zhou, Haocheng Wang, Jing Chen, Zhe Sage |
author_sort | Xiao, Zhengdong |
collection | PubMed |
description | Pain is a complex multidimensional experience encompassing sensory-discriminative, affective-motivational and cognitive-emotional components mediated by different neural mechanisms. Investigations of neurophysiological signals from simultaneous recordings of two or more cortical circuits may reveal important circuit mechanisms on cortical pain processing. The anterior cingulate cortex (ACC) and primary somatosensory cortex (S1) represent two most important cortical circuits related to sensory and affective processing of pain. Here, we recorded in vivo extracellular activity of the ACC and S1 simultaneously from male adult Sprague-Dale rats (n = 5), while repetitive noxious laser stimulations were delivered to animalÕs hindpaw during pain experiments. We identified spontaneous pain-like events based on stereotyped pain behaviors in rats. We further conducted systematic analyses of spike and local field potential (LFP) recordings from both ACC and S1 during evoked and spontaneous pain episodes. From LFP recordings, we found stronger phase-amplitude coupling (theta phase vs. gamma amplitude) in the S1 than the ACC (n = 10 sessions), in both evoked (p = 0.058) and spontaneous pain-like behaviors (p = 0.017, paired signed rank test). In addition, pain-modulated ACC and S1 neuronal firing correlated with the amplitude of stimulus-induced event-related potentials (ERPs) during evoked pain episodes. We further designed statistical and machine learning methods to detect pain signals by integrating ACC and S1 ensemble spikes and LFPs. Together, these results reveal differential coding roles between the ACC and S1 in cortical pain processing, as well as point to distinct neural mechanisms between evoked and putative spontaneous pain at both LFP and cellular levels. |
format | Online Article Text |
id | pubmed-6492531 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-64925312019-05-17 Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex Xiao, Zhengdong Martinez, Erik Kulkarni, Prathamesh M. Zhang, Qiaosheng Hou, Qianning Rosenberg, David Talay, Robert Shalot, Leor Zhou, Haocheng Wang, Jing Chen, Zhe Sage Front Cell Neurosci Cellular Neuroscience Pain is a complex multidimensional experience encompassing sensory-discriminative, affective-motivational and cognitive-emotional components mediated by different neural mechanisms. Investigations of neurophysiological signals from simultaneous recordings of two or more cortical circuits may reveal important circuit mechanisms on cortical pain processing. The anterior cingulate cortex (ACC) and primary somatosensory cortex (S1) represent two most important cortical circuits related to sensory and affective processing of pain. Here, we recorded in vivo extracellular activity of the ACC and S1 simultaneously from male adult Sprague-Dale rats (n = 5), while repetitive noxious laser stimulations were delivered to animalÕs hindpaw during pain experiments. We identified spontaneous pain-like events based on stereotyped pain behaviors in rats. We further conducted systematic analyses of spike and local field potential (LFP) recordings from both ACC and S1 during evoked and spontaneous pain episodes. From LFP recordings, we found stronger phase-amplitude coupling (theta phase vs. gamma amplitude) in the S1 than the ACC (n = 10 sessions), in both evoked (p = 0.058) and spontaneous pain-like behaviors (p = 0.017, paired signed rank test). In addition, pain-modulated ACC and S1 neuronal firing correlated with the amplitude of stimulus-induced event-related potentials (ERPs) during evoked pain episodes. We further designed statistical and machine learning methods to detect pain signals by integrating ACC and S1 ensemble spikes and LFPs. Together, these results reveal differential coding roles between the ACC and S1 in cortical pain processing, as well as point to distinct neural mechanisms between evoked and putative spontaneous pain at both LFP and cellular levels. Frontiers Media S.A. 2019-04-24 /pmc/articles/PMC6492531/ /pubmed/31105532 http://dx.doi.org/10.3389/fncel.2019.00165 Text en Copyright © 2019 Xiao, Martinez, Kulkarni, Zhang, Hou, Rosenberg, Talay, Shalot, Zhou, Wang and Chen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Cellular Neuroscience Xiao, Zhengdong Martinez, Erik Kulkarni, Prathamesh M. Zhang, Qiaosheng Hou, Qianning Rosenberg, David Talay, Robert Shalot, Leor Zhou, Haocheng Wang, Jing Chen, Zhe Sage Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex |
title | Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex |
title_full | Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex |
title_fullStr | Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex |
title_full_unstemmed | Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex |
title_short | Cortical Pain Processing in the Rat Anterior Cingulate Cortex and Primary Somatosensory Cortex |
title_sort | cortical pain processing in the rat anterior cingulate cortex and primary somatosensory cortex |
topic | Cellular Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6492531/ https://www.ncbi.nlm.nih.gov/pubmed/31105532 http://dx.doi.org/10.3389/fncel.2019.00165 |
work_keys_str_mv | AT xiaozhengdong corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT martinezerik corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT kulkarniprathameshm corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT zhangqiaosheng corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT houqianning corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT rosenbergdavid corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT talayrobert corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT shalotleor corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT zhouhaocheng corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT wangjing corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex AT chenzhesage corticalpainprocessingintheratanteriorcingulatecortexandprimarysomatosensorycortex |