The anterior cingulate cortex controls the hyperactivity in subthalamic neurons in male mice with comorbid chronic pain and depression
Neurons in the subthalamic nucleus (STN) become hyperactive following nerve injury and promote pain-related responses in mice. Considering that the anterior cingulate cortex (ACC) is involved in pain and emotion processing and projects to the STN, we hypothesize that ACC neurons may contribute to hy...
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description | Neurons in the subthalamic nucleus (STN) become hyperactive following nerve injury and promote pain-related responses in mice. Considering that the anterior cingulate cortex (ACC) is involved in pain and emotion processing and projects to the STN, we hypothesize that ACC neurons may contribute to hyperactivity in STN neurons in chronic pain. In the present study, we showed that ACC neurons enhanced activity in response to noxious stimuli and to alterations in emotional states and became hyperactive in chronic pain state established by spared nerve injury of the sciatic nerve (SNI) in mice. In naïve mice, STN neurons were activated by noxious stimuli, but not by alterations in emotional states. Pain responses in STN neurons were attenuated in both naïve and SNI mice when ACC neurons were inhibited. Furthermore, optogenetic activation of the ACC-STN pathway induced bilateral hyperalgesia and depression-like behaviors in naive mice; conversely, inhibition of this pathway is sufficient to attenuate hyperalgesia and depression-like behaviors in SNI mice and naïve mice subjected to stimulation of STN neurons. Finally, mitigation of pain-like and depression-like behaviors in SNI mice by inhibition of the ACC-STN projection was eliminated by activation of STN neurons. Our results demonstrate that hyperactivity in the ACC-STN pathway may be an important pathophysiology in comorbid chronic pain and depression. Thus, the ACC-STN pathway may be an intervention target for the treatment of the comorbid chronic pain and depression. |
doi_str_mv | 10.1371/journal.pbio.3002518 |
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Considering that the anterior cingulate cortex (ACC) is involved in pain and emotion processing and projects to the STN, we hypothesize that ACC neurons may contribute to hyperactivity in STN neurons in chronic pain. In the present study, we showed that ACC neurons enhanced activity in response to noxious stimuli and to alterations in emotional states and became hyperactive in chronic pain state established by spared nerve injury of the sciatic nerve (SNI) in mice. In naïve mice, STN neurons were activated by noxious stimuli, but not by alterations in emotional states. Pain responses in STN neurons were attenuated in both naïve and SNI mice when ACC neurons were inhibited. Furthermore, optogenetic activation of the ACC-STN pathway induced bilateral hyperalgesia and depression-like behaviors in naive mice; conversely, inhibition of this pathway is sufficient to attenuate hyperalgesia and depression-like behaviors in SNI mice and naïve mice subjected to stimulation of STN neurons. Finally, mitigation of pain-like and depression-like behaviors in SNI mice by inhibition of the ACC-STN projection was eliminated by activation of STN neurons. Our results demonstrate that hyperactivity in the ACC-STN pathway may be an important pathophysiology in comorbid chronic pain and depression. Thus, the ACC-STN pathway may be an intervention target for the treatment of the comorbid chronic pain and depression.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3002518</identifier><identifier>PMID: 38386616</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Anterior cingulate cortex ; Behavior ; Biology and Life Sciences ; Care and treatment ; Chronic Pain ; Comorbidity ; Cortex (cingulate) ; Depression ; Depression, Mental ; Electrical stimuli ; Emotional factors ; Emotions ; Gyrus Cinguli - physiology ; Hyperactivity ; Hyperalgesia ; Influence ; Male ; Medicine and Health Sciences ; Mice ; Nerves ; Neurons ; Neurons - physiology ; Pain ; Pain perception ; Pathophysiology ; Research and Analysis Methods ; Sciatic nerve ; Social Sciences ; Solitary tract nucleus ; Stimuli ; Subthalamic nucleus ; Surgery ; Thalamus</subject><ispartof>PLoS biology, 2024-02, Vol.22 (2), p.e3002518-e3002518</ispartof><rights>Copyright: © 2024 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Wang et al 2024 Wang et al</rights><rights>2024 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c696t-10c2764d6e54d304f000abc7e87bf2e2f215b06f2af420b5e74fa93d5002ed053</citedby><cites>FETCH-LOGICAL-c696t-10c2764d6e54d304f000abc7e87bf2e2f215b06f2af420b5e74fa93d5002ed053</cites><orcidid>0000-0001-9649-7450</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10883538/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10883538/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38386616$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Ying-Di</creatorcontrib><creatorcontrib>Bao, Shu-Ting</creatorcontrib><creatorcontrib>Gao, Yuan</creatorcontrib><creatorcontrib>Chen, Jin</creatorcontrib><creatorcontrib>Jia, Tao</creatorcontrib><creatorcontrib>Yin, Cui</creatorcontrib><creatorcontrib>Cao, Jun-Li</creatorcontrib><creatorcontrib>Xiao, Cheng</creatorcontrib><creatorcontrib>Zhou, Chunyi</creatorcontrib><title>The anterior cingulate cortex controls the hyperactivity in subthalamic neurons in male mice with comorbid chronic pain and depression</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Neurons in the subthalamic nucleus (STN) become hyperactive following nerve injury and promote pain-related responses in mice. Considering that the anterior cingulate cortex (ACC) is involved in pain and emotion processing and projects to the STN, we hypothesize that ACC neurons may contribute to hyperactivity in STN neurons in chronic pain. In the present study, we showed that ACC neurons enhanced activity in response to noxious stimuli and to alterations in emotional states and became hyperactive in chronic pain state established by spared nerve injury of the sciatic nerve (SNI) in mice. In naïve mice, STN neurons were activated by noxious stimuli, but not by alterations in emotional states. Pain responses in STN neurons were attenuated in both naïve and SNI mice when ACC neurons were inhibited. Furthermore, optogenetic activation of the ACC-STN pathway induced bilateral hyperalgesia and depression-like behaviors in naive mice; conversely, inhibition of this pathway is sufficient to attenuate hyperalgesia and depression-like behaviors in SNI mice and naïve mice subjected to stimulation of STN neurons. Finally, mitigation of pain-like and depression-like behaviors in SNI mice by inhibition of the ACC-STN projection was eliminated by activation of STN neurons. Our results demonstrate that hyperactivity in the ACC-STN pathway may be an important pathophysiology in comorbid chronic pain and depression. Thus, the ACC-STN pathway may be an intervention target for the treatment of the comorbid chronic pain and depression.</description><subject>Analysis</subject><subject>Animals</subject><subject>Anterior cingulate cortex</subject><subject>Behavior</subject><subject>Biology and Life Sciences</subject><subject>Care and treatment</subject><subject>Chronic Pain</subject><subject>Comorbidity</subject><subject>Cortex (cingulate)</subject><subject>Depression</subject><subject>Depression, Mental</subject><subject>Electrical stimuli</subject><subject>Emotional factors</subject><subject>Emotions</subject><subject>Gyrus Cinguli - physiology</subject><subject>Hyperactivity</subject><subject>Hyperalgesia</subject><subject>Influence</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Mice</subject><subject>Nerves</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Pain</subject><subject>Pain perception</subject><subject>Pathophysiology</subject><subject>Research and Analysis Methods</subject><subject>Sciatic nerve</subject><subject>Social Sciences</subject><subject>Solitary tract nucleus</subject><subject>Stimuli</subject><subject>Subthalamic nucleus</subject><subject>Surgery</subject><subject>Thalamus</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk81u1DAQxyMEomXhDRBE4gKHXfwRx84JVRUfK1VUgsLVcpzJxlViL7ZTui_Ac-OwadVFPYB8GGv8m__YM54se47RClOO31660VvVr7a1cSuKEGFYPMiOMSvYkgvBHt7ZH2VPQrhMDKmIeJwdUUFFWeLyOPt10UGubARvnM-1sZuxVxFy7XyE62Rs9K4PeUxYt9uCVzqaKxN3ubF5GOvYqV4NRucWRu9smNyD6iFPPsh_mtgljcH52jS57hKR0K1KkLJN3sDWQwjG2afZo1b1AZ7NdpF9-_D-4vTT8uz84_r05Gypy6qMS4w04WXRlMCKhqKiRQipWnMQvG4JkJZgVqOyJaotCKoZ8KJVFW1Yejo0iNFF9nKvu-1dkHMJg6SorDDnJZuI9Z5onLqUW28G5XfSKSP_OJzfSOWj0T1IDJVgtKk10VXBOBWkUoxjEI1KN9Mkab2bs431AI2GVEzVH4genljTyY27khgJQVnq0iJ7PSt492OEEOVggoa-VxbcGCSpKEG4FGWV0Fd_ofc_b6Y2qUnS2NalxHoSlSdcMMF5gSdqdQ-VVgOpr85Ca5L_IODNQcD0b-A6btQYglx__fIf7Od_Z8-_H7LFntXeheChvS00RnIamZuCyGlk5DwyKezF3SbdBt3MCP0NrBETVQ</recordid><startdate>20240222</startdate><enddate>20240222</enddate><creator>Wang, Ying-Di</creator><creator>Bao, Shu-Ting</creator><creator>Gao, Yuan</creator><creator>Chen, Jin</creator><creator>Jia, Tao</creator><creator>Yin, Cui</creator><creator>Cao, Jun-Li</creator><creator>Xiao, Cheng</creator><creator>Zhou, Chunyi</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0001-9649-7450</orcidid></search><sort><creationdate>20240222</creationdate><title>The anterior cingulate cortex controls the hyperactivity in subthalamic neurons in male mice with comorbid chronic pain and depression</title><author>Wang, Ying-Di ; Bao, Shu-Ting ; Gao, Yuan ; Chen, Jin ; Jia, Tao ; Yin, Cui ; Cao, Jun-Li ; Xiao, Cheng ; Zhou, Chunyi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c696t-10c2764d6e54d304f000abc7e87bf2e2f215b06f2af420b5e74fa93d5002ed053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Anterior cingulate cortex</topic><topic>Behavior</topic><topic>Biology and Life Sciences</topic><topic>Care and treatment</topic><topic>Chronic Pain</topic><topic>Comorbidity</topic><topic>Cortex (cingulate)</topic><topic>Depression</topic><topic>Depression, Mental</topic><topic>Electrical stimuli</topic><topic>Emotional factors</topic><topic>Emotions</topic><topic>Gyrus Cinguli - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Ying-Di</au><au>Bao, Shu-Ting</au><au>Gao, Yuan</au><au>Chen, Jin</au><au>Jia, Tao</au><au>Yin, Cui</au><au>Cao, Jun-Li</au><au>Xiao, Cheng</au><au>Zhou, Chunyi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The anterior cingulate cortex controls the hyperactivity in subthalamic neurons in male mice with comorbid chronic pain and depression</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2024-02-22</date><risdate>2024</risdate><volume>22</volume><issue>2</issue><spage>e3002518</spage><epage>e3002518</epage><pages>e3002518-e3002518</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Neurons in the subthalamic nucleus (STN) become hyperactive following nerve injury and promote pain-related responses in mice. Considering that the anterior cingulate cortex (ACC) is involved in pain and emotion processing and projects to the STN, we hypothesize that ACC neurons may contribute to hyperactivity in STN neurons in chronic pain. In the present study, we showed that ACC neurons enhanced activity in response to noxious stimuli and to alterations in emotional states and became hyperactive in chronic pain state established by spared nerve injury of the sciatic nerve (SNI) in mice. In naïve mice, STN neurons were activated by noxious stimuli, but not by alterations in emotional states. Pain responses in STN neurons were attenuated in both naïve and SNI mice when ACC neurons were inhibited. Furthermore, optogenetic activation of the ACC-STN pathway induced bilateral hyperalgesia and depression-like behaviors in naive mice; conversely, inhibition of this pathway is sufficient to attenuate hyperalgesia and depression-like behaviors in SNI mice and naïve mice subjected to stimulation of STN neurons. Finally, mitigation of pain-like and depression-like behaviors in SNI mice by inhibition of the ACC-STN projection was eliminated by activation of STN neurons. Our results demonstrate that hyperactivity in the ACC-STN pathway may be an important pathophysiology in comorbid chronic pain and depression. Thus, the ACC-STN pathway may be an intervention target for the treatment of the comorbid chronic pain and depression.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38386616</pmid><doi>10.1371/journal.pbio.3002518</doi><orcidid>https://orcid.org/0000-0001-9649-7450</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animals Anterior cingulate cortex Behavior Biology and Life Sciences Care and treatment Chronic Pain Comorbidity Cortex (cingulate) Depression Depression, Mental Electrical stimuli Emotional factors Emotions Gyrus Cinguli - physiology Hyperactivity Hyperalgesia Influence Male Medicine and Health Sciences Mice Nerves Neurons Neurons - physiology Pain Pain perception Pathophysiology Research and Analysis Methods Sciatic nerve Social Sciences Solitary tract nucleus Stimuli Subthalamic nucleus Surgery Thalamus |
title | The anterior cingulate cortex controls the hyperactivity in subthalamic neurons in male mice with comorbid chronic pain and depression |
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