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Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli
1 Department of Oral Sciences, University of Minnesota, Minneapolis, Minnesota 55455 2 Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455 3 Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota 55455 4 Department of Anesthesiology, Yale Medical Scho...
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Published in: | Journal of neurophysiology 2004-01, Vol.91 (1), p.213-222 |
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creator | Simone, Donald A Zhang, Xijing Li, Jun Zhang, Jun-Ming Honda, Christopher N LaMotte, Robert H Giesler, Glenn J., Jr |
description | 1 Department of Oral Sciences, University of Minnesota, Minneapolis, Minnesota 55455
2 Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455
3 Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota 55455
4 Department of Anesthesiology, Yale Medical School, New Haven, Connecticut 06510
Submitted 30 May 2003;
accepted in final form 30 September 2003
We investigated the role of mechanosensitive spinothalamic tract (STT) neurons in mediating 1 ) the itch evoked by intradermal injection of histamine, 2 ) the enhanced sense of itch evoked by innocuous stroking (alloknesis), and 3 ) the enhanced pain evoked by punctate stimulation (hyperalgesia) of the skin surrounding the injection site. Responses to intradermal injections of histamine and capsaicin were compared in STT neurons recorded in either the superficial or the deep dorsal horn of the anesthetized monkey. Each neuron was identified by antidromic activation from the ventral posterior lateral nucleus of thalamus and classified by its initial responses to mechanical stimuli as wide dynamic range (WDR) or high-threshold (HT). Approximately half of the WDRs and one of the HTs responded weakly to histamine, some with a duration > 5 min, the maximal time allotted. WDRs but not HTs exhibited a significant increase in response to punctate stimulation after histamine consistent with their possible role in mediating histamine-induced hyperalgesia. Neither type of neuron exhibited significant changes in response to stroking, consistent with their unlikely role in mediating alloknesis. Furthermore, nearly all STT neurons exhibited vigorous and persistent responses to capsaicin, after which they became sensitized to stroking and to punctate stimulation. We conclude that the STT neurons in our sample are more likely to contribute to pain, allodynia, and hyperalgesia than to itch and alloknesis.
Address for reprint requests and other correspondence: D. A. Simone, Department of Oral Sciences, University of Minnesota, 515 Delaware St. SE, 17252 Moos, Minneapolis, MN 55455 (E-mail: simon003{at}umn.edu ). |
doi_str_mv | 10.1152/jn.00527.2003 |
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2 Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455
3 Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota 55455
4 Department of Anesthesiology, Yale Medical School, New Haven, Connecticut 06510
Submitted 30 May 2003;
accepted in final form 30 September 2003
We investigated the role of mechanosensitive spinothalamic tract (STT) neurons in mediating 1 ) the itch evoked by intradermal injection of histamine, 2 ) the enhanced sense of itch evoked by innocuous stroking (alloknesis), and 3 ) the enhanced pain evoked by punctate stimulation (hyperalgesia) of the skin surrounding the injection site. Responses to intradermal injections of histamine and capsaicin were compared in STT neurons recorded in either the superficial or the deep dorsal horn of the anesthetized monkey. Each neuron was identified by antidromic activation from the ventral posterior lateral nucleus of thalamus and classified by its initial responses to mechanical stimuli as wide dynamic range (WDR) or high-threshold (HT). Approximately half of the WDRs and one of the HTs responded weakly to histamine, some with a duration > 5 min, the maximal time allotted. WDRs but not HTs exhibited a significant increase in response to punctate stimulation after histamine consistent with their possible role in mediating histamine-induced hyperalgesia. Neither type of neuron exhibited significant changes in response to stroking, consistent with their unlikely role in mediating alloknesis. Furthermore, nearly all STT neurons exhibited vigorous and persistent responses to capsaicin, after which they became sensitized to stroking and to punctate stimulation. We conclude that the STT neurons in our sample are more likely to contribute to pain, allodynia, and hyperalgesia than to itch and alloknesis.
Address for reprint requests and other correspondence: D. A. Simone, Department of Oral Sciences, University of Minnesota, 515 Delaware St. SE, 17252 Moos, Minneapolis, MN 55455 (E-mail: simon003{at}umn.edu ).</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00527.2003</identifier><identifier>PMID: 14715718</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Action Potentials - drug effects ; Action Potentials - physiology ; Analysis of Variance ; Animals ; Capsaicin ; Electrophysiology ; Evoked Potentials ; Histamine ; Hot Temperature ; Hyperalgesia - chemically induced ; Hyperalgesia - etiology ; Hyperalgesia - physiopathology ; Injections, Intradermal - methods ; Laminectomy - methods ; Macaca fascicularis ; Physical Stimulation - methods ; Posterior Horn Cells - drug effects ; Posterior Horn Cells - physiology ; Pruritus - chemically induced ; Pruritus - physiopathology ; Reaction Time ; Skin - drug effects ; Skin - innervation ; Spinothalamic Tracts - cytology ; Spinothalamic Tracts - drug effects ; Spinothalamic Tracts - physiology ; Stimulation, Chemical ; Thalamus - anatomy & histology ; Thalamus - physiology ; Time Factors</subject><ispartof>Journal of neurophysiology, 2004-01, Vol.91 (1), p.213-222</ispartof><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c460t-b46946d9c7db26c4483084b70cf6026dd69b5a82acc284a8eb1b14701ae75c673</citedby><cites>FETCH-LOGICAL-c460t-b46946d9c7db26c4483084b70cf6026dd69b5a82acc284a8eb1b14701ae75c673</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/14715718$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Simone, Donald A</creatorcontrib><creatorcontrib>Zhang, Xijing</creatorcontrib><creatorcontrib>Li, Jun</creatorcontrib><creatorcontrib>Zhang, Jun-Ming</creatorcontrib><creatorcontrib>Honda, Christopher N</creatorcontrib><creatorcontrib>LaMotte, Robert H</creatorcontrib><creatorcontrib>Giesler, Glenn J., Jr</creatorcontrib><title>Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>1 Department of Oral Sciences, University of Minnesota, Minneapolis, Minnesota 55455
2 Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455
3 Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota 55455
4 Department of Anesthesiology, Yale Medical School, New Haven, Connecticut 06510
Submitted 30 May 2003;
accepted in final form 30 September 2003
We investigated the role of mechanosensitive spinothalamic tract (STT) neurons in mediating 1 ) the itch evoked by intradermal injection of histamine, 2 ) the enhanced sense of itch evoked by innocuous stroking (alloknesis), and 3 ) the enhanced pain evoked by punctate stimulation (hyperalgesia) of the skin surrounding the injection site. Responses to intradermal injections of histamine and capsaicin were compared in STT neurons recorded in either the superficial or the deep dorsal horn of the anesthetized monkey. Each neuron was identified by antidromic activation from the ventral posterior lateral nucleus of thalamus and classified by its initial responses to mechanical stimuli as wide dynamic range (WDR) or high-threshold (HT). Approximately half of the WDRs and one of the HTs responded weakly to histamine, some with a duration > 5 min, the maximal time allotted. WDRs but not HTs exhibited a significant increase in response to punctate stimulation after histamine consistent with their possible role in mediating histamine-induced hyperalgesia. Neither type of neuron exhibited significant changes in response to stroking, consistent with their unlikely role in mediating alloknesis. Furthermore, nearly all STT neurons exhibited vigorous and persistent responses to capsaicin, after which they became sensitized to stroking and to punctate stimulation. We conclude that the STT neurons in our sample are more likely to contribute to pain, allodynia, and hyperalgesia than to itch and alloknesis.
Address for reprint requests and other correspondence: D. A. Simone, Department of Oral Sciences, University of Minnesota, 515 Delaware St. SE, 17252 Moos, Minneapolis, MN 55455 (E-mail: simon003{at}umn.edu ).</description><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>Analysis of Variance</subject><subject>Animals</subject><subject>Capsaicin</subject><subject>Electrophysiology</subject><subject>Evoked Potentials</subject><subject>Histamine</subject><subject>Hot Temperature</subject><subject>Hyperalgesia - chemically induced</subject><subject>Hyperalgesia - etiology</subject><subject>Hyperalgesia - physiopathology</subject><subject>Injections, Intradermal - methods</subject><subject>Laminectomy - methods</subject><subject>Macaca fascicularis</subject><subject>Physical Stimulation - methods</subject><subject>Posterior Horn Cells - drug effects</subject><subject>Posterior Horn Cells - physiology</subject><subject>Pruritus - chemically induced</subject><subject>Pruritus - physiopathology</subject><subject>Reaction Time</subject><subject>Skin - drug effects</subject><subject>Skin - innervation</subject><subject>Spinothalamic Tracts - cytology</subject><subject>Spinothalamic Tracts - drug effects</subject><subject>Spinothalamic Tracts - physiology</subject><subject>Stimulation, Chemical</subject><subject>Thalamus - anatomy & histology</subject><subject>Thalamus - physiology</subject><subject>Time Factors</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><recordid>eNptkLtPwzAQxi0EgvIYWVEmtpSz83AyoooCUgWIltk4jtO6cuJgO4L-97i0iIXpXr_7dPchdIlhjHFGbtbdGCAjdEwAkgM0Cj0S46wsDtEIIOQJUHqCTp1bAwDNgByjE5xSnFFcjND7xLQ9t8qZLjJN9Cpdbzon3bZ4sarlXkbzXnXGr7jmrRLRwnLhoyc52ABG3gRssMqHCe_q6FYvzVJ2oZp71Q5anaOjhmsnL_bxDL1N7xaTh3j2fP84uZ3FIs3Bx1Wal2lel4LWFclFmhYJFGlFQTQ5kLyu87LKeEG4EKRIeSErXIUvAHNJM5HT5Axd73R7az4G6TxrlRNSa95JMziGS5IVADiA8Q4U1jhnZcP67Z92wzCwraVs3bEfS9nW0sBf7YWHqpX1H733MABkB6zUcvWprGT9auOU0Wa5YdNB64X88kG0xAwzghPW183fuf8thQN-4eQblDaR-w</recordid><startdate>20040101</startdate><enddate>20040101</enddate><creator>Simone, Donald A</creator><creator>Zhang, Xijing</creator><creator>Li, Jun</creator><creator>Zhang, Jun-Ming</creator><creator>Honda, Christopher N</creator><creator>LaMotte, Robert H</creator><creator>Giesler, Glenn J., Jr</creator><general>Am Phys Soc</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>7TK</scope></search><sort><creationdate>20040101</creationdate><title>Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli</title><author>Simone, Donald A ; Zhang, Xijing ; Li, Jun ; Zhang, Jun-Ming ; Honda, Christopher N ; LaMotte, Robert H ; Giesler, Glenn J., Jr</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c460t-b46946d9c7db26c4483084b70cf6026dd69b5a82acc284a8eb1b14701ae75c673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>Analysis of Variance</topic><topic>Animals</topic><topic>Capsaicin</topic><topic>Electrophysiology</topic><topic>Evoked Potentials</topic><topic>Histamine</topic><topic>Hot Temperature</topic><topic>Hyperalgesia - chemically induced</topic><topic>Hyperalgesia - etiology</topic><topic>Hyperalgesia - physiopathology</topic><topic>Injections, Intradermal - methods</topic><topic>Laminectomy - methods</topic><topic>Macaca fascicularis</topic><topic>Physical Stimulation - methods</topic><topic>Posterior Horn Cells - drug effects</topic><topic>Posterior Horn Cells - physiology</topic><topic>Pruritus - chemically induced</topic><topic>Pruritus - physiopathology</topic><topic>Reaction Time</topic><topic>Skin - drug effects</topic><topic>Skin - innervation</topic><topic>Spinothalamic Tracts - cytology</topic><topic>Spinothalamic Tracts - drug effects</topic><topic>Spinothalamic Tracts - physiology</topic><topic>Stimulation, Chemical</topic><topic>Thalamus - anatomy & histology</topic><topic>Thalamus - physiology</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Simone, Donald A</creatorcontrib><creatorcontrib>Zhang, Xijing</creatorcontrib><creatorcontrib>Li, Jun</creatorcontrib><creatorcontrib>Zhang, Jun-Ming</creatorcontrib><creatorcontrib>Honda, Christopher N</creatorcontrib><creatorcontrib>LaMotte, Robert H</creatorcontrib><creatorcontrib>Giesler, Glenn J., Jr</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Simone, Donald A</au><au>Zhang, Xijing</au><au>Li, Jun</au><au>Zhang, Jun-Ming</au><au>Honda, Christopher N</au><au>LaMotte, Robert H</au><au>Giesler, Glenn J., Jr</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2004-01-01</date><risdate>2004</risdate><volume>91</volume><issue>1</issue><spage>213</spage><epage>222</epage><pages>213-222</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>1 Department of Oral Sciences, University of Minnesota, Minneapolis, Minnesota 55455
2 Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455
3 Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota 55455
4 Department of Anesthesiology, Yale Medical School, New Haven, Connecticut 06510
Submitted 30 May 2003;
accepted in final form 30 September 2003
We investigated the role of mechanosensitive spinothalamic tract (STT) neurons in mediating 1 ) the itch evoked by intradermal injection of histamine, 2 ) the enhanced sense of itch evoked by innocuous stroking (alloknesis), and 3 ) the enhanced pain evoked by punctate stimulation (hyperalgesia) of the skin surrounding the injection site. Responses to intradermal injections of histamine and capsaicin were compared in STT neurons recorded in either the superficial or the deep dorsal horn of the anesthetized monkey. Each neuron was identified by antidromic activation from the ventral posterior lateral nucleus of thalamus and classified by its initial responses to mechanical stimuli as wide dynamic range (WDR) or high-threshold (HT). Approximately half of the WDRs and one of the HTs responded weakly to histamine, some with a duration > 5 min, the maximal time allotted. WDRs but not HTs exhibited a significant increase in response to punctate stimulation after histamine consistent with their possible role in mediating histamine-induced hyperalgesia. Neither type of neuron exhibited significant changes in response to stroking, consistent with their unlikely role in mediating alloknesis. Furthermore, nearly all STT neurons exhibited vigorous and persistent responses to capsaicin, after which they became sensitized to stroking and to punctate stimulation. We conclude that the STT neurons in our sample are more likely to contribute to pain, allodynia, and hyperalgesia than to itch and alloknesis.
Address for reprint requests and other correspondence: D. A. Simone, Department of Oral Sciences, University of Minnesota, 515 Delaware St. SE, 17252 Moos, Minneapolis, MN 55455 (E-mail: simon003{at}umn.edu ).</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>14715718</pmid><doi>10.1152/jn.00527.2003</doi><tpages>10</tpages></addata></record> |
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source | American Physiological Society:Jisc Collections:American Physiological Society Journals ‘Read Publish & Join’ Agreement:2023-2024 (Reading list); American Physiological Society Free |
subjects | Action Potentials - drug effects Action Potentials - physiology Analysis of Variance Animals Capsaicin Electrophysiology Evoked Potentials Histamine Hot Temperature Hyperalgesia - chemically induced Hyperalgesia - etiology Hyperalgesia - physiopathology Injections, Intradermal - methods Laminectomy - methods Macaca fascicularis Physical Stimulation - methods Posterior Horn Cells - drug effects Posterior Horn Cells - physiology Pruritus - chemically induced Pruritus - physiopathology Reaction Time Skin - drug effects Skin - innervation Spinothalamic Tracts - cytology Spinothalamic Tracts - drug effects Spinothalamic Tracts - physiology Stimulation, Chemical Thalamus - anatomy & histology Thalamus - physiology Time Factors |
title | Comparison of Responses of Primate Spinothalamic Tract Neurons to Pruritic and Algogenic Stimuli |
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