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Synapse-specific opioid modulation of thalamo-cortico-striatal circuits
The medial thalamus (MThal), anterior cingulate cortex (ACC) and striatum play important roles in affective-motivational pain processing and reward learning. Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate tran...
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| Published in: | eLife 2019-05, Vol.8 |
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| description | The medial thalamus (MThal), anterior cingulate cortex (ACC) and striatum play important roles in affective-motivational pain processing and reward learning. Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate transmission between these brain regions in mouse. Mu-opioid receptor (MOR) agonists potently inhibited MThal inputs without affecting ACC inputs to individual striatal medium spiny neurons (MSNs). MOR activation also inhibited MThal inputs to the pyramidal neurons in the ACC. In contrast, delta-opioid receptor (DOR) agonists disinhibited ACC pyramidal neuron responses to MThal inputs by suppressing local feed-forward GABA signaling from parvalbumin-positive interneurons. As a result, DOR activation in the ACC facilitated poly-synaptic (thalamo-cortico-striatal) excitation of MSNs by MThal inputs. These results suggest that opioid effects on pain and reward may be shaped by the relative selectivity of opioid drugs to the specific circuit components. |
| doi_str_mv | 10.7554/elife.45146 |
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Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate transmission between these brain regions in mouse. Mu-opioid receptor (MOR) agonists potently inhibited MThal inputs without affecting ACC inputs to individual striatal medium spiny neurons (MSNs). MOR activation also inhibited MThal inputs to the pyramidal neurons in the ACC. In contrast, delta-opioid receptor (DOR) agonists disinhibited ACC pyramidal neuron responses to MThal inputs by suppressing local feed-forward GABA signaling from parvalbumin-positive interneurons. As a result, DOR activation in the ACC facilitated poly-synaptic (thalamo-cortico-striatal) excitation of MSNs by MThal inputs. These results suggest that opioid effects on pain and reward may be shaped by the relative selectivity of opioid drugs to the specific circuit components.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/elife.45146</identifier><identifier>PMID: 31099753</identifier><language>eng</language><publisher>England: eLife Science Publications, Ltd</publisher><subject>Agonists ; Analgesics, Opioid - metabolism ; Animals ; Brain ; Corpus Striatum - drug effects ; cortex ; Cortex (cingulate) ; Experiments ; feed-forward inhibition ; GABA ; Glutamate ; Gyrus Cinguli - drug effects ; Interneurons ; Learning - drug effects ; Legal fees ; Mice ; Narcotics ; Neostriatum ; Nerve Net - drug effects ; Neurons ; Neuroscience ; Neurosciences ; opioid ; opioid receptor ; Opioid receptors (type delta) ; Opioid receptors (type mu) ; Opioids ; Pain ; Parvalbumin ; Physiological aspects ; Prefrontal cortex ; Pyramidal cells ; Receptors, Opioid, delta - agonists ; Receptors, Opioid, mu - agonists ; Reinforcement ; Software ; Spiny neurons ; Statistical analysis ; Striatum ; Synapses ; Synapses - drug effects ; Thalamus ; Thalamus - drug effects ; γ-Aminobutyric acid</subject><ispartof>eLife, 2019-05, Vol.8</ispartof><rights>2019, Birdsong et al.</rights><rights>COPYRIGHT 2019 eLife Science Publications, Ltd.</rights><rights>2019, Birdsong et al. 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Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019, Birdsong et al 2019 Birdsong et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c642t-6a1704bcb75d5a6aeaed7945c7f0bd43723cdd4ee4f4b942c7d8b4a16ac7f18f3</citedby><cites>FETCH-LOGICAL-c642t-6a1704bcb75d5a6aeaed7945c7f0bd43723cdd4ee4f4b942c7d8b4a16ac7f18f3</cites><orcidid>0000-0003-4799-333X ; 0000-0002-3532-8319</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2233052673/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2233052673?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31099753$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Birdsong, William T</creatorcontrib><creatorcontrib>Jongbloets, Bart C</creatorcontrib><creatorcontrib>Engeln, Kim A</creatorcontrib><creatorcontrib>Wang, Dong</creatorcontrib><creatorcontrib>Scherrer, Grégory</creatorcontrib><creatorcontrib>Mao, Tianyi</creatorcontrib><title>Synapse-specific opioid modulation of thalamo-cortico-striatal circuits</title><title>eLife</title><addtitle>Elife</addtitle><description>The medial thalamus (MThal), anterior cingulate cortex (ACC) and striatum play important roles in affective-motivational pain processing and reward learning. Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate transmission between these brain regions in mouse. Mu-opioid receptor (MOR) agonists potently inhibited MThal inputs without affecting ACC inputs to individual striatal medium spiny neurons (MSNs). MOR activation also inhibited MThal inputs to the pyramidal neurons in the ACC. In contrast, delta-opioid receptor (DOR) agonists disinhibited ACC pyramidal neuron responses to MThal inputs by suppressing local feed-forward GABA signaling from parvalbumin-positive interneurons. As a result, DOR activation in the ACC facilitated poly-synaptic (thalamo-cortico-striatal) excitation of MSNs by MThal inputs. These results suggest that opioid effects on pain and reward may be shaped by the relative selectivity of opioid drugs to the specific circuit components.</description><subject>Agonists</subject><subject>Analgesics, Opioid - metabolism</subject><subject>Animals</subject><subject>Brain</subject><subject>Corpus Striatum - drug effects</subject><subject>cortex</subject><subject>Cortex (cingulate)</subject><subject>Experiments</subject><subject>feed-forward inhibition</subject><subject>GABA</subject><subject>Glutamate</subject><subject>Gyrus Cinguli - drug effects</subject><subject>Interneurons</subject><subject>Learning - drug effects</subject><subject>Legal fees</subject><subject>Mice</subject><subject>Narcotics</subject><subject>Neostriatum</subject><subject>Nerve Net - drug effects</subject><subject>Neurons</subject><subject>Neuroscience</subject><subject>Neurosciences</subject><subject>opioid</subject><subject>opioid receptor</subject><subject>Opioid receptors (type delta)</subject><subject>Opioid receptors (type mu)</subject><subject>Opioids</subject><subject>Pain</subject><subject>Parvalbumin</subject><subject>Physiological aspects</subject><subject>Prefrontal cortex</subject><subject>Pyramidal cells</subject><subject>Receptors, Opioid, delta - agonists</subject><subject>Receptors, Opioid, mu - agonists</subject><subject>Reinforcement</subject><subject>Software</subject><subject>Spiny neurons</subject><subject>Statistical analysis</subject><subject>Striatum</subject><subject>Synapses</subject><subject>Synapses - drug effects</subject><subject>Thalamus</subject><subject>Thalamus - drug effects</subject><subject>γ-Aminobutyric acid</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkl1rFDEUhgdRbKm98l4GvFHKrMnka-ZGKMXWhQXBKngXzuRjm2VmMiaZYv-9mW6tXTG5SDh5zpuTk7coXmO0EozRD6Z31qwow5Q_K45rxFCFGvrj-ZP9UXEa4w7lIWjT4PZlcUQwalvByHFxdX03whRNFSejnHWq9JPzTpeD13MPyfmx9LZMN9DD4CvlQ3LKVzEFBwn6UrmgZpfiq-KFhT6a04f1pPh--enbxedq8-VqfXG-qRSndao4YIFopzrBNAMOBowWLWVKWNRpSkRNlNbUGGpp19JaCd10FDCHTODGkpNivdfVHnZyCm6AcCc9OHkf8GErYSmxNxIUoQgLqkQWU4DbhguuWIsI47puIWt93GtNczcYrcyYAvQHoocno7uRW38rOaM415oF3j0IBP9zNjHJwUVl-h5G4-co65rghvKmXtC3_6A7P4cxt2qhCGI1F-QvtYX8ADdan-9Vi6g8Zy1vEOKYZWr1HypPbYb8OaOxLscPEt4fJGQmmV9pC3OMcn399ZA927Mq-BiDsY_9wEgulpNmky0n7y2X6TdPW_jI_jEY-Q2saNCl</recordid><startdate>20190517</startdate><enddate>20190517</enddate><creator>Birdsong, William T</creator><creator>Jongbloets, Bart C</creator><creator>Engeln, Kim A</creator><creator>Wang, Dong</creator><creator>Scherrer, Grégory</creator><creator>Mao, Tianyi</creator><general>eLife Science Publications, Ltd</general><general>eLife Sciences Publications Ltd</general><general>eLife Sciences Publications, Ltd</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>ISR</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-4799-333X</orcidid><orcidid>https://orcid.org/0000-0002-3532-8319</orcidid></search><sort><creationdate>20190517</creationdate><title>Synapse-specific opioid modulation of thalamo-cortico-striatal circuits</title><author>Birdsong, William T ; Jongbloets, Bart C ; Engeln, Kim A ; Wang, Dong ; Scherrer, Grégory ; Mao, Tianyi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c642t-6a1704bcb75d5a6aeaed7945c7f0bd43723cdd4ee4f4b942c7d8b4a16ac7f18f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Agonists</topic><topic>Analgesics, Opioid - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals (DOAJ)</collection><jtitle>eLife</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Birdsong, William T</au><au>Jongbloets, Bart C</au><au>Engeln, Kim A</au><au>Wang, Dong</au><au>Scherrer, Grégory</au><au>Mao, Tianyi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Synapse-specific opioid modulation of thalamo-cortico-striatal circuits</atitle><jtitle>eLife</jtitle><addtitle>Elife</addtitle><date>2019-05-17</date><risdate>2019</risdate><volume>8</volume><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>The medial thalamus (MThal), anterior cingulate cortex (ACC) and striatum play important roles in affective-motivational pain processing and reward learning. Opioids affect both pain and reward through uncharacterized modulation of this circuitry. This study examined opioid actions on glutamate transmission between these brain regions in mouse. Mu-opioid receptor (MOR) agonists potently inhibited MThal inputs without affecting ACC inputs to individual striatal medium spiny neurons (MSNs). MOR activation also inhibited MThal inputs to the pyramidal neurons in the ACC. In contrast, delta-opioid receptor (DOR) agonists disinhibited ACC pyramidal neuron responses to MThal inputs by suppressing local feed-forward GABA signaling from parvalbumin-positive interneurons. As a result, DOR activation in the ACC facilitated poly-synaptic (thalamo-cortico-striatal) excitation of MSNs by MThal inputs. These results suggest that opioid effects on pain and reward may be shaped by the relative selectivity of opioid drugs to the specific circuit components.</abstract><cop>England</cop><pub>eLife Science Publications, Ltd</pub><pmid>31099753</pmid><doi>10.7554/elife.45146</doi><orcidid>https://orcid.org/0000-0003-4799-333X</orcidid><orcidid>https://orcid.org/0000-0002-3532-8319</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Agonists Analgesics, Opioid - metabolism Animals Brain Corpus Striatum - drug effects cortex Cortex (cingulate) Experiments feed-forward inhibition GABA Glutamate Gyrus Cinguli - drug effects Interneurons Learning - drug effects Legal fees Mice Narcotics Neostriatum Nerve Net - drug effects Neurons Neuroscience Neurosciences opioid opioid receptor Opioid receptors (type delta) Opioid receptors (type mu) Opioids Pain Parvalbumin Physiological aspects Prefrontal cortex Pyramidal cells Receptors, Opioid, delta - agonists Receptors, Opioid, mu - agonists Reinforcement Software Spiny neurons Statistical analysis Striatum Synapses Synapses - drug effects Thalamus Thalamus - drug effects γ-Aminobutyric acid |
| title | Synapse-specific opioid modulation of thalamo-cortico-striatal circuits |
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