Extensive Overlap of Mu-Opioid and Nicotinic Sensitivity in Cortical Interneurons
We studied μ-opioid transmission in acute slices of rat neocortex using whole-cell recordings and single-cell reverse transcription–polymerase chain reaction. The μ-opioid receptor (MOR) was found in γ-aminobutyric acidergic (GABAergic) interneurons that were either layer I cells frequently expressi...
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| Veröffentlicht in: | Cerebral cortex (New York, N.Y. 1991) N.Y. 1991), 2007-08, Vol.17 (8), p.1948-1957 |
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| container_title | Cerebral cortex (New York, N.Y. 1991) |
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| creator | Férézou, Isabelle Hill, Elisa L. Cauli, Bruno Gibelin, Nathalie Kaneko, Takeshi Rossier, Jean Lambolez, Bertrand |
| description | We studied μ-opioid transmission in acute slices of rat neocortex using whole-cell recordings and single-cell reverse transcription–polymerase chain reaction. The μ-opioid receptor (MOR) was found in γ-aminobutyric acidergic (GABAergic) interneurons that were either layer I cells frequently expressing neuropeptide Y or layers II–V cells expressing vasoactive intestinal peptide and enkephalin (Enk). We found that μ-opioid agonists inhibit these interneurons that are selectively excited by nicotinic agonists. The extensive overlap of μ-opioid and nicotinic responsiveness allowed μ-opioid agonists to inhibit nicotinic excitation of responsive interneurons and of their GABAergic output onto pyramidal cells. Finally, nicotinic stimulation resulted in a dynamic sequence where GABAergic transmission was first enhanced and then depressed below its baseline. This latter disinhibitory effect was prevented by a μ-opioid antagonist, indicating that excitation of nicotinic-responsive interneurons induced the release of endogenous Enk, which in turn led to MOR activation. Our results suggest that neocortical μ-opioid transmission acts as an inhibitory feedback onto nicotinic-responsive interneurons, which may change network excitability and inhibition patterns during cholinergic excitation. |
| doi_str_mv | 10.1093/cercor/bhl104 |
| format | Article |
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The μ-opioid receptor (MOR) was found in γ-aminobutyric acidergic (GABAergic) interneurons that were either layer I cells frequently expressing neuropeptide Y or layers II–V cells expressing vasoactive intestinal peptide and enkephalin (Enk). We found that μ-opioid agonists inhibit these interneurons that are selectively excited by nicotinic agonists. The extensive overlap of μ-opioid and nicotinic responsiveness allowed μ-opioid agonists to inhibit nicotinic excitation of responsive interneurons and of their GABAergic output onto pyramidal cells. Finally, nicotinic stimulation resulted in a dynamic sequence where GABAergic transmission was first enhanced and then depressed below its baseline. This latter disinhibitory effect was prevented by a μ-opioid antagonist, indicating that excitation of nicotinic-responsive interneurons induced the release of endogenous Enk, which in turn led to MOR activation. Our results suggest that neocortical μ-opioid transmission acts as an inhibitory feedback onto nicotinic-responsive interneurons, which may change network excitability and inhibition patterns during cholinergic excitation.</description><identifier>ISSN: 1047-3211</identifier><identifier>EISSN: 1460-2199</identifier><identifier>DOI: 10.1093/cercor/bhl104</identifier><identifier>PMID: 17068095</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animals ; Cerebral Cortex ; Cerebral Cortex - drug effects ; Cerebral Cortex - physiology ; Electrophysiology ; enkephalin ; Enkephalins ; Enkephalins - biosynthesis ; Enkephalins - genetics ; Excitatory Postsynaptic Potentials ; Excitatory Postsynaptic Potentials - drug effects ; GABAergic interneuron ; gamma-Aminobutyric Acid ; gamma-Aminobutyric Acid - physiology ; Interneurons ; Interneurons - drug effects ; Interneurons - physiology ; Life Sciences ; Neocortex ; Neocortex - drug effects ; Neocortex - physiology ; Nerve Net ; Nerve Net - cytology ; Nerve Net - physiology ; Neurobiology ; Neurons and Cognition ; Nicotinic Agonists ; Nicotinic Agonists - pharmacology ; nicotinic receptor ; Patch-Clamp Techniques ; Potassium Channels ; Potassium Channels - drug effects ; Potassium Channels - metabolism ; Rats ; Rats, Wistar ; Receptors, Nicotinic ; Receptors, Nicotinic - drug effects ; Receptors, Nicotinic - genetics ; Receptors, Nicotinic - physiology ; Receptors, Opioid, mu ; Receptors, Opioid, mu - drug effects ; Receptors, Opioid, mu - genetics ; Receptors, Opioid, mu - physiology ; Reverse Transcriptase Polymerase Chain Reaction ; Synaptic Transmission ; Synaptic Transmission - genetics ; Synaptic Transmission - physiology ; μ-opioid receptor</subject><ispartof>Cerebral cortex (New York, N.Y. 1991), 2007-08, Vol.17 (8), p.1948-1957</ispartof><rights>2006 The Authors 2007</rights><rights>2006 The Authors</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c493t-6ee3cf69da48a9c5079977ea50c918650e759e83b2b739b0f52e21984cb417673</citedby><cites>FETCH-LOGICAL-c493t-6ee3cf69da48a9c5079977ea50c918650e759e83b2b739b0f52e21984cb417673</cites><orcidid>0000-0003-1471-4621 ; 0000-0001-7602-1295 ; 0000-0003-1821-2135 ; 0000-0002-0653-480X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,1578,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17068095$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00184047$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Férézou, Isabelle</creatorcontrib><creatorcontrib>Hill, Elisa L.</creatorcontrib><creatorcontrib>Cauli, Bruno</creatorcontrib><creatorcontrib>Gibelin, Nathalie</creatorcontrib><creatorcontrib>Kaneko, Takeshi</creatorcontrib><creatorcontrib>Rossier, Jean</creatorcontrib><creatorcontrib>Lambolez, Bertrand</creatorcontrib><title>Extensive Overlap of Mu-Opioid and Nicotinic Sensitivity in Cortical Interneurons</title><title>Cerebral cortex (New York, N.Y. 1991)</title><addtitle>Cereb Cortex</addtitle><description>We studied μ-opioid transmission in acute slices of rat neocortex using whole-cell recordings and single-cell reverse transcription–polymerase chain reaction. The μ-opioid receptor (MOR) was found in γ-aminobutyric acidergic (GABAergic) interneurons that were either layer I cells frequently expressing neuropeptide Y or layers II–V cells expressing vasoactive intestinal peptide and enkephalin (Enk). We found that μ-opioid agonists inhibit these interneurons that are selectively excited by nicotinic agonists. The extensive overlap of μ-opioid and nicotinic responsiveness allowed μ-opioid agonists to inhibit nicotinic excitation of responsive interneurons and of their GABAergic output onto pyramidal cells. Finally, nicotinic stimulation resulted in a dynamic sequence where GABAergic transmission was first enhanced and then depressed below its baseline. This latter disinhibitory effect was prevented by a μ-opioid antagonist, indicating that excitation of nicotinic-responsive interneurons induced the release of endogenous Enk, which in turn led to MOR activation. Our results suggest that neocortical μ-opioid transmission acts as an inhibitory feedback onto nicotinic-responsive interneurons, which may change network excitability and inhibition patterns during cholinergic excitation.</description><subject>Animals</subject><subject>Cerebral Cortex</subject><subject>Cerebral Cortex - drug effects</subject><subject>Cerebral Cortex - physiology</subject><subject>Electrophysiology</subject><subject>enkephalin</subject><subject>Enkephalins</subject><subject>Enkephalins - biosynthesis</subject><subject>Enkephalins - genetics</subject><subject>Excitatory Postsynaptic Potentials</subject><subject>Excitatory Postsynaptic Potentials - drug effects</subject><subject>GABAergic interneuron</subject><subject>gamma-Aminobutyric Acid</subject><subject>gamma-Aminobutyric Acid - physiology</subject><subject>Interneurons</subject><subject>Interneurons - drug effects</subject><subject>Interneurons - physiology</subject><subject>Life Sciences</subject><subject>Neocortex</subject><subject>Neocortex - drug effects</subject><subject>Neocortex - physiology</subject><subject>Nerve Net</subject><subject>Nerve Net - cytology</subject><subject>Nerve Net - physiology</subject><subject>Neurobiology</subject><subject>Neurons and Cognition</subject><subject>Nicotinic Agonists</subject><subject>Nicotinic Agonists - pharmacology</subject><subject>nicotinic receptor</subject><subject>Patch-Clamp Techniques</subject><subject>Potassium Channels</subject><subject>Potassium Channels - drug effects</subject><subject>Potassium Channels - metabolism</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Receptors, Nicotinic</subject><subject>Receptors, Nicotinic - drug effects</subject><subject>Receptors, Nicotinic - genetics</subject><subject>Receptors, Nicotinic - physiology</subject><subject>Receptors, Opioid, mu</subject><subject>Receptors, Opioid, mu - drug effects</subject><subject>Receptors, Opioid, mu - genetics</subject><subject>Receptors, Opioid, mu - physiology</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Synaptic Transmission</subject><subject>Synaptic Transmission - genetics</subject><subject>Synaptic Transmission - physiology</subject><subject>μ-opioid receptor</subject><issn>1047-3211</issn><issn>1460-2199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0UFvFCEUB3BibGytHr2aiYfGHqaFGRjg2KzVbbp2NWpsvBCGfZNSZ2EEZtN--7KZTZt46QlCfnmP9_4IvSP4hGBZnxoIxofT9qYnmL5AB4Q2uKyIlC_zHVNe1hUh--h1jLcYE16x6hXaJxw3Akt2gL6f3yVw0W6gWG4g9HoofFd8HcvlYL1dFdqtiitrfLLOmuLHlia7sem-sK6Y-ZCs0X1x4RIEB2PwLr5Be53uI7zdnYfo1-fzn7N5uVh-uZidLUpDZZ3KBqA2XSNXmgotDcNcSs5BM2wkEQ3DwJkEUbdVy2vZ4o5VkMcS1LSU8IbXh-h4qnujezUEu9bhXnlt1fxsobZveVxB8wY2JNujyQ7B_xshJrW20UDfawd-jIpjjpkg4llIJKdCVCzDD__BWz8GlwfORgjaSLZtW07IBB9jgO7xnwSrbXpqSk9N6WX_fld0bNewetK7uDL4OAE_Ds_W2vW2McHdI9bhr8rL40zNr_-o3-TT1aW4_qZo_QCgnLJL</recordid><startdate>20070801</startdate><enddate>20070801</enddate><creator>Férézou, Isabelle</creator><creator>Hill, Elisa L.</creator><creator>Cauli, Bruno</creator><creator>Gibelin, Nathalie</creator><creator>Kaneko, Takeshi</creator><creator>Rossier, Jean</creator><creator>Lambolez, Bertrand</creator><general>Oxford University Press</general><general>Oxford Publishing Limited (England)</general><general>Oxford University Press (OUP)</general><scope>BSCLL</scope><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>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0003-1471-4621</orcidid><orcidid>https://orcid.org/0000-0001-7602-1295</orcidid><orcidid>https://orcid.org/0000-0003-1821-2135</orcidid><orcidid>https://orcid.org/0000-0002-0653-480X</orcidid></search><sort><creationdate>20070801</creationdate><title>Extensive Overlap of Mu-Opioid and Nicotinic Sensitivity in Cortical Interneurons</title><author>Férézou, Isabelle ; 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The μ-opioid receptor (MOR) was found in γ-aminobutyric acidergic (GABAergic) interneurons that were either layer I cells frequently expressing neuropeptide Y or layers II–V cells expressing vasoactive intestinal peptide and enkephalin (Enk). We found that μ-opioid agonists inhibit these interneurons that are selectively excited by nicotinic agonists. The extensive overlap of μ-opioid and nicotinic responsiveness allowed μ-opioid agonists to inhibit nicotinic excitation of responsive interneurons and of their GABAergic output onto pyramidal cells. Finally, nicotinic stimulation resulted in a dynamic sequence where GABAergic transmission was first enhanced and then depressed below its baseline. This latter disinhibitory effect was prevented by a μ-opioid antagonist, indicating that excitation of nicotinic-responsive interneurons induced the release of endogenous Enk, which in turn led to MOR activation. Our results suggest that neocortical μ-opioid transmission acts as an inhibitory feedback onto nicotinic-responsive interneurons, which may change network excitability and inhibition patterns during cholinergic excitation.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>17068095</pmid><doi>10.1093/cercor/bhl104</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-1471-4621</orcidid><orcidid>https://orcid.org/0000-0001-7602-1295</orcidid><orcidid>https://orcid.org/0000-0003-1821-2135</orcidid><orcidid>https://orcid.org/0000-0002-0653-480X</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Animals Cerebral Cortex Cerebral Cortex - drug effects Cerebral Cortex - physiology Electrophysiology enkephalin Enkephalins Enkephalins - biosynthesis Enkephalins - genetics Excitatory Postsynaptic Potentials Excitatory Postsynaptic Potentials - drug effects GABAergic interneuron gamma-Aminobutyric Acid gamma-Aminobutyric Acid - physiology Interneurons Interneurons - drug effects Interneurons - physiology Life Sciences Neocortex Neocortex - drug effects Neocortex - physiology Nerve Net Nerve Net - cytology Nerve Net - physiology Neurobiology Neurons and Cognition Nicotinic Agonists Nicotinic Agonists - pharmacology nicotinic receptor Patch-Clamp Techniques Potassium Channels Potassium Channels - drug effects Potassium Channels - metabolism Rats Rats, Wistar Receptors, Nicotinic Receptors, Nicotinic - drug effects Receptors, Nicotinic - genetics Receptors, Nicotinic - physiology Receptors, Opioid, mu Receptors, Opioid, mu - drug effects Receptors, Opioid, mu - genetics Receptors, Opioid, mu - physiology Reverse Transcriptase Polymerase Chain Reaction Synaptic Transmission Synaptic Transmission - genetics Synaptic Transmission - physiology μ-opioid receptor |
| title | Extensive Overlap of Mu-Opioid and Nicotinic Sensitivity in Cortical Interneurons |
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