Accumbens D2-MSN hyperactivity drives antipsychotic-induced behavioral supersensitivity
Antipsychotic-induced dopamine supersensitivity, or behavioral supersensitivity, is a problematic consequence of long-term antipsychotic treatment characterized by the emergence of motor abnormalities, refractory symptoms, and rebound psychosis. The underlying mechanisms are unclear and no approache...
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| Veröffentlicht in: | Molecular psychiatry 2021-11, Vol.26 (11), p.6159-6169 |
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| creator | Kruyer, Anna Parrilla-Carrero, Jeffrey Powell, Courtney Brandt, Lasse Gutwinski, Stefan Angelis, Ariana Chalhoub, Reda M. Jhou, Thomas C. Kalivas, Peter W. Amato, Davide |
| description | Antipsychotic-induced dopamine supersensitivity, or behavioral supersensitivity, is a problematic consequence of long-term antipsychotic treatment characterized by the emergence of motor abnormalities, refractory symptoms, and rebound psychosis. The underlying mechanisms are unclear and no approaches exist to prevent or reverse these unwanted effects of antipsychotic treatment. Here we demonstrate that behavioral supersensitivity stems from long-lasting pre, post and perisynaptic plasticity, including insertion of Ca
2+
-permeable AMPA receptors and loss of D2 receptor-dependent inhibitory postsynaptic currents (IPSCs) in D2 receptor-expressing medium spiny neurons (D2-MSNs) in the nucleus accumbens core (NAcore). The resulting hyperexcitability, prominent in a subpopulation of D2-MSNs (21%), caused locomotor sensitization to cocaine and was associated with behavioral endophenotypes of antipsychotic treatment resistance and substance use disorder, including disrupted extinction learning and augmented cue-induced cocaine-seeking behavior. Chemogenetic restoration of IPSCs in D2-MSNs in the NAcore was sufficient to prevent antipsychotic-induced supersensitivity, pointing to an entirely novel therapeutic direction for overcoming this condition. |
| doi_str_mv | 10.1038/s41380-021-01235-6 |
| format | Article |
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2+
-permeable AMPA receptors and loss of D2 receptor-dependent inhibitory postsynaptic currents (IPSCs) in D2 receptor-expressing medium spiny neurons (D2-MSNs) in the nucleus accumbens core (NAcore). The resulting hyperexcitability, prominent in a subpopulation of D2-MSNs (21%), caused locomotor sensitization to cocaine and was associated with behavioral endophenotypes of antipsychotic treatment resistance and substance use disorder, including disrupted extinction learning and augmented cue-induced cocaine-seeking behavior. Chemogenetic restoration of IPSCs in D2-MSNs in the NAcore was sufficient to prevent antipsychotic-induced supersensitivity, pointing to an entirely novel therapeutic direction for overcoming this condition.</description><identifier>ISSN: 1359-4184</identifier><identifier>EISSN: 1476-5578</identifier><identifier>DOI: 10.1038/s41380-021-01235-6</identifier><identifier>PMID: 34349226</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13 ; 14/1 ; 14/19 ; 14/35 ; 42 ; 631/378 ; 64 ; 64/110 ; 692/699/476 ; 82 ; 96 ; 96/63 ; Antipsychotic Agents - pharmacology ; Antipsychotic drugs ; Antipsychotics ; Behavioral Sciences ; Biological Psychology ; Calcium permeability ; Cocaine ; Cocaine - pharmacology ; Complications and side effects ; Dopamine D2 receptors ; Health aspects ; Hyperactivity ; Immediate Communication ; Inhibitory postsynaptic potentials ; Medicine ; Medicine & Public Health ; Neurosciences ; Nucleus accumbens ; Nucleus Accumbens - metabolism ; Pharmacotherapy ; Psychiatry ; Psychosis ; Psychotropic drugs ; Receptors, Dopamine D1 - metabolism ; Receptors, Dopamine D2 - metabolism ; Spiny neurons ; Substance abuse treatment ; Treatment resistance ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><ispartof>Molecular psychiatry, 2021-11, Vol.26 (11), p.6159-6169</ispartof><rights>The Author(s) 2021</rights><rights>2021. The Author(s).</rights><rights>COPYRIGHT 2021 Nature Publishing Group</rights><rights>The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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-c607t-d35ef107b14549f58cd0d046957df81be638e5dff513e37bf974d8df83f7581c3</citedby><cites>FETCH-LOGICAL-c607t-d35ef107b14549f58cd0d046957df81be638e5dff513e37bf974d8df83f7581c3</cites><orcidid>0000-0003-3630-0147 ; 0000-0001-9267-9492 ; 0000-0001-9487-0119</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41380-021-01235-6$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41380-021-01235-6$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34349226$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kruyer, Anna</creatorcontrib><creatorcontrib>Parrilla-Carrero, Jeffrey</creatorcontrib><creatorcontrib>Powell, Courtney</creatorcontrib><creatorcontrib>Brandt, Lasse</creatorcontrib><creatorcontrib>Gutwinski, Stefan</creatorcontrib><creatorcontrib>Angelis, Ariana</creatorcontrib><creatorcontrib>Chalhoub, Reda M.</creatorcontrib><creatorcontrib>Jhou, Thomas C.</creatorcontrib><creatorcontrib>Kalivas, Peter W.</creatorcontrib><creatorcontrib>Amato, Davide</creatorcontrib><title>Accumbens D2-MSN hyperactivity drives antipsychotic-induced behavioral supersensitivity</title><title>Molecular psychiatry</title><addtitle>Mol Psychiatry</addtitle><addtitle>Mol Psychiatry</addtitle><description>Antipsychotic-induced dopamine supersensitivity, or behavioral supersensitivity, is a problematic consequence of long-term antipsychotic treatment characterized by the emergence of motor abnormalities, refractory symptoms, and rebound psychosis. The underlying mechanisms are unclear and no approaches exist to prevent or reverse these unwanted effects of antipsychotic treatment. Here we demonstrate that behavioral supersensitivity stems from long-lasting pre, post and perisynaptic plasticity, including insertion of Ca
2+
-permeable AMPA receptors and loss of D2 receptor-dependent inhibitory postsynaptic currents (IPSCs) in D2 receptor-expressing medium spiny neurons (D2-MSNs) in the nucleus accumbens core (NAcore). The resulting hyperexcitability, prominent in a subpopulation of D2-MSNs (21%), caused locomotor sensitization to cocaine and was associated with behavioral endophenotypes of antipsychotic treatment resistance and substance use disorder, including disrupted extinction learning and augmented cue-induced cocaine-seeking behavior. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kruyer, Anna</au><au>Parrilla-Carrero, Jeffrey</au><au>Powell, Courtney</au><au>Brandt, Lasse</au><au>Gutwinski, Stefan</au><au>Angelis, Ariana</au><au>Chalhoub, Reda M.</au><au>Jhou, Thomas C.</au><au>Kalivas, Peter W.</au><au>Amato, Davide</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Accumbens D2-MSN hyperactivity drives antipsychotic-induced behavioral supersensitivity</atitle><jtitle>Molecular psychiatry</jtitle><stitle>Mol Psychiatry</stitle><addtitle>Mol Psychiatry</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>26</volume><issue>11</issue><spage>6159</spage><epage>6169</epage><pages>6159-6169</pages><issn>1359-4184</issn><eissn>1476-5578</eissn><abstract>Antipsychotic-induced dopamine supersensitivity, or behavioral supersensitivity, is a problematic consequence of long-term antipsychotic treatment characterized by the emergence of motor abnormalities, refractory symptoms, and rebound psychosis. The underlying mechanisms are unclear and no approaches exist to prevent or reverse these unwanted effects of antipsychotic treatment. Here we demonstrate that behavioral supersensitivity stems from long-lasting pre, post and perisynaptic plasticity, including insertion of Ca
2+
-permeable AMPA receptors and loss of D2 receptor-dependent inhibitory postsynaptic currents (IPSCs) in D2 receptor-expressing medium spiny neurons (D2-MSNs) in the nucleus accumbens core (NAcore). The resulting hyperexcitability, prominent in a subpopulation of D2-MSNs (21%), caused locomotor sensitization to cocaine and was associated with behavioral endophenotypes of antipsychotic treatment resistance and substance use disorder, including disrupted extinction learning and augmented cue-induced cocaine-seeking behavior. Chemogenetic restoration of IPSCs in D2-MSNs in the NAcore was sufficient to prevent antipsychotic-induced supersensitivity, pointing to an entirely novel therapeutic direction for overcoming this condition.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>34349226</pmid><doi>10.1038/s41380-021-01235-6</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-3630-0147</orcidid><orcidid>https://orcid.org/0000-0001-9267-9492</orcidid><orcidid>https://orcid.org/0000-0001-9487-0119</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 13 14/1 14/19 14/35 42 631/378 64 64/110 692/699/476 82 96 96/63 Antipsychotic Agents - pharmacology Antipsychotic drugs Antipsychotics Behavioral Sciences Biological Psychology Calcium permeability Cocaine Cocaine - pharmacology Complications and side effects Dopamine D2 receptors Health aspects Hyperactivity Immediate Communication Inhibitory postsynaptic potentials Medicine Medicine & Public Health Neurosciences Nucleus accumbens Nucleus Accumbens - metabolism Pharmacotherapy Psychiatry Psychosis Psychotropic drugs Receptors, Dopamine D1 - metabolism Receptors, Dopamine D2 - metabolism Spiny neurons Substance abuse treatment Treatment resistance α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors |
| title | Accumbens D2-MSN hyperactivity drives antipsychotic-induced behavioral supersensitivity |
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