Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections

Glutamatergic projections from the medial prefrontal cortex (mPFC) to nucleus accumbens (NAc) contribute to cocaine relapse. Here we show that silent synapse-based remodeling of the two major mPFC-to-NAc projections differentially regulated the progressive increase in cue-induced cocaine seeking aft...

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Vydané v:	Neuron (Cambridge, Mass.) Ročník 83; číslo 6; s. 1453
Hlavní autori:	Ma, Yao-Ying, Lee, Brian R, Wang, Xiusong, Guo, Changyong, Liu, Lei, Cui, Ranji, Lan, Yan, Balcita-Pedicino, Judith J, Wolf, Marina E, Sesack, Susan R, Shaham, Yavin, Schlüter, Oliver M, Huang, Yanhua H, Dong, Yan
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States 17.09.2014
Predmet:	Animals Cocaine-Related Disorders - physiopathology Craving - physiology Drug-Seeking Behavior - physiology Electrophysiology Male Neural Pathways - drug effects Neural Pathways - physiopathology Neuronal Plasticity - physiology Nucleus Accumbens - drug effects Nucleus Accumbens - physiopathology Optogenetics Prefrontal Cortex - drug effects Prefrontal Cortex - physiopathology Rats Rats, Sprague-Dawley Synapses - drug effects Synapses - physiology
ISSN:	1097-4199, 1097-4199
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Abstract	Glutamatergic projections from the medial prefrontal cortex (mPFC) to nucleus accumbens (NAc) contribute to cocaine relapse. Here we show that silent synapse-based remodeling of the two major mPFC-to-NAc projections differentially regulated the progressive increase in cue-induced cocaine seeking after withdrawal (incubation of cocaine craving). Specifically, cocaine self-administration in rats generated AMPA receptor-silent glutamatergic synapses within both infralimbic (IL) and prelimbic mPFC (PrL) to NAc projections, measured after 1 day of withdrawal. After 45 days of withdrawal, IL-to-NAc silent synapses became unsilenced/matured by recruiting calcium-permeable (CP) AMPARs, whereas PrL-to-NAc silent synapses matured by recruiting non-CP-AMPARs, resulting in differential remodeling of these projections. Optogenetic reversal of silent synapse-based remodeling of IL-to-NAc and PrL-to-NAc projections potentiated and inhibited, respectively, incubation of cocaine craving on withdrawal day 45. Thus, pro- and antirelapse circuitry remodeling is induced in parallel after cocaine self-administration. These results may provide substrates for utilizing endogenous antirelapse mechanisms to reduce cocaine relapse.
AbstractList	Glutamatergic projections from the medial prefrontal cortex (mPFC) to nucleus accumbens (NAc) contribute to cocaine relapse. Here we show that silent synapse-based remodeling of the two major mPFC-to-NAc projections differentially regulated the progressive increase in cue-induced cocaine seeking after withdrawal (incubation of cocaine craving). Specifically, cocaine self-administration in rats generated AMPA receptor-silent glutamatergic synapses within both infralimbic (IL) and prelimbic mPFC (PrL) to NAc projections, measured after 1 day of withdrawal. After 45 days of withdrawal, IL-to-NAc silent synapses became unsilenced/matured by recruiting calcium-permeable (CP) AMPARs, whereas PrL-to-NAc silent synapses matured by recruiting non-CP-AMPARs, resulting in differential remodeling of these projections. Optogenetic reversal of silent synapse-based remodeling of IL-to-NAc and PrL-to-NAc projections potentiated and inhibited, respectively, incubation of cocaine craving on withdrawal day 45. Thus, pro- and antirelapse circuitry remodeling is induced in parallel after cocaine self-administration. These results may provide substrates for utilizing endogenous antirelapse mechanisms to reduce cocaine relapse. Glutamatergic projections from the medial prefrontal cortex (mPFC) to nucleus accumbens (NAc) contribute to cocaine relapse. Here we show that silent synapse-based remodeling of the two major mPFC-to-NAc projections differentially regulated the progressive increase in cue-induced cocaine seeking after withdrawal (incubation of cocaine craving). Specifically, cocaine self-administration in rats generated AMPA receptor-silent glutamatergic synapses within both infralimbic (IL) and prelimbic mPFC (PrL) to NAc projections, measured after 1 day of withdrawal. After 45 days of withdrawal, IL-to-NAc silent synapses became unsilenced/matured by recruiting calcium-permeable (CP) AMPARs, whereas PrL-to-NAc silent synapses matured by recruiting non-CP-AMPARs, resulting in differential remodeling of these projections. Optogenetic reversal of silent synapse-based remodeling of IL-to-NAc and PrL-to-NAc projections potentiated and inhibited, respectively, incubation of cocaine craving on withdrawal day 45. Thus, pro- and antirelapse circuitry remodeling is induced in parallel after cocaine self-administration. These results may provide substrates for utilizing endogenous antirelapse mechanisms to reduce cocaine relapse.Glutamatergic projections from the medial prefrontal cortex (mPFC) to nucleus accumbens (NAc) contribute to cocaine relapse. Here we show that silent synapse-based remodeling of the two major mPFC-to-NAc projections differentially regulated the progressive increase in cue-induced cocaine seeking after withdrawal (incubation of cocaine craving). Specifically, cocaine self-administration in rats generated AMPA receptor-silent glutamatergic synapses within both infralimbic (IL) and prelimbic mPFC (PrL) to NAc projections, measured after 1 day of withdrawal. After 45 days of withdrawal, IL-to-NAc silent synapses became unsilenced/matured by recruiting calcium-permeable (CP) AMPARs, whereas PrL-to-NAc silent synapses matured by recruiting non-CP-AMPARs, resulting in differential remodeling of these projections. Optogenetic reversal of silent synapse-based remodeling of IL-to-NAc and PrL-to-NAc projections potentiated and inhibited, respectively, incubation of cocaine craving on withdrawal day 45. Thus, pro- and antirelapse circuitry remodeling is induced in parallel after cocaine self-administration. These results may provide substrates for utilizing endogenous antirelapse mechanisms to reduce cocaine relapse.
Author	Ma, Yao-Ying Wolf, Marina E Shaham, Yavin Schlüter, Oliver M Wang, Xiusong Cui, Ranji Lee, Brian R Guo, Changyong Liu, Lei Dong, Yan Balcita-Pedicino, Judith J Sesack, Susan R Huang, Yanhua H Lan, Yan
Author_xml	– sequence: 1 givenname: Yao-Ying surname: Ma fullname: Ma, Yao-Ying organization: Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA – sequence: 2 givenname: Brian R surname: Lee fullname: Lee, Brian R organization: Allen Institute for Brain Science, Seattle, WA 98103, USA – sequence: 3 givenname: Xiusong surname: Wang fullname: Wang, Xiusong organization: Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15260, USA – sequence: 4 givenname: Changyong surname: Guo fullname: Guo, Changyong organization: Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA – sequence: 5 givenname: Lei surname: Liu fullname: Liu, Lei organization: School of Life Science, Northeastern Normal University, Jilin, China – sequence: 6 givenname: Ranji surname: Cui fullname: Cui, Ranji organization: School of Life Science, Northeastern Normal University, Jilin, China – sequence: 7 givenname: Yan surname: Lan fullname: Lan, Yan organization: Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA – sequence: 8 givenname: Judith J surname: Balcita-Pedicino fullname: Balcita-Pedicino, Judith J organization: Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA – sequence: 9 givenname: Marina E surname: Wolf fullname: Wolf, Marina E organization: Department of Neuroscience, Rosalind Franklin University of Medicine and Science, North Chicago, IL 60064, USA – sequence: 10 givenname: Susan R surname: Sesack fullname: Sesack, Susan R organization: Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA; Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15260, USA – sequence: 11 givenname: Yavin surname: Shaham fullname: Shaham, Yavin organization: Behavioral Neuroscience Branch, Intramural Research Program, NIDA, NIH, Baltimore, MD 21224, USA – sequence: 12 givenname: Oliver M surname: Schlüter fullname: Schlüter, Oliver M organization: Molecular Neurobiology and Cluster of Excellence "Nanoscale Microscopy and Molecular Physiology of the Brain," European Neuroscience Institute, 37077 Göttingen, Germany – sequence: 13 givenname: Yanhua H surname: Huang fullname: Huang, Yanhua H email: huangy3@upmc.edu organization: Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15260, USA. Electronic address: huangy3@upmc.edu – sequence: 14 givenname: Yan surname: Dong fullname: Dong, Yan email: yandong@pitt.edu organization: Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15260, USA; Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15260, USA. Electronic address: yandong@pitt.edu
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25199705$$D View this record in MEDLINE/PubMed
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PublicationTitle	Neuron (Cambridge, Mass.)
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PublicationYear	2014
References	25233302 - Neuron. 2014 Sep 17;83(6):1234-6 Neuron. 2014 Dec 17;84(6):1344-5
References_xml	– reference: 25233302 - Neuron. 2014 Sep 17;83(6):1234-6 – reference: - Neuron. 2014 Dec 17;84(6):1344-5
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Snippet	Glutamatergic projections from the medial prefrontal cortex (mPFC) to nucleus accumbens (NAc) contribute to cocaine relapse. Here we show that silent...
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SubjectTerms	Animals Cocaine-Related Disorders - physiopathology Craving - physiology Drug-Seeking Behavior - physiology Electrophysiology Male Neural Pathways - drug effects Neural Pathways - physiopathology Neuronal Plasticity - physiology Nucleus Accumbens - drug effects Nucleus Accumbens - physiopathology Optogenetics Prefrontal Cortex - drug effects Prefrontal Cortex - physiopathology Rats Rats, Sprague-Dawley Synapses - drug effects Synapses - physiology
Title	Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections
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