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

Yao Ying Ma, Brian R. Lee, Xiusong Wang, Changyong Guo, Lei Liu, Ranji Cui, Yan Lan, Judith J. Balcita-Pedicino, Marina Wolf, Susan R. Sesack, Yavin Shaham, Oliver M. Schlüter, Yanhua H. Huang, Yan Dong

Research output: Contribution to journalArticle

143 Citations (Scopus)

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 1day of withdrawal. After 45days 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.

Original languageEnglish (US)
Pages (from-to)1453-1467
Number of pages15
JournalNeuron
Volume83
Issue number6
DOIs
StatePublished - Jan 1 2014
Externally publishedYes

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Nucleus Accumbens
Prefrontal Cortex
Cocaine
Synapses
Self Administration
Optogenetics
Recurrence
AMPA Receptors
Craving
Cues
Calcium

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections. / Ma, Yao Ying; Lee, Brian R.; Wang, Xiusong; Guo, Changyong; Liu, Lei; Cui, Ranji; Lan, Yan; Balcita-Pedicino, Judith J.; Wolf, Marina; Sesack, Susan R.; Shaham, Yavin; Schlüter, Oliver M.; Huang, Yanhua H.; Dong, Yan.

In: Neuron, Vol. 83, No. 6, 01.01.2014, p. 1453-1467.

Research output: Contribution to journalArticle

Ma, YY, Lee, BR, Wang, X, Guo, C, Liu, L, Cui, R, Lan, Y, Balcita-Pedicino, JJ, Wolf, M, Sesack, SR, Shaham, Y, Schlüter, OM, Huang, YH & Dong, Y 2014, 'Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections', Neuron, vol. 83, no. 6, pp. 1453-1467. https://doi.org/10.1016/j.neuron.2014.08.023
Ma, Yao Ying ; Lee, Brian R. ; Wang, Xiusong ; Guo, Changyong ; Liu, Lei ; Cui, Ranji ; Lan, Yan ; Balcita-Pedicino, Judith J. ; Wolf, Marina ; Sesack, Susan R. ; Shaham, Yavin ; Schlüter, Oliver M. ; Huang, Yanhua H. ; Dong, Yan. / Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections. In: Neuron. 2014 ; Vol. 83, No. 6. pp. 1453-1467.
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