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The Journal of Neuroscience, July 25, 2007, 27(30):7921-7928; doi:10.1523/JNEUROSCI.1859-07.2007

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Behavioral/Systems/Cognitive
Cocaine Experience Controls Bidirectional Synaptic Plasticity in the Nucleus Accumbens

Saïd Kourrich,¹ Patrick E. Rothwell,^1,2 Jason R. Klug,¹ and Mark J. Thomas^1,2

¹Departments of Neuroscience and Psychology and Institute of Human Genetics, and ²Graduate Program in Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455

Correspondence should be addressed to Dr. Mark J. Thomas, University of Minnesota, 6-145 Jackson Hall, 321 Church Street Southeast, Minneapolis, MN 55455. Email: tmhomas{at}umn.edu

Plasticity of glutamatergic synapses is a fundamental mechanism through which experience changes neural function to impact future behavior. In animal models of addiction, glutamatergic signaling in the nucleus accumbens (NAc) exerts powerful control over drug-seeking behavior. However, little is known about whether, how or when experience with drugs may trigger synaptic plasticity in this key nucleus. Using whole-cell synaptic physiology in NAc brain slices, we demonstrate that a progression of bidirectional changes in glutamatergic synaptic strength occurs after repeated in vivo exposure to cocaine. During a protracted drug-free period, NAc neurons from cocaine-experienced mice develop a robust potentiation of AMPAR-mediated synaptic transmission. However, a single re-exposure to cocaine during extended withdrawal becomes a potent stimulus for synaptic depression, abruptly reversing the initial potentiation. These enduring modifications in AMPAR-mediated responses and plasticity may provide a neural substrate for disrupted processing of drug-related stimuli in drug-experienced individuals.

Key words: AMPAR; NMDAR; metaplasticity; synaptic scaling; long-term depression; psychostimulant; addiction

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Received Dec. 20, 2006; revised June 11, 2007; accepted June 11, 2007.

Correspondence should be addressed to Dr. Mark J. Thomas, University of Minnesota, 6-145 Jackson Hall, 321 Church Street Southeast, Minneapolis, MN 55455. Email: tmhomas{at}umn.edu

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Cocaine Experience Guides Dynamic Changes in AMPA Receptors within the Nucleus Accumbens

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