Phosphodiesterase 4 inhibition impairs cocaine-induced inhibitory synaptic plasticity and conditioned place preference

Neuropsychopharmacology. 2012 Oct;37(11):2377-87. doi: 10.1038/npp.2012.93. Epub 2012 Jun 20.

Abstract

Endocannabinoid-mediated long-term depression of inhibitory synaptic transmission (I-LTD) in the ventral tegmental area (VTA) is implicated in cocaine-induced inhibitory synaptic plasticity and behavioral effects. It remains poorly understood, however, how this I-LTD is regulated and whether this regulation affects cocaine-seeking behavior. I-LTD requires cyclic adenosine 3', 5'-monophosphate (cAMP)-dependent protein kinase A (PKA) signaling, raising the possibility that modulators of cAMP/PKA signaling may regulate I-LTD and the reinforcement behavior. Phosphodiesterase (PDE) 4 hydrolyses cAMP and terminates cAMP/PKA signaling. Here, we report that selective PDE4 inhibitors rolipram and Ro 20-1724 blocked I-LTD and acute depression of inhibitory postsynaptic currents (IPSCs) induced by D₂ dopamine receptor and cannabinoid CB₁ receptor agonists in VTA dopamine neurons. We also show that intra-VTA microinjections of PDE4 inhibitor rolipram impaired the acquisition, but not the expression, of conditioned place preference (CPP) to cocaine. Systemic administration of rolipram also increased cAMP response element-binding protein (CREB) phosphorylation and activation in the VTA. Together, our results suggest that blockade of cocaine-induced inhibitory synaptic plasticity (I-LTD) and enhancement of CREB activation are two putative cellular mechanisms by which PDE4 inhibition impairs the acquisition of cocaine CPP.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • CREB-Binding Protein / metabolism
  • Cocaine / administration & dosage*
  • Conditioning, Operant / drug effects*
  • Conditioning, Operant / physiology
  • Cyclic Nucleotide Phosphodiesterases, Type 4 / metabolism*
  • Dopamine / metabolism
  • Dopamine Uptake Inhibitors / administration & dosage*
  • Drug Administration Routes
  • Drug Interactions
  • Electric Stimulation
  • Enzyme Inhibitors / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / drug effects
  • Male
  • Microinjections
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / genetics*
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / drug effects
  • Tyrosine 3-Monooxygenase / metabolism
  • Valine / analogs & derivatives
  • Valine / pharmacology
  • Ventral Tegmental Area / cytology
  • Ventral Tegmental Area / drug effects

Substances

  • Dopamine Uptake Inhibitors
  • Enzyme Inhibitors
  • Excitatory Amino Acid Antagonists
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • 2-amino-5-phosphopentanoic acid
  • Tyrosine 3-Monooxygenase
  • CREB-Binding Protein
  • Cyclic Nucleotide Phosphodiesterases, Type 4
  • Valine
  • Cocaine
  • Dopamine