Exposure to cocaine alters dynorphin-mediated regulation of excitatory synaptic transmission in nucleus accumbens neurons

Biol Psychiatry. 2011 Feb 1;69(3):228-35. doi: 10.1016/j.biopsych.2010.09.014. Epub 2010 Oct 27.

Abstract

Background: Dysregulation of excitatory synaptic input to nucleus accumbens (NAc) medium spiny neurons (MSNs) underlies a key pathophysiology of drug addiction and addiction-associated emotional and motivational alterations. Dynorphin peptides, which exhibit higher affinity to κ type opioid receptors, are upregulated within the NAc upon exposure to cocaine administration, and the increased dynorphin-signaling in the NAc has been critically implicated in negative mood observed in cocaine- or stress-exposed animals. Despite such apparent behavioral significance of the NAc dynorphins, the understanding of how dynorphins regulate excitatory synaptic transmission in the NAc remains incomplete.

Methods: We used electrophysiological recording in brain slices to examine the effects of dynorphins on excitatory synaptic transmission in the NAc.

Results: We focused on two key dynorphins, dynorphin A and B. Our current results show that dynorphin A and B differentially regulated excitatory postsynaptic currents (EPSCs) in NAc MSNs. Whereas perfusions of both dynorphin A and B to NAc slices decreased EPSCs in MSNs, the effect of dynorphin A but not dynorphin B was completely reversed by the κ receptor-selective antagonist nor-binaltorphimine. These results implicate κ receptor-independent mechanisms in dynorphin B-mediated synaptic effects in the NAc. Furthermore, repeated exposure to cocaine (15 mg/kg/day via intraperitoneal injection for 5 days, with 1, 2, or 14 days withdrawal) completely abolished dynorphin A-mediated modulation of EPSCs in NAc MSNs, whereas the effect of dynorphin B remained largely unchanged.

Conclusions: Given the quantitatively higher abundance of dynorphin B in the NAc, our present results suggest that the dynorphin B-mediated, κ receptor-independent pathways predominate in the overall effect of dynorphins in cocaine-pretreated animals and potentially in cocaine-induced alterations in mood.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cocaine / pharmacology*
  • Drug Interactions
  • Dynorphins / pharmacology*
  • Dynorphins / physiology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Male
  • Naltrexone / analogs & derivatives
  • Naltrexone / pharmacology
  • Neurons / physiology
  • Nucleus Accumbens / drug effects*
  • Nucleus Accumbens / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Opioid, kappa / antagonists & inhibitors
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology*

Substances

  • Receptors, Opioid, kappa
  • norbinaltorphimine
  • Naltrexone
  • Dynorphins
  • Cocaine