Cortical activation of accumbens hyperpolarization-active NMDARs mediates aversion-resistant alcohol intake

Nat Neurosci. 2013 Aug;16(8):1094-100. doi: 10.1038/nn.3445. Epub 2013 Jun 30.

Abstract

Compulsive drinking despite serious adverse medical, social and economic consequences is a characteristic of alcohol use disorders in humans. Although frontal cortical areas have been implicated in alcohol use disorders, little is known about the molecular mechanisms and pathways that sustain aversion-resistant intake. Here, we show that nucleus accumbens core (NAcore) NMDA-type glutamate receptors and medial prefrontal (mPFC) and insula glutamatergic inputs to the NAcore are necessary for aversion-resistant alcohol consumption in rats. Aversion-resistant intake was associated with a new type of NMDA receptor adaptation, in which hyperpolarization-active NMDA receptors were present at mPFC and insula but not amygdalar inputs in the NAcore. Accordingly, inhibition of Grin2c NMDA receptor subunits in the NAcore reduced aversion-resistant alcohol intake. None of these manipulations altered intake when alcohol was not paired with an aversive consequence. Our results identify a mechanism by which hyperpolarization-active NMDA receptors under mPFC- and insula-to-NAcore inputs sustain aversion-resistant alcohol intake.

Publication types

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

MeSH terms

  • Alcohol Deterrents / pharmacology*
  • Alcohol Drinking / blood
  • Alcohol Drinking / drug therapy
  • Alcohol Drinking / physiopathology*
  • Amygdala / chemistry
  • Animals
  • Avoidance Learning / physiology*
  • Bacterial Proteins / analysis
  • Cerebral Cortex / chemistry
  • Cerebral Cortex / physiopathology*
  • Conditioning, Operant
  • Drug Resistance / physiology*
  • Ethanol / blood
  • Excitatory Amino Acid Antagonists / pharmacology
  • Halorhodopsins / analysis
  • Luminescent Proteins / analysis
  • Male
  • Nerve Tissue Proteins / physiology*
  • Nucleus Accumbens / physiopathology*
  • Optogenetics
  • Patch-Clamp Techniques
  • Piperidines / pharmacology
  • Prefrontal Cortex / chemistry
  • Prefrontal Cortex / physiopathology*
  • Quinine / pharmacology*
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • Random Allocation
  • Rats
  • Rats, Wistar
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Receptors, N-Methyl-D-Aspartate / physiology*
  • Valine / analogs & derivatives
  • Valine / pharmacology

Substances

  • Alcohol Deterrents
  • Bacterial Proteins
  • Excitatory Amino Acid Antagonists
  • Grin2d protein, mouse
  • Halorhodopsins
  • Luminescent Proteins
  • NR2B NMDA receptor
  • Nerve Tissue Proteins
  • Piperidines
  • RNA, Small Interfering
  • Receptors, N-Methyl-D-Aspartate
  • yellow fluorescent protein, Bacteria
  • Ethanol
  • 2-amino-5-phosphopentanoic acid
  • Quinine
  • Valine
  • ifenprodil