Involvement of nucleus accumbens AMPA receptor trafficking in augmentation of D- amphetamine reward in food-restricted rats

Psychopharmacology (Berl). 2014 Aug;231(15):3055-63. doi: 10.1007/s00213-014-3476-7. Epub 2014 Feb 18.

Abstract

Rationale: Chronic food restriction (FR) increases behavioral responsiveness to drugs of abuse and associated environments. Pre- and postsynaptic neuroadaptations have been identified in the mesoaccumbens dopamine pathway of FR subjects but the mechanistic basis of increased drug reward magnitude remains unclear.

Objectives: Effects of FR on basal and D-amphetamine-induced trafficking of AMPA receptor subunits to the nucleus accumbens (NAc) postsynaptic density (PSD) were examined, and AMPA receptor involvement in augmentation of D-amphetamine reward was tested.

Materials and methods: FR and ad libitum fed (AL) rats were injected with D-amphetamine (2.5 mg/kg, i.p.) or vehicle. Brains were harvested and subcellular fractionation and Western analyses were used to assess AMPA receptor abundance in NAc homogenate and PSD fractions. A follow-up experiment used a curve-shift protocol of intracranial self-stimulation to assess the effect of 1-naphthylacetyl spermine (1-NASPM), a blocker of Ca(2+)-permeable AMPA receptors, on rewarding effects of D-amphetamine microinjected in NAc shell.

Results: FR increased GluA1 in the PSD, and D-amphetamine increased p-Ser845-GluA1, GluA1, GluA2, but not GluA3, with a greater effect in FR than AL rats. D-amphetamine lowered reward thresholds, with greater effects in FR than AL rats, and 1-NASPM selectively reversed the enhancing effect of FR.

Conclusions: Results suggest that FR leads to increased synaptic incorporation of GluA1 homomers to potentiate rewarding effects of appetitive stimuli and, as a maladaptive byproduct, D-amphetamine. The D-amphetamine-induced increase in synaptic p-Ser845-GluA1, GluA1, and GluA2 may contribute to the rewarding effect of D-amphetamine, but may also be a mechanism of synaptic strengthening and behavior modification.

Publication types

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

MeSH terms

  • Animals
  • Central Nervous System Stimulants / pharmacology*
  • Dextroamphetamine / pharmacology*
  • Excitatory Amino Acid Antagonists / pharmacology
  • Food Deprivation / physiology*
  • Male
  • Nucleus Accumbens / drug effects*
  • Nucleus Accumbens / physiopathology
  • Protein Transport / drug effects
  • Protein Transport / physiology
  • Rats, Sprague-Dawley
  • Receptors, AMPA / antagonists & inhibitors
  • Receptors, AMPA / metabolism*
  • Reward*
  • Self Stimulation
  • Spermine / analogs & derivatives
  • Spermine / pharmacology

Substances

  • Central Nervous System Stimulants
  • Excitatory Amino Acid Antagonists
  • Receptors, AMPA
  • glutamate receptor ionotropic, AMPA 3
  • 1-naphthylacetylspermine
  • Spermine
  • glutamate receptor ionotropic, AMPA 2
  • glutamate receptor ionotropic, AMPA 1
  • Dextroamphetamine