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

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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 Ca2+-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.

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Acknowledgements

This research was supported by DA003956 (K.D. C.) and 5T32 DA007254 (X-X. P) from the National Institute on Drug Abuse, and NS061920 from the National Institute on Neurological Disorders and Stroke (E.B.Z.).

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Authors and Affiliations

  1. Department of Psychiatry, New York University School of Medicine, 550 First Avenue, New York, NY, 10016, USA

    Xing-Xiang Peng, Soledad Cabeza de Vaca & Kenneth D. Carr

  2. Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, 550 First Avenue, New York, NY, 10016, USA

    Edward B. Ziff & Kenneth D. Carr

  3. Alexandria Center for Life Sciences, 450 East 29th Street, New York, NY, 10016, USA

    Kenneth D. Carr

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  1. Xing-Xiang Peng
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  2. Soledad Cabeza de Vaca
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  4. Kenneth D. Carr
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Correspondence to Kenneth D. Carr.

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Peng, XX., Cabeza de Vaca, S., Ziff, E.B. et al. Involvement of nucleus accumbens AMPA receptor trafficking in augmentation of D- amphetamine reward in food-restricted rats. Psychopharmacology 231, 3055–3063 (2014). https://doi.org/10.1007/s00213-014-3476-7

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