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The Journal of Neuroscience, July 27, 2005, 25(30):7054-7061; doi:10.1523/JNEUROSCI.1529-05.2005

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Behavioral/Systems/Cognitive
Homer2 Is Necessary for EtOH-Induced Neuroplasticity

Karen K. Szumlinski,¹ Kevin D. Lominac,¹ Erik B. Oleson,¹ Jennifer K. Walker,¹ Ashley Mason,¹ Marlin H. Dehoff,³ Matthias Klugman,⁴ Stephanie Cagle,¹ Kristine Welt,¹ Matthew During,⁵ Paul F. Worley,³ Lawrence D. Middaugh,^1,2 and Peter W. Kalivas¹

¹Department of Neurosciences and ²Department of Psychiatry and Behavioral Science and Charleston Alcohol Research Center, Medical University of South Carolina, Charleston, South Carolina 29425, ³Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, ⁴Interdisciplinary Center for Neurosciences, University of Heidelberg, 69123 Heidelberg, Germany, and ⁵Department of Molecular Medicine and Pathology, University of Auckland, Auckland 1003, New Zealand

Homer proteins are integral to the assembly of proteins regulating glutamate signaling and synaptic plasticity. Constitutive Homer2 gene deletion [knock-out (KO)] and rescue with adeno-associated viral (AAV) transfection of Homer2b was used to demonstrate the importance of Homer proteins in neuroplasticity produced by repeated ethanol (EtOH) administration. Homer2 KO mice avoided drinking high concentrations of EtOH and did not develop place preference or locomotor sensitization after repeated EtOH administration. The deficient behavioral plasticity to EtOH after Homer2 deletion was paralleled by a lack of augmentation in the rise in extracellular dopamine and glutamate elicited by repeated EtOH injections. The genotypic differences in EtOH-induced change in behavior and neurochemistry were essentially reversed by AAV-mediated transfection of Homer2b into accumbens cells including, differences in EtOH preference, locomotor sensitization, and EtOH-induced elevations in extracellular glutamate and dopamine. These data demonstrate a necessary and active role for accumbens Homer2 expression in regulating EtOH-induced behavioral and cellular neuroplasticity.

Key words: Homer proteins; EtOH; NMDA receptor; neuroplasticity; glutamate; dopamine

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Received April 19, 2005; revised May 24, 2005; accepted June 12, 2005.

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