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Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain

Authors

  • Almira Vazdarjanova,

    1. Synapses and Cognitive Neuroscience Center and Department of Neurology, School of Medicine, Medical College of Georgia, Augusta, Georgia 30912
    2. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
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  • Victor Ramirez-Amaya,

    1. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
    2. Deoartamento de Neurobiologia Conductual y Cognitiva, Instituto de Neurobiologia, Universidad Nacional Autonoma de Mexico
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  • Nathan Insel,

    1. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
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  • Thane K. Plummer,

    1. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
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  • Susanna Rosi,

    1. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
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  • Shoaib Chowdhury,

    1. Departments of Neuroscience and Neurology, Johns Hopkins University, Baltimore, Maryland 21205
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  • Dalia Mikhael,

    1. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
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  • Paul F. Worley,

    1. Departments of Neuroscience and Neurology, Johns Hopkins University, Baltimore, Maryland 21205
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  • John F. Guzowski,

    1. Department of Neurobiology and Behavior and Center for the Neurobiology of Learning and Memory, University of California, Irvine, California 92697
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  • Carol A. Barnes

    Corresponding author
    1. Arizona Research Laboratories, Division of Neural Systems, Memory and Aging; University of Arizona, Tucson, Arizona 85724
    2. Departments of Psychology and Neurology, University of Arizona, Tucson, Arizona 85724
    • University of Arizona, Neural Systems, Memory & Aging, Life Sciences North, Room 384, PO Box 245115, Tucson, AZ 85724
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Abstract

Active behavior, such as exploring a novel environment, induces the expression of the immediate-early gene Arc (activity-regulated cytoskeletal associated protein, or Arg 3.1) in many brain regions, including the hippocampus, neocortex, and striatum. Arc messenger ribonucleic acid and protein are localized in activated dendrites, and Arc protein is required for the maintenance of long-term potentiation and memory consolidation. Although previous evidence suggests that Arc is expressed in neurons, there is no direct demonstration that only neurons can express Arc. Furthermore, there is no characterization of the main neuronal types that express Arc. The data reported here show that behavior- or seizure-induced Arc expression in the hippocampus, primary somatosensory cortex, and dorsal striatum of rats colocalizes only with neuronal (NeuN-positive) and not with glial (GFAP-positive) cells. Furthermore, Arc was found exclusively in non-GABAergic α-CaMKII-positive hippocampal and neocortical neurons of rats that had explored a novel environment. Some GAD65/67-positive neurons in these regions were observed to express Arc, but only after a very strong stimulus (electroconvulsive seizure). In the dorsal striatum, spatial exploration induced Arc only in GABAergic and α-CaMKII-positive neurons. Combined, these results show that although a very strong stimulus (seizure) can induce Arc in a variety of neurons, behavior induces Arc in the CaMKII-positive principal neurons of the hippocampus, neocortex, and dorsal striatum. These results, coupled with recent in vitro findings of interactions between Arc and CaMKII, are consistent with the hypothesis that Arc and CaMKII act as plasticity partners to promote functional and/or structural synaptic modifications that accompany learning. J. Comp. Neurol. 498:317–329, 2006. © 2006 Wiley-Liss, Inc.

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