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Evidence for “direct” and “indirect” pathways through the song system basal ganglia

Authors

  • Michael A. Farries,

    1. Department of Biology, University of Washington, Seattle, Washington 98195-6515
    2. Department of Otolaryngology, University of Washington, Seattle, Washington 98195-6515
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  • Long Ding,

    1. Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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  • David J. Perkel

    Corresponding author
    1. Department of Biology, University of Washington, Seattle, Washington 98195-6515
    2. Department of Otolaryngology, University of Washington, Seattle, Washington 98195-6515
    • Department of Otolaryngology, University of Washington, Box 356515, 1959 NE Pacific St., HSB BB1165, Seattle, WA 98195-6515
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Abstract

Song learning in oscine birds relies on a circuit known as the “anterior forebrain pathway,” which includes a specialized region of the avian basal ganglia. This region, area X, is embedded within a telencephalic structure considered homologous to the striatum, the input structure of the mammalian basal ganglia. Area X has many features in common with the mammalian striatum, yet has distinctive traits, including largely aspiny projection neurons that directly innervate the thalamus and a cell type that physiologically resembles neurons recorded in the mammalian globus pallidus. We have proposed that area X is a mixture of striatum and globus pallidus and has the same functional organization as circuits in the mammalian basal ganglia. Using electrophysiological and anatomical approaches, we found that area X contains a functional analog of the “direct” striatopallidothalamic pathway of mammals: axons of the striatal spiny neurons make close contacts on the somata and dendrites of pallidal cells. A subset of pallidal neurons project directly to the thalamus. Surprisingly, we found evidence that many pallidal cells may not project to the thalamus, but rather participate in a functional analog of the mammalian “indirect” pathway, which may oppose the effects of the direct pathway. Our results deepen our understanding of how information flows through area X and provide more support for the notion that song learning in oscines employs physiological mechanisms similar to basal ganglia-dependent forms of motor learning in mammals. J. Comp. Neurol. 484:93–104, 2005. © 2005 Wiley-Liss, Inc.

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