A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input

Authors

  • Samuel D. Gale,

    1. Graduate Program in Neurobiology and Behavior, University of Washington, Seattle, Washington 98195
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    • The first two authors contributed equally to this work.

  • Abigail L. Person,

    1. Graduate Program in Neurobiology and Behavior, University of Washington, Seattle, Washington 98195
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    • The first two authors contributed equally to this work.

  • David J. Perkel

    Corresponding author
    1. Departments of Biology and Otolaryngology, University of Washington, Seattle, Washington 98195
    • Departments of Biology and Otolaryngology, University of Washington, 1959 NE Pacific St. HSB BB1165 Box 356515, Seattle, WA 98195
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Abstract

Dopamine has been implicated in mediating contextual modulation of motor behaviors and learning in many species. In songbirds, dopamine may act on the basal ganglia nucleus Area X to influence the neural activity that contributes to vocal learning and contextual changes in song variability. Neurons in midbrain dopamine centers, the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA), densely innervate Area X and show singing-related changes in firing rate. In addition, dopamine levels in Area X change during singing. It is unknown, however, how song-related information could reach dopaminergic neurons. Here we report an anatomical pathway that could provide song-related information to the SNc and VTA. By using injections of bidirectionally transported fluorescent tracers in adult male zebra finches, we show that Area X and other song control nuclei do not project directly to the SNc or VTA. Instead, we describe an indirect pathway from Area X to midbrain dopaminergic neurons via a connection in the ventral pallidum (VP). Specifically, Area X projects to the VP via axon collaterals of Area X output neurons that also project to the thalamus. Dual injections revealed that the area of VP receiving input from Area X projects to the SNc and VTA. Furthermore, VP terminals in the SNc and VTA overlap with cells that project back to Area X. A portion of the arcopallium also projects to the SNc and VTA and could carry auditory information. These data demonstrate an anatomical loop through which Area X activity could influence its dopaminergic input. J. Comp. Neurol. 508:824–839, 2008. © 2008 Wiley-Liss, Inc.

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