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The Journal of Neuroscience, August 24, 2005, 25(34):7743-7753; doi:10.1523/JNEUROSCI.1904-05.2005

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Behavioral/Systems/Cognitive
Subthalamic Neurons Coordinate Basal Ganglia Function through Differential Neural Pathways

Yasunobu Yasoshima,¹ Nobuyuki Kai,¹ Shigetaka Yoshida,³ Sadao Shiosaka,⁴ Yoshimasa Koyama,⁵ Yukihiko Kayama,² and Kazuto Kobayashi¹

¹Department of Molecular Genetics, Institute of Biomedical Sciences, and ²Department of Physiology, Fukushima Medical University School of Medicine, Fukushima 960-1295, Japan, ³Department of Anatomy, Asahikawa Medical College, Asahikawa 78-8510, Japan, ⁴Department of Structural Cellular Biology, Nara Institute of Science and Technology, Ikoma 606-8501, Japan, and ⁵Department of Science and Technology, Fukushima University, Fukushima 960-1296, Japan

The subthalamic nucleus (STN) is a key component of basal ganglia circuitry that mediates a variety of motor functions. The STN neurons send glutamatergic projections to the output structures of basal ganglia, including the substantia nigra pars reticulata (SNr) and the entopeduncular nucleus, and also innervate the globus pallidus (GP). However, the mechanism by which the STN regulates motor functions in the neural circuitry is not fully understood. Here we performed conditional ablation of the STN neurons by using immunotoxin-mediated cell targeting. We then analyzed dopamine (DA)-mediated motor behavior and firing activity of the SNr and GP neurons. Ablation of the STN neurons increased spontaneous movement and reduced hyperactivity in response to DA stimulation. Ablation of these neurons modulated the pattern and rate of spontaneous firing of the SNr neurons, although it did not substantially affect spontaneous firing of the GP neurons. The ablation attenuated DA-induced suppression of the firing rate of the SNr neurons and inhibited DA-induced elevation of the rate of the GP neurons. In addition, pharmacological blockade of GP activation in response to DA stimulation inhibited the suppression of SNr activity and the resultant motor activation. These results suggest that the STN neurons suppress spontaneous behavior through their direct projection to the output neurons and that, in response to DA, they contribute to expression of behavior by acting on the output neurons mainly through the GP-mediated pathways. We conclude that the STN coordinates motor behavior through differential neural pathways depending on the state of DA transmission.

Key words: dopamine; motor control; basal ganglia; subthalamic nucleus; firing activity; immunotoxin-mediated cell targeting

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Received Dec 17, 2004; revised July 13, 2005; accepted July 14, 2005.

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