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The Journal of Neuroscience, January 14, 2009, 29(2):444-453; doi:10.1523/JNEUROSCI.4029-08.2009

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Behavioral/Systems/Cognitive
Single Nigrostriatal Dopaminergic Neurons Form Widely Spread and Highly Dense Axonal Arborizations in the Neostriatum

Wakoto Matsuda,¹ Takahiro Furuta,¹ Kouichi C. Nakamura,^1,2 Hiroyuki Hioki,¹ Fumino Fujiyama,¹ Ryohachi Arai,³  and Takeshi Kaneko^1,2

¹Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan, ²Core Research for Evolutionary Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan, and ³Department of Anatomy, Shiga University of Medical Science, Otsu 520-2192, Japan

Correspondence should be addressed to Prof. Takeshi Kaneko, Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan. Email: kaneko{at}mbs.med.kyoto-u.ac.jp

The axonal arbors of single nigrostriatal dopaminergic neurons were visualized with a viral vector expressing membrane-targeted green fluorescent protein in rat brain. All eight reconstructed tyrosine hydroxylase-positive dopaminergic neurons possessed widely spread and highly dense axonal arborizations in the neostriatum. All of them emitted very little axon collateral arborization outside of the striatum except for tiny arborization in the external pallidum. The striatal axonal bush of each reconstructed dopaminergic neuron covered 0.45–5.7% (mean ± SD = 2.7 ± 1.5%) of the total volume of the neostriatum. Furthermore, all the dopaminergic neurons innervated both striosome and matrix compartments of the neostriatum, although each neuron's arborization tended to favor one of these compartments. Our findings demonstrate that individual dopaminergic neurons of the substantia nigra can broadcast a dopamine signal and exert strong influence over a large number of striatal neurons. This divergent signaling should be a key to the function of the nigrostriatal system in dopamine-based learning and suggests that neurodegeneration of individual nigral neurons can affect multiple neurons in the striatum. Thus, these results would also contribute to understanding the clinicopathology of Parkinson's disease and related syndromes.

Key words: dopamine; nigrostriatal; Parkinson's disease; reinforcement; striatum; tyrosine hydroxylase

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Received Aug. 23, 2008; revised Nov. 28, 2008; accepted Nov. 30, 2008.

Correspondence should be addressed to Prof. Takeshi Kaneko, Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan. Email: kaneko{at}mbs.med.kyoto-u.ac.jp

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