Postnatal development of tyrosine hydroxylase mRNA-expressing neurons in mouse neostriatum

Authors

  • Masao Masuda,

    1. Neuropathophysiology Research Group, Tokyo Metropolitan Institute of Gerontology, Itabashi, Tokyo, Japan
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    • Present address: Department of Pharmaceutical Sciences, Tokyo Metropolitan Institute of Public Health, Shinjuku, Tokyo 169-0073, Japan.

  • Masami Miura,

    1. Neuropathophysiology Research Group, Tokyo Metropolitan Institute of Gerontology, Itabashi, Tokyo, Japan
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  • Ritsuko Inoue,

    1. Neuropathophysiology Research Group, Tokyo Metropolitan Institute of Gerontology, Itabashi, Tokyo, Japan
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  • Michiko Imanishi,

    1. Department of System Neuroscience, Tokyo Metropolitan Institute for Neuroscience, Fuchu, Tokyo, Japan
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  • Sachiko Saino-Saito,

    1. Department of Anatomy and Cell Biology, Yamagata University School of Medicine, Yamagata, Japan
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    • Present address: Yamagata Prefectural Kahoku Hospital, Kahoku, Yamagata 999-3511, Japan.

  • Masahiko Takada,

    1. Department of System Neuroscience, Tokyo Metropolitan Institute for Neuroscience, Fuchu, Tokyo, Japan
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    • Present address: Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.

  • Kazuto Kobayashi,

    1. Department of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University School of Medicine, Fukushima, Japan
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  • Toshihiko Aosaki

    1. Neuropathophysiology Research Group, Tokyo Metropolitan Institute of Gerontology, Itabashi, Tokyo, Japan
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Toshihiko Aosaki, as above.
E-mail: aosaki@tmig.or.jp

Abstract

The striatum harbors a small number of tyrosine hydroxylase (TH) mRNA-containing GABAergic neurons that express TH immunoreactivity after dopamine depletion, some of which reportedly resembled striatal medium spiny projection neurons (MSNs). To clarify whether the TH mRNA-expressing neurons were a subset of MSNs, we characterized their postnatal development of electrophysiological and morphological properties using a transgenic mouse strain expressing enhanced green fluorescent protein (EGFP) under the control of the rat TH gene promoter. At postnatal day (P)1, EGFP-TH+ neurons were present as clusters in the striatum and, thereafter, gradually scattered ventromedially by P18 without regard to the striatal compartments. They were immunonegative for calbindin, but immunopositive for enkephalin (54.5%) and dynorphin (80.0%). Whole-cell patch-clamp recordings revealed at least two distinct neuronal types, termed EGFP-TH+ Type A and B. Whereas Type B neurons were aspiny and negative for the MSN marker dopamine- and cyclic AMP-regulated phosphoprotein of 32 kDa (DARPP-32), Type A neurons constituted 75% of the EGFP+ cells, had dendritic spines (24.6%), contained DARPP-32 (73.6%) and a proportion acquired TH immunoreactivity after injections of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and 3-nitropropionic acid. The membrane properties and N-methyl-d-aspartate : non-N-methyl-d-aspartate excitatory postsynaptic current ratio of Type A neurons were very similar to MSNs at P18. However, their resting membrane potentials and spike widths were statistically different from those of MSNs. In addition, the calbindin-like, DARPP-32-like and dynorphin B-like immunoreactivity of Type A neurons developed differently from that of MSNs in the matrix. Thus, Type A neurons closely resemble MSNs, but constitute a cell type distinct from classical MSNs.

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