Preprodynorphin-expressing neurons constitute a large subgroup of somatostatin-expressing GABAergic interneurons in the mouse neocortex

Authors

  • Jaerin Sohn,

    1. Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    2. Research Fellow of Japan Society for the Promotion of Science (JSPS), Tokyo, Japan
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  • Hiroyuki Hioki,

    1. Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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  • Shinichiro Okamoto,

    1. Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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  • Takeshi Kaneko

    Corresponding author
    1. Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • Correspondence to: Takeshi Kaneko, M.D., Ph.D., Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan. E-mail: kaneko@mbs.med.kyoto-u.ac.jp

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ABSTRACT

Dynorphins, leumorphin, and neoendorphins are preprodynorphin (PPD)-derived peptides and ligands for κ-opioid receptors. Using an antibody to PPD C-terminal, we investigated the chemical and molecular characteristics of PPD-expressing neurons in mouse neocortex. PPD-immunopositive neuronal somata were distributed most frequently in layer 5 and less frequently in layers 2–4 and 6 throughout neocortical regions. Combined labeling of immunofluorescence and fluorescent mRNA signals revealed that almost all PPD-immunopositive neurons expressed glutamic acid decarboxylase but not vesicular glutamate transporter, indicating their γ-aminobutyric acid (GABA)ergic characteristics, and that PPD-immunopositive neurons accounted for 15% of GABAergic interneurons in the primary somatosensory area. As GABAergic interneurons were divided into several groups by specific markers, we further examined the chemical characteristics of PPD-expressing neurons by the double immunofluorescence labeling method. More than 95% of PPD-immunopositive neurons were also somatostatin (SOM)-immunopositive in the primary somatosensory, primary motor, orbitofrontal, and primary visual areas, but only 24% were SOM-immunopositive in the medial prefrontal cortex. In the primary somatosensory area, PPD-immunopositive neurons constituted 50%, 79%, 55%, and 17% of SOM-immunopositive neurons in layers 2–3, 4, 5, and 6, respectively. Although SOM-expressing neurons contained calretinin-, neuropeptide Y-, nitric oxide synthase-, and reelin-expressing neurons as subgroups, only reelin immunoreactivity was detected in many PPD-immunopositive neurons. These results indicate that PPD-expressing neurons constitute a large subgroup of SOM-expressing cortical interneurons, and the PPD/SOM-expressing GABAergic neurons might serve not only as inhibitory elements in the local cortical circuit, but also as modulators for cortical neurons expressing κ-opioid and/or SOM receptors. J. Comp. Neurol. 522:1506–1526, 2014. © 2013 Wiley Periodicals, Inc.

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