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Distribution of excitatory and inhibitory axon terminals on the rat hypoglossal motoneurons

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Abstract

Detailed information about the excitatory and inhibitory synapses on the hypoglossal motoneurons may help understand the neural mechanism for control of the hypoglossal motoneuron excitability and hence the precise and coordinated movements of the tongue during chewing, swallowing and licking. For this, we investigated the distribution of GABA-, glycine (Gly)- and glutamate (Glut)-immunopositive (+) axon terminals on the genioglossal (GG) motoneurons by retrograde tracing, electron microscopic immunohistochemistry, and quantitative analysis. Small GG motoneurons (< 400 μm2 in cross-sectional area) had fewer primary dendrites, significantly higher nuclear/cytoplasmic ratio, and smaller membrane area covered by synaptic boutons than large GG motoneurons (> 400 μm2). The fraction of inhibitory boutons (GABA + only, Gly + only, and mixed GABA +/Gly + boutons) of all boutons was significantly higher for small GG motoneurons than for large ones, whereas the fraction of Glut + boutons was significantly higher for large GG motoneurons than for small ones. Almost all boutons (> 95%) on both small and large GG motoneurons were GABA + , Gly + or Glut + . The frequency of mixed GABA +/Gly + boutons was the highest among inhibitory boutons types for both small and large GG motoneurons. These findings may elucidate the anatomical substrate for precise regulation of the motoneuron firing required for the fine movements of the tongue, and also suggest that the excitability of small and large GG motoneurons may be regulated differently.

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Acknowledgements

The authors sincerely thank Dr. Juli Valtschanoff for helpful discussion and careful reading of the manuscript. We also sincerely thank Dr. O.P. Ottersen for the gift of the glutamate, GABA and glycine antibodies and the sandwich block for the test sections.

Funding

This work was supported by the National Research Foundation of Korea (NRF) Grant funded by the Korea government (MSIT, NRF-2017R1A5A2015391, NRF-2017R1A2B2003561).

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  1. Sang Kyoo Paik, Hong Il Yoo, Seung Ki Choi contributed equally to this work.

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  1. Department of Anatomy and Neurobiology, School of Dentistry, Kyungpook National University, 188-1, 2-Ga, Samdeok-Dong, Jung-Gu, Daegu, 700-412, South Korea

    Sang Kyoo Paik, Seung Ki Choi, Jin Young Bae, Sook Kyung Park & Yong Chul Bae

  2. Department of Anatomy and Neuroscience, College of Medicine, Eulji University, 77 Gyeryong-ro 771 beon-gil, Jung-Gu, Daejeon, 34824, South Korea

    Hong Il Yoo

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  1. Sang Kyoo Paik
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Paik, S.K., Yoo, H.I., Choi, S.K. et al. Distribution of excitatory and inhibitory axon terminals on the rat hypoglossal motoneurons. Brain Struct Funct 224, 1767–1779 (2019). https://doi.org/10.1007/s00429-019-01874-0

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