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Vesicular glutamate transporter 1 (VGLUT1)- and VGLUT2-immunopositive axon terminals on the rat jaw-closing and jaw-opening motoneurons

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Abstract

To provide information on the glutamatergic synapses on the trigeminal motoneurons, which may be important for understanding the mechanism of control of jaw movements, we investigated the distribution of vesicular glutamate transporter (VGLUT)1-immunopositive (+) and VGLUT2 + axon terminals (boutons) on the rat jaw-closing (JC) and jaw-opening (JO) motoneurons, and their morphological determinants of synaptic strength by retrograde tracing, electron microscopic immunohistochemistry, and quantitative ultrastructural analysis. We found that (1) the large majority of VGLUT + boutons on JC and JO motoneurons were VGLUT2+, (2) the density of VGLUT1 + boutons terminating on JC motoneurons was significantly higher than that on JO motoneurons, (3) the density of VGLUT1 + boutons terminating on non-primary dendrites of JC motoneurons was significantly higher than that on somata or primary dendrites, whereas the density of VGLUT2 + boutons was not significantly different between JC and JO motoneurons and among various compartments of the postsynaptic neurons, and (4) the bouton volume, mitochondrial volume, and active zone area of the VGLUT1 + boutons forming synapses on JC motoneurons were significantly bigger than those of VGLUT2 + boutons. These findings suggest that JC and JO motoneurons receive glutamatergic input primarily from VGLUT2-expressing intrinsic neurons (premotoneurons), and may be controlled differently by neurons in the trigeminal mesencephalic nucleus and by glutamatergic premotoneurons.

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Notes

  1. We used the formula V (µ3) = \({\text{~}}\mathop \sum \nolimits_{{i=1}}^{n} 0.{\text{075A}}i{\text{~}}\) and Area (µ2) =\({\text{~}}\mathop \sum \nolimits_{{i=1}}^{n} 0.{\text{075}}Li{\text{~}}\): “V” is the volume of a bouton or mitochondria, “A” is the cross-sectional area of the bouton or mitochondria of the bouton measured in an individual section. “Area” is the active zone area of a bouton, “L” is length of presynaptic density of the bouton measured in an individual section. “n” is the number of sections in the series.

Abbreviations

JC:

Jaw-closing

JO:

Jaw-opening

VGLUT1:

Vesicular glutamate transporter 1

VGLUT2:

Vesicular glutamate transporter 2

Vmes:

Trigeminal mesencephalic nucleus

Vmo:

Trigeminal motor nucleus

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Acknowledgements

The authors sincerely thank Dr. Juli Valtschanoff for helpful discussion and careful reading of the manuscript.

Funding

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

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Author notes

  1. Sook Kyung Park, Sang Jin Ko and Sang Kyoo Paik are contributed equally to this work.

Authors and Affiliations

  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

    Sook Kyung Park, Sang Jin Ko, Sang Kyoo Paik & Yong Chul Bae

  2. Research Division, Korea Brain Research Institute, Daegu, 700-010, South Korea

    Jong-Cheol Rah & Kea Joo Lee

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  1. Sook Kyung Park
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Correspondence to Yong Chul Bae.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Park, S.K., Ko, S.J., Paik, S.K. et al. Vesicular glutamate transporter 1 (VGLUT1)- and VGLUT2-immunopositive axon terminals on the rat jaw-closing and jaw-opening motoneurons. Brain Struct Funct 223, 2323–2334 (2018). https://doi.org/10.1007/s00429-018-1636-y

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