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The ultrastructure of macaque mesencephalic trigeminal nucleus neurons

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Abstract

Primary afferents originating from the mesencephalic trigeminal nucleus provide the main source of proprioceptive information guiding mastication, and thus represent an important component of this critical function. Unlike those of other primary afferents, their cell bodies lie within the central nervous system. It is believed that this unusual central location allows them to be regulated by synaptic input. In this study, we explored the ultrastructure of macaque mesencephalic trigeminal nucleus neurons to determine the presence and nature of this synaptic input in a primate. We first confirmed the location of macaque mesencephalic trigeminal neurons by retrograde labeling from the masticatory muscles. Since the labeled neurons were by far the largest cells located at the edge of the periaqueductal gray, we could undertake sampling for electron microscopy based on soma size. Ultrastructurally, mesencephalic trigeminal neurons had very large somata with euchromatic nuclei that sometimes displayed deeply indented nuclear membranes. Terminal profiles with varied vesicle characteristics and synaptic density thicknesses were found in contact with either their somatic plasma membranes or somatic spines. However, in contradistinction to other, much smaller, somata in the region, the plasma membranes of the mesencephalic trigeminal somata had only a few synaptic contacts. They did extend numerous somatic spines of various lengths into the neuropil, but most of these also lacked synaptic contact. The observed ultrastructural organization indicates that macaque trigeminal mesencephalic neurons do receive synaptic contacts, but despite their central location, they only avail themselves of very limited input.

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Data availability

The electron micrographs that formed the basis for this study are available for examination by request to the authors.

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Acknowledgements

We wish to acknowledge the help of Jayne Bernanke, Glenn Hoskins, and Jeremy Sullivan in the ultrastructural preparation of tissues. In addition, we thank Susan Warren, PhD for helpful comments on earlier drafts of this manuscript.

Funding

This work was supported by the National Institutes of Health [grant number EY014263] to PJM.

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Contributions

Experimental design, surgical procedures and figure production: PJM. Ultrastructural analysis, writing and editing: NW and PJM.

Corresponding author

Correspondence to Niping Wang.

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The authors have no conflicts of interest, financial or otherwise, with respect to the publication of this manuscript.

Ethical use of animal statement

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 standards of the institution at which the studies were conducted. Specifically, they were undertaken under protocols approved by the Institutional Animal Care and Use Committee of the University of Mississippi Medical Center (USDA Animal Welfare Assurance # D16-00174) and housed in an AAALAC accredited facility.

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The authors did not use artificial intelligence in the analysis of the data or the production of this manuscript.

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Communicated by Bill J Yates.

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221_2023_6746_MOESM1_ESM.jpg

Supplementary file1 Supplemental Fig. 1 Examples of connecting process axon and somatic contact via spinous processes. A. Mes V soma displays a long segment of a connecting process axon (Ax). Boxed area in A shown at higher magnification in B, where the spinous process (Sp) extending from a soma on the right comes into contact with the plasma membrane of the soma on the left (JPG 2778 KB)

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Wang, N., May, P.J. The ultrastructure of macaque mesencephalic trigeminal nucleus neurons. Exp Brain Res 242, 295–307 (2024). https://doi.org/10.1007/s00221-023-06746-y

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  • DOI: https://doi.org/10.1007/s00221-023-06746-y

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