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The Cerebellar Cortex Receives Orofacial Proprioceptive Signals from the Supratrigeminal Nucleus via the Mossy Fiber Pathway in Rats

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Abstract

Proprioceptive sensory information from muscle spindles is essential for the regulation of motor functions. However, little is known about the motor control regions in the cerebellar cortex that receive proprioceptive signals from muscle spindles distributed throughout the body, including the orofacial muscles. Therefore, in this study, we investigated the pattern of projections in the rat cerebellar cortex derived from the supratrigeminal nucleus (Su5), which conveys orofacial proprioceptive information from jaw-closing muscle spindles (JCMSs). Injections of an anterograde tracer into the Su5 revealed that many bilateral axon terminals (rosettes) were distributed in the granular layer of the cerebellar cortex (including the simple lobule B, crus II and flocculus) in a various sized, multiple patchy pattern. We could also detect JCMS proprioceptive signals in these cerebellar cortical regions, revealing for the first time that they receive muscle proprioceptive inputs in rats. Retrograde tracer injections confirmed that the Su5 directly sends outputs to the cerebellar cortical areas. Furthermore, we injected an anterograde tracer into the external cuneate nucleus (ECu), which receives proprioceptive signals from the forelimb and neck muscle spindles, to distinguish between the Su5- and ECu-derived projections in the cerebellar cortex. The labeled terminals from the ECu were distributed predominantly in the vermis of the cerebellar cortex. Almost no overlap was seen in the terminal distributions of the Su5 and ECu projections. Our findings demonstrate that the rat cerebellar cortex receives orofacial proprioceptive input that is processed differently from the proprioceptive signals from the other regions of the body.

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Data Availability

All data and materials are available upon request.

Code Availability

Not applicable.

Abbreviations

I–X:

Lobules I–X

5C:

Caudal subnucleus of the trigeminal spinal nucleus

5I:

Interpolar subnucleus of the trigeminal spinal nucleus

7n:

Facial nerve

10:

Dorsal motor nucleus of vagus

12 :

Hypoglossal nucleus

AP:

Area postrema

BDA:

Biotinylated dextran amine

BPn:

Basilar pontine nuclei

Cop:

Copula pyramidis

Crus I:

Crus I of the ansiform lobule

Crus II:

Crus II of the ansiform lobule

CTb:

Cholera toxin B subunit

Cu:

Cuneate nucleus

cu:

Cuneate fasciculus

ECu:

External cuneate nucleus

FG:

Fluorogold

FL:

Flocculus

Gr:

Gracile nucleus

H II–V:

Hemisphere of lobules II–V

I5:

Intertrigeminal region

JCMS:

Jaw-closing muscle spindle

KF:

Kölliker-Fuse nucleus

LC:

Locus coeruleus

LRt:

Lateral reticular nucleus

M1:

Primary motor cortex

Me5:

Trigeminal mesencephalic nucleus

me5:

Trigeminal mesencephalic tract

Mo5:

Trigeminal motor nucleus

Pa5:

Paratrigeminal nucleus

PB:

Phosphate buffer

Pb:

Parabrachial nucleus

PFL:

Paraflocculus

PM:

Paramedian lobule

Pr5:

Trigeminal principal nucleus

RtTg:

Reticulotegmental nucleus of the pons

scp:

Superior cerebellar peduncle

Sim A:

Simple lobule A

Sim B:

Simple lobule B

Sol:

Solitary tract nucleus

sp5:

Spinal trigeminal tract

Su5:

Supratrigeminal nucleus

Ves:

Vestibular nuclei

VPM:

Ventral posteromedial thalamic nucleus

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Funding

This work was supported by Grants-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (DC-1 21J21394 to Y.Ts.; 20K09888 to F.S.; 18KK0259 and 21K09814 to A.Y.).

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Authors and Affiliations

  1. Department of Oral Anatomy and Neurobiology, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Yumi Tsutsumi, Fumihiko Sato, Takahiro Furuta & Atsushi Yoshida

  2. Faculty of Health Care Science, Takarazuka University of Medical and Health Care, Takarazuka, Hyogo, 666-0162, Japan

    Katsuro Uchino & Atsushi Yoshida

  3. Department of Physical Therapy, Faculty of Health Science, Morinomiya University of Medical Sciences, Osaka, 559-8611, Japan

    Masayuki Moritani

  4. Department of Anatomy and Neurobiology, School of Dentistry, Kyungpook National University, Daegu, 700-412, Korea

    Yong Chul Bae

  5. Department of Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, 565-0871, Japan

    Takafumi Kato

  6. Division of Physiology and Cell Biology, Kobe University Graduate School of Medicine, Kobe, Hyogo, 650-0017, Japan

    Yoshihisa Tachibana

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  1. Yumi Tsutsumi
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  2. Fumihiko Sato
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  8. Yoshihisa Tachibana
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  9. Atsushi Yoshida
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Contributions

All authors read and approved the final manuscript. AY and YTs conceptualized the hypothesis, designed and supervised the experiments, and directed the data analysis. YTs and FS carried out the experiments and data analysis. MM and KU helped with the experiments and data analysis. AY, YTs, TF, YCB, TK and YTa finalized the figures and text.

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Correspondence to Atsushi Yoshida.

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Tsutsumi, Y., Sato, F., Furuta, T. et al. The Cerebellar Cortex Receives Orofacial Proprioceptive Signals from the Supratrigeminal Nucleus via the Mossy Fiber Pathway in Rats. Cerebellum 22, 663–679 (2023). https://doi.org/10.1007/s12311-022-01434-z

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