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Proprioceptive thalamus receiving forelimb and neck muscle spindle inputs via the external cuneate nucleus in the rat

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Abstract

Proprioceptive signals from body muscles have historically been considered to project to the rostrodorsal shell of the ventrobasal thalamic complex [the ventral posterolateral nucleus (VPL) and ventral posteromedial nucleus (VPM)]. However, we have recently found that proprioception from rat jaw-closing muscle spindles (JCMSs) is conveyed via the supratrigeminal nucleus to the caudo-ventromedial edge of the VPM, but not to the rostrodorsal shell of the VPM. Therefore, proprioception from other body muscles may also project to thalamic regions other than the rostrodorsal shell of the VPL. We thus examined the thalamic projection from the rat external cuneate nucleus (ECu), which receives proprioceptive inputs from forelimb and neck muscles. After injection of anterograde tracer into the ECu, axon terminals were contralaterally labeled in the ventromedial part (VPLvm) of the VPL, but not in the rostrodorsal shell of the VPL. After anterograde tracer injection into the cuneate nucleus (Cu), axon terminals were widely labeled in the contralateral VPL including the VPLvm. In the VPLvm, we electrophysiologically confirmed the proprioceptive inputs responsive to electrical stimulation of the ECu or median nerve and to the pressure of forelimb/neck muscles or wrist flexion. After retrograde tracer injection into the VPLvm, neurons were contralaterally labeled in the ECu and Cu. After retrograde tracer injection into the VPL where no such proprioceptive inputs were recorded, no ECu neurons were labeled. These findings indicate that proprioception from forelimb/neck muscle spindles and JCMSs is somatotopically transmitted to the ventromedial floor of the ventrobasal thalamic complex, but not to its rostrodorsal shell.

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Abbreviations

5C:

Trigeminal caudal subnucleus

5I:

Trigeminal interpolar subnucleus

5O:

Trigeminal oral subnucleus

10:

Dorsal motor nucleus of vagus

12:

Hypoglossal nucleus

ABC:

Avidin–biotin-peroxidase complex

Amb:

Ambiguus nucleus

BDA:

Biotinylated dextranamine

CL:

Centrolateral thalamic nucleus

CM:

Central medial thalamic nucleus

CTb:

Cholera toxin B subunit

Cu:

Cuneate nucleus

cu:

Cuneate fasciculus

DAB:

Diaminobenzidine

ECu:

External cuneate nucleus

FG:

Fluorogold

fr:

Fasciculus retroflexus

Gr:

Gracile nucleus

HRP:

Horseradish peroxidase

i.p.:

Intraperitoneal administration

JCMS:

Jaw-closing muscle spindle

MD:

Mediodorsal thalamic nucleus

Me5:

Trigeminal mesencephalic nucleus

ml:

Medial lemniscus

Mo5:

Trigeminal motor nucleus

mt:

Mammillothalamic tract

OPC:

Oval paracentral thalamic nucleus

PB:

Phosphate buffer

PBS:

Phosphate-buffered saline

PC:

Paracentral thalamic nucleus

Pf:

Parafascicular thalamic nucleus

Po:

Posterior thalamic nucleus

Pr5:

Trigeminal principal nucleus

Rt:

Reticular thalamic nucleus

Sm:

Submedial thalamic nucleus

Sol:

Nucleus of the solitary tract

sp5:

Spinal trigeminal tract

Su5:

Supratrigeminal nucleus

Ve:

Vestibular nucleus

VL:

Ventrolateral thalamic nucleus

VM:

Ventromedial thalamic nucleus

VPL:

Ventral posterolateral thalamic nucleus

VPLvm:

Ventromedial part of the VPL

VPM:

Ventral posteromedial thalamic nucleus

VPMcvm:

Caudo-ventromedial edge of the VPM

VPPC:

Parvicellular part of the ventral posterior thalamic nucleus

X:

Nucleus X

Z:

Nucleus Z

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Acknowledgements

We are indebted to Dr. Etsuko Ikenoue and Dr. Katsuro Uchino for their technical help. This work was supported by Grants-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (18K19641, 18KK0259 to A. Y. and 17K11608 to F. S.) and the Osaka Medical Research Foundation for Intractable Diseases to H. O.

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Author notes

  1. Tahsinul Haque

    Present address: Department of Oral Medicine and Diagnostic Sciences, College of Dentistry, King Saud University, Riyadh, 11545, Saudi Arabia

Authors and Affiliations

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

    Yume Uemura, Tahsinul Haque, Fumihiko Sato, Yumi Tsutsumi, Takahiro Furuta, Yoshihisa Tachibana & Atsushi Yoshida

  2. Department of Orthodontics and Dentofacial Orthopedics, Graduate School of Dentistry, Osaka University, Suita, Osaka, 565-0871, Japan

    Yume Uemura, Haruka Ohara, Ayaka Oka & Takashi Yamashiro

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

    Yong Chul Bae

  4. Division of System Neuroscience, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki, Chuo, Kobe, Hyogo, 650-0017, Japan

    Yoshihisa Tachibana

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  1. Yume Uemura
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Contributions

All authors read and approved the final manuscript. AY and YTa conceptualized the hypothesis, designed and supervised the experiments and directed the data analysis. YU, TH and FS carried out the experiments and data analysis. YTs, HO, AO, and TF helped perform experiments and data analysis. AY, YU, YCB, TY, and YTa finalized the figures and text.

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Correspondence to Yoshihisa Tachibana or Atsushi Yoshida.

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Uemura, Y., Haque, T., Sato, F. et al. Proprioceptive thalamus receiving forelimb and neck muscle spindle inputs via the external cuneate nucleus in the rat. Brain Struct Funct 225, 2177–2192 (2020). https://doi.org/10.1007/s00429-020-02118-2

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