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Orofacial proprioceptive thalamus of the rat

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Abstract

The ascending pathway mediating proprioception from the orofacial region is still not fully known. The present study elucidated the relay of jaw-closing muscle spindle (JCMS) inputs from brainstem to thalamus in rats. We injected an anterograde tracer into the electrophysiologically identified supratrigeminal nucleus (Su5), known to receive JCMS input. Many thalamic axon terminals were labeled and were found mainly contralaterally in a small, unpredicted area of the caudo-ventromedial edge (VPMcvm) of ventral posteromedial thalamic nucleus (VPM). Electrical stimulation of the masseter nerve and passive jaw movements induced large responses in the VPMcvm. The VPMcvm is far from the rostrodorsal part of ventral posterolateral thalamic nucleus (VPL) where proprioceptive inputs from the body are represented. After injection of a retrograde tracer into the electrophysiologically identified VPMcvm, many neurons were labeled almost exclusively in the contralateral Su5, whereas no labeled neurons were found in the principal sensory trigeminal nucleus (Pr5) and spinal trigeminal nucleus (Sp5). In contrast, after injection of a retrograde tracer into the core of VPM, many neurons were labeled contralaterally in the Pr5 and Sp5, but none in the Su5. We conclude that JCMS input excites trigeminothalamic projection neurons in the Su5 which project primarily to the VPMcvm in marked contrast to other proprioceptors and sensory receptors in the orofacial region which project to the core VPM. These findings suggest that lesions or deep brain stimulation in the human equivalent of VPMcvm may be useful for treatment of movement disorders (e.g., orofacial tremor) without affecting other sensations.

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Abbreviations

3V:

Third ventricle

7n:

Facial nerve

10:

Dorsal motor nucleus of vagus

12:

Hypoglossal nucleus

ABC:

Avidin-biotin-peroxidase complex

APT:

Anterior pretectal nucleus

AVM:

Area ventral to the Mo5 and medial to the Pr5

BDA:

Biotinylated dextranamine

CL:

Centrolateral thalamic nucleus

CM:

Central medial thalamic nucleus

contra:

Contralateral

Cu:

Cuneate nucleus

DAB:

Diaminobenzidine

DBS:

Deep brain stimulation

FG:

Fluorogold

fr:

Fasciculus retroflexus

Gr:

Gracile nucleus

HRP:

Horseradish peroxidase

I5:

Intertrigeminal region

IMD:

Intermediodorsal thalamic nucleus

ipsi:

Ipsilateral

JCMS:

Jaw-closing muscle spindle

KF:

Kölliker–Fuse nucleus

LHb:

Lateral habenular nucleus

LPB:

Lateral parabrachial nucleus

m5:

Trigeminal motor nerve

Me5:

Mesencephalic trigeminal nucleus

me5:

Mesencephalic trigeminal tract

MD:

Mediodorsal thalamic nucleus

MHb:

Medial habenular nucleus

ml:

Medial lemniscus

Mo5:

Trigeminal motor nucleus

MPB:

Medial parabrachial nucleus

PB:

Parabrachial nucleus

PC:

Paracentral thalamic nucleus

PF:

Parafascicular thalamic nucleus

PhB:

Phosphate buffer

PhBS:

Phosphate buffered saline

Po:

Posterior thalamic nucleus

Pr5:

Principal sensory trigeminal nucleus

PV:

Paraventricular thalamic nucleus

scp:

Superior cerebellar peduncle

SO:

Superior olive

Sol:

Nucleus of the solitary tract

Sp5:

Spinal trigeminal nucleus

sp5:

Spinal trigeminal tract

Sp5C:

Sp5, caudal part

Sp5I:

Sp5, interpolar part

Sp5O:

Sp5, oral part

Su5:

Supratrigeminal nucleus

TMB:

Tetramethyl benzidine

Vim:

Ventral intermediate thalamic nucleus

VM:

Ventromedial thalamic nucleus

VPL:

Ventral posterolateral thalamic nucleus

VPLo:

Oral part of the VPL

VPM:

Ventral posteromedial thalamic nucleus

VPMcvm:

Caudo-ventromedial edge of the VPM

VPPC:

Parvicellular part of ventral posterior thalamic nucleus

WGA-HRP:

Wheat-germ agglutinin conjugated horseradish peroxidase

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Acknowledgements

We are indebted to Dr. Akiko Tomita, Dr. Yume Uemura, Ms. Etsuko Ikenoue and Ms. Yumi Tsutsumi for their technical help. This work was supported by Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant 26293391 and 16K15775 to A.Y. and Grant 15H06387 to O.H.)

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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, Graduate School of Dentistry, Osaka University, 1-8 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Atsushi Yoshida, Takashi Fujio, Fumihiko Sato, Md Sams Sazzad Ali, Tahsinul Haque, Haruka Ohara, Takafumi Kato & Yoshihisa Tachibana

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

    Masayuki Moritani

  3. Department of Physiology and Faculty of Dentistry, University of Toronto, Toronto, ON, M5S 1A8, Canada

    Jonathan O. Dostrovsky

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  1. Atsushi Yoshida
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  2. Takashi Fujio
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  3. Fumihiko Sato
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Correspondence to Atsushi Yoshida.

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Yoshida, A., Fujio, T., Sato, F. et al. Orofacial proprioceptive thalamus of the rat. Brain Struct Funct 222, 2655–2669 (2017). https://doi.org/10.1007/s00429-016-1363-1

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