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Brain Structure and Function

, Volume 222, Issue 6, pp 2655–2669 | Cite as

Orofacial proprioceptive thalamus of the rat

  • Atsushi YoshidaEmail author
  • Takashi Fujio
  • Fumihiko Sato
  • Md Sams Sazzad Ali
  • Tahsinul Haque
  • Haruka Ohara
  • Masayuki Moritani
  • Takafumi Kato
  • Jonathan O. Dostrovsky
  • Yoshihisa Tachibana
Original Article

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.

Keywords

Orofacial deep sensation VPM Trigeminal Supratrigeminal nucleus Thalamotomy DBS 

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

Notes

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.)

Compliance with ethical standards

Conflict of interest

The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Atsushi Yoshida
    • 1
    Email author
  • Takashi Fujio
    • 1
  • Fumihiko Sato
    • 1
  • Md Sams Sazzad Ali
    • 1
  • Tahsinul Haque
    • 1
    • 4
  • Haruka Ohara
    • 1
  • Masayuki Moritani
    • 2
  • Takafumi Kato
    • 1
  • Jonathan O. Dostrovsky
    • 3
  • Yoshihisa Tachibana
    • 1
  1. 1.Department of Oral Anatomy and Neurobiology, Graduate School of DentistryOsaka UniversitySuitaJapan
  2. 2.Department of Physical Therapy, Faculty of Health ScienceMorinomiya University of Medical SciencesOsakaJapan
  3. 3.Department of Physiology and Faculty of DentistryUniversity of TorontoTorontoCanada
  4. 4.Department of Oral Medicine and Diagnostic Sciences, College of DentistryKing Saud UniversityRiyadhSaudi Arabia

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