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Efferent and afferent connections of supratrigeminal neurons conveying orofacial muscle proprioception in rats

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Abstract

The supratrigeminal nucleus (Su5) is a key structure for controlling jaw movements; it receives proprioceptive sensation from jaw-closing muscle spindles (JCMSs) and sends projections to the trigeminal motor nucleus (Mo5). However, the central projections and regulation of JCMS proprioceptive sensation are not yet fully understood. Therefore, we aimed to reveal the efferent and afferent connections of the Su5 using neuronal tract tracings. Anterograde tracer injections into the Su5 revealed that the Su5 sends contralateral projections (or bilateral projections with a contralateral predominance) to the Su5, basilar pontine nuclei, pontine reticular nucleus, deep mesencephalic nucleus, superior colliculus, caudo-ventromedial edge of the ventral posteromedial thalamic nucleus, parafascicular thalamic nucleus, zona incerta, and lateral hypothalamus, and ipsilateral projections (or bilateral projections with an ipsilateral predominance) to the intertrigeminal region, trigeminal oral subnucleus, dorsal medullary reticular formation, and hypoglossal nucleus as well as the Mo5. Retrograde tracer injections into the Su5 demonstrated that the Su5 receives bilateral projections with a contralateral predominance (or contralateral projections) from the primary and secondary somatosensory cortices, granular insular cortex, and Su5, and ipsilateral projections (or bilateral projections with an ipsilateral predominance) from the dorsal peduncular cortex, bed nuclei of stria terminalis, central amygdaloid nucleus, lateral hypothalamus, parasubthalamic nucleus, trigeminal mesencephalic nucleus, parabrachial nucleus, juxtatrigeminal region, trigeminal oral and caudal subnuclei, and dorsal medullary reticular formation. These findings suggest that the Su5, which receives JCMS proprioception, has efferent and afferent connections with multiple brain regions that are involved in emotional and autonomic functions as well as orofacial motor functions.

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Abbreviations

3:

Oculomotor nucleus

5C:

Caudal subnucleus of the trigeminal spinal nucleus

5I:

Interpolar subnucleus of the trigeminal spinal nucleus

5O:

Oral subnucleus of the trigeminal spinal nucleus

5Or:

Rostro-dorsomedial part of the 5O

7n:

Facial nerve

10:

Dorsal motor nucleus of the vagus

ac:

Anterior commissure

Acb:

Accumbens nucleus

ACg:

Anterior cingulate cortex

AD:

Anterodorsal thalamic nucleus

Agl:

Lateral agranular cortex

Agm:

Medial agranular cortex

AI:

Agranular insular cortex

Amb:

Ambiguus nucleus

AmBl:

Basolateral amygdaloid nucleus

AmC:

Central amygdaloid nucleus

AmL:

Lateral amygdaloid nucleus

AP:

Area postrema

Aq:

Aqueduct

Au:

Auditory cortex

AV:

Anteroventral thalamic nucleus

BDA:

Biotinylated dextranamine

BPn:

Basilar pontine nuclei

BST:

Bed nucleus of stria terminalis

BSTl:

Lateral division of the BST

BSTm:

Medial division of the BST

CC:

Central canal

cc:

Corpus callosum

CL:

Centrolateral thalamic nucleus

Cl:

Claustrum

CM:

Central medial thalamic nucleus

CPu:

Caudate putamen

CTb:

Cholera toxin B subunit

Cu:

Cuneate nucleus

cu:

Cuneate fasciculus

dGIrvs2:

Dorsal part of the GI rostroventrally adjacent to the rostralmost part of the S2

DI:

Dysgranular insular cortex

dmRf:

Dorsal medullary reticular formation

DP:

Dorsal peduncular cortex

DpMe:

Deep mesencephalic nucleus

DR:

Dorsal raphe nucleus

DTg:

Dorsal tegmental nucleus

Ect:

Ectorhinal cortex

ECu:

External cuneate nucleus

f:

Fornix

fr:

Fasciculus retroflexus

GI:

Granular insular cortex

Gr:

Gracile nucleus

I5:

Intertrigeminal region

IC:

Inferior colliculus

ic:

Internal capsule

IL:

Infralimbic cortex

IO:

Inferior olive

IPAC:

Interstitial nucleus of the posterior limb of the anterior commissure

J5:

Juxtatrigeminal region

JCm:

Jaw-closing motor nucleus

JCMS:

Jaw-closing muscle spindle

JOm:

Jaw-opening motor nucleus

KF:

Kölliker-Fuse nucleus

LEnt:

Lateral entorhinal cortex

lf:

Longitudinal fasciculus

LGP:

Lateral globus pallidus

LH:

Lateral hypothalamus

LO:

Lateral orbital cortex

MD:

Mediodorsal thalamic nucleus

Me5:

Trigeminal mesencephalic nucleus

MGP:

Medial globus pallidus

ml:

Medial lemniscus

MO:

Medial orbital cortex

Mo5:

Trigeminal motor nucleus

OPC:

Oval paracentral thalamic nucleus

ox:

Optic chiasm

PA:

Parietal association cortex

Pa5:

Paratrigeminal nucleus

PAG:

Periaqueductal gray

PB:

Phosphate buffer

Pb:

Parabrachial nucleus

PBS:

Phosphate-buffered saline

PC:

Paracentral thalamic nucleus

Pf:

Parafascicular thalamic nucleus

PnR:

Pontine reticular nucleus

Po:

Posterior thalamic nucleus

Pr:

Prepositus nucleus

Pr5:

Trigeminal principal nucleus

PRh:

Perirhinal cortex

PrL:

Prelimbic cortex

Psth:

Parasubthalamic nucleus

PvH:

Paraventricular hypothalamic nucleus

py:

Pyramidal tract

pyx:

Pyramidal decussation

R:

Red nucleus

Rfvm:

Reticular formation ventral to the Mo5

RRF:

Retrorubral field

Rt:

Reticular thalamic nucleus

RtTg:

Reticulotegmental nucleus

S1:

Primary somatosensory cortex

S2:

Secondary somatosensory cortex

SC:

Superior colliculus

scp:

Superior cerebellar peduncle

Sm:

Submedial thalamic nucleus

SNc:

Substantia nigra pars compacta

SNr:

Substantia nigra pars reticulata

Sol:

Solitary tract nucleus

sp5:

Spinal trigeminal tract

st:

Stria terminalis

Sth:

Subthalamic nucleus

Su5:

Supratrigeminal nucleus

TA:

Temporal association cortex

tth:

Trigeminothalamic tract

VA:

Ventral anterior thalamic nucleus

Ve:

Vestibular nucleus

VII:

Facial nucleus

VL:

Ventrolateral thalamic nucleus

VM:

Ventromedial thalamic nucleus

VO:

Ventral orbital cortex

VPL:

Ventral posterolateral thalamic nucleus

VPM:

Ventral posteromedial thalamic nucleus

VPMcvm:

Caudo-ventromedial edge of the VPM

VPPC:

Parvicellular part of the ventral posterior thalamic nucleus

XII:

Hypoglossal nucleus

ZI:

Zona incerta

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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 (18K19641 and 18KK0259 to A.Y., and 17K11608 and 20K09888 to F.S.).

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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

    Atsushi Yoshida, Misaki Inoue, Fumihiko Sato, Yayoi Morita, Yumi Tsutsumi, Takahiro Furuta & Katsuro Uchino

  2. Department of Acupuncture, Takarazuka University of Medical and Health Care, Takarazuka, Hyogo, 666-0162, Japan

    Katsuro Uchino

  3. College of Dentistry, Dar Al Uloom University, Riyadh, 11512, Saudi Arabia

    Fatema Akhter

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

    Yong Chul Bae

  5. Department of Physiology and Cell Biology, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki, Chuo, Kobe, Hyogo, 650-0017, Japan

    Yoshihisa Tachibana

  6. Department of Oral Physiology, Showa University School of Dentistry, Shinagawa-ku, Tokyo, 142-8555, Japan

    Tomio Inoue

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  1. Atsushi Yoshida
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  2. Misaki Inoue
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  10. Yoshihisa Tachibana
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  11. Tomio Inoue
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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. MI, FS, YM and YTs, carried out the experiments and data analysis. TF and KU helped with the experiments and data analysis. AY, MI, FA, YCB, YTa and TI finalized the figures and text.

Corresponding authors

Correspondence to Atsushi Yoshida or Yoshihisa Tachibana.

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Detailed protocols for the care and use of laboratory animals were approved by the animal ethics committees of the Osaka University Graduate School of Dentistry.

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Yoshida, A., Inoue, M., Sato, F. et al. Efferent and afferent connections of supratrigeminal neurons conveying orofacial muscle proprioception in rats. Brain Struct Funct 227, 111–129 (2022). https://doi.org/10.1007/s00429-021-02391-9

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