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Widespread corticopetal projections from the oval paracentral nucleus of the intralaminar thalamic nuclei conveying orofacial proprioception in rats

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Abstract

The oval paracentral nucleus (OPC) was initially isolated from the paracentral nucleus (PC) within the intralaminar thalamic nuclei in rats. We have recently shown that the rat OPC receives proprioceptive inputs from jaw-closing muscle spindles (JCMSs). However, it remains unknown which cortical areas receive thalamic inputs from the OPC, and whether the cortical areas receiving the OPC inputs are distinct from those receiving inputs from the other intralaminar nuclei and sensory thalamic nuclei. To address this issue, we injected an anterograde tracer, biotinylated dextranamine (BDA), into the OPC, which was electrophysiologically identified by recording of proprioceptive inputs from the JCMSs. Many BDA-labeled axonal fibers and terminals from the OPC were ipsilaterally observed in the rostral and rostroventral regions of the primary somatosensory cortex (S1), the rostral region of the secondary somatosensory cortex (S2), and the most rostrocaudal levels of the granular insular cortex (GI). In contrast, a BDA injection into the caudal PC, which was located slightly rostral to the OPC, resulted in ipsilateral labeling of axonal fibers and terminals in the rostrolateral region of the medial agranular cortex and the rostromedial region of the lateral agranular cortex. Furthermore, injections of a retrograde tracer, Fluorogold, into these S1, S2, and GI regions, resulted in preferential labeling of neurons in the ipsilateral OPC among the intralaminar and sensory thalamic nuclei. These findings reveal that the rat OPC has widespread, but strong corticopetal projections, indicating that there exist divergent corticopetal pathways from the intralaminar thalamic nucleus, which process JCMS proprioceptive sensation.

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Abbreviations

5C:

Trigeminal sensory nucleus caudalis

5I:

Trigeminal sensory nucleus interpolaris

12:

Hypoglossal nucleus

ABC:

Avidin–biotin-peroxidase complex

ac:

Anterior commissure

Acb:

Accumbens nucleus

AcbC:

Core part of the Acb

AcbS:

Shell part of the Acb

ACg:

Anterior cingulate cortex

Agl:

Lateral agranular cortex

Agm:

Medial agranular cortex

AI:

Agranular insular cortex

BDA:

Biotinylated dextranamine

cc:

Corpus callosum

CeA:

Central amygdaloid nucleus

Cl:

Claustrum

CL:

Centrolateral thalamic nucleus

CM:

Central medial thalamic nucleus

CPu:

Caudate putamen

Cu:

Cuneate nucleus

DAB:

Diaminobenzidine

dGIrvs2:

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

DI:

Dysgranular insular cortex

DLO:

Dorsolateral orbital cortex

DP:

Dorsal peduncular cortex

ECu:

External cuneate nucleus

FG:

Fluorogold

fr:

Fasciculus retroflexus

GI:

Granular insular cortex

ic:

Internal capsule

IL:

Infralimbic cortex

IPAC:

Interstitial nucleus of the posterior limb of the anterior commissure

JCMS:

Jaw-closing muscle spindle

LGP:

Lateral globus pallidus

LO:

Lateral orbital cortex

MD:

Mediodorsal thalamic nucleus

Me5:

Trigeminal mesencephalic nucleus

ml:

Medial lemniscus

MO:

Medial orbital cortex

Mo5:

Trigeminal motor nucleus

mt:

Mammillothalamic tract

OPC:

Oval paracentral thalamic nucleus

Or:

Orbital cortex

Pb:

Parabrachial nucleus

PB:

Phosphate buffer

PBS:

Phosphate-buffered saline

PC:

Paracentral thalamic nucleus

PF:

Parafascicular thalamic nucleus

Pom:

Medial part of posterior thalamic complex

PrL:

Prelimbic cortex

RF:

Rhinal fissure

Rt:

Reticular thalamic nucleus

S1:

Primary somatosensory cortex

S2:

Secondary somatosensory cortex

sm:

Stria medullaris of the thalamus

Sm:

Submedial thalamic nucleus

Sol:

Solitary tract nucleus

Su5:

Supratrigeminal nucleus

TSNC:

Trigeminal sensory nuclear complex

Va:

Outer part of layer V

VA:

Ventral anterior thalamic nucleus

Vb:

Inner part of layer V

VL:

Ventrolateral thalamic nucleus

VM:

Ventromedial thalamic nucleus

VO:

Ventral orbital cortex

VPL:

Ventral posterolateral thalamic nucleus

VPLo:

Oral region of the VPL

VPM:

Ventral posteromedial thalamic nucleus

VPMcvm:

Caudo-ventromedial edge of the VPM

VPPC:

Parvicellular part of the ventral posterior thalamic nucleus

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Acknowledgements

We are indebted to Dr. Katsuro Uchino, Dr. Haruka Ohara, and Dr. Yume Uemura 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, 20K09888 to F.S.).

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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

  2. Yumi Tsutsumi and Yuka Mizuno equally contribute to this study.

Authors and Affiliations

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

    Yumi Tsutsumi, Yuka Mizuno, Tahsinul Haque, Fumihiko Sato, Takahiro Furuta & Atsushi Yoshida

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

    Yuka Mizuno, Ayaka Oka & Takashi Yamashiro

  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. Division of System Neuroscience, Kobe University Graduate School of Medicine, Kobe, Hyogo, 650-0017, Japan

    Yoshihisa Tachibana

Authors
  1. Yumi Tsutsumi
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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. YTs, YM, TH, and FS carried out the experiments and data analysis. TF and AO helped perform experiments and data analysis. AY, YTs, TF, MM, YCB, TY, and YTa finalized the figures and text.

Corresponding authors

Correspondence to Yoshihisa Tachibana or Atsushi Yoshida.

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Tsutsumi, Y., Mizuno, Y., Haque, T. et al. Widespread corticopetal projections from the oval paracentral nucleus of the intralaminar thalamic nuclei conveying orofacial proprioception in rats. Brain Struct Funct 226, 1115–1133 (2021). https://doi.org/10.1007/s00429-021-02228-5

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