Advanced Search

Journal Navigation

Journal Home

Subscriptions

Archive

Contact Us

Table of Contents

Click here to sign up for SAGE Journal Email Alerts today!

Sign In to gain access to subscriptions and/or personal tools.
Journal of Dental Research
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Kido, M.A.
Right arrow Articles by Tanaka, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kido, M.A.
Right arrow Articles by Tanaka, T.
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

A Topographical and Ultrastructural Study of Sensory Trigeminal Nerve Endings in the Rat Temporomandibular Joint as Demonstrated by Anterograde Transport of Wheat Germ Agglutinin-Horseradish Peroxidase (WGA-HRP)

M.A. Kido

Department of Oral Anatomy I, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

T. Kiyoshima

Department of Oral Pathology, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

T. Ibuki

Department of Prosthetic Dentistry I, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

S. Shimizu

Department of Oral and Maxillofacial Surgery II, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

T. Kondo

Department of Oral Anatomy I, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

Y. Terada

Department of Prosthetic Dentistry I, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

T. Tanaka

Department of Oral Anatomy I, Faculty of Dentistry, Kyushu University 61, Fukuoka 812-82, Japan

To extend our previous light microscopic observations concerning the distribution of trigeminal sensory nerves in the synovium of the rat temporomandibular joint, we investigated the detailed distribution and fine structure of sensory nerve endings at the light and electron microscopic level by the anterograde transport method using wheat germ agglutinin-horseradish peroxidase (WGA-HRP) injected into the trigeminal ganglion. At the light microscopic level, HRP-labeled nerve fibers were observed in the joint capsule and peripheral portion of the disc. The anterior portion of the disc was more densely innervated than the posterior portion, while no nerves were found in the central portion. At the electron microscopic level, HRP reaction products were observed intra-axonally in the thinly myelinated (AS) and unmyelinated (C) axons in the anterior portion of the joint capsule, and were also localized in the extracellular space surrounding the unmyelinated fibers and terminals. In the subsynovial layer of the synovial membrane, the majority of labeled axons located near blood vessels or among the collagenous fibrils were covered by Schwann cell sheaths, although some naked axon terminals without sheaths were also found. These unsheathed terminals contained mitochondria, small clear vesicles, and large granular vesicles, and were close to the synovial A and/or B cells near the joint cavity. The minimum distance between the terminals and synovial cells was 75 nm. This is the first demonstration of trigeminal sensory nerve terminals close to synovial lining cells or joint cavity and suggests that neuropeptides such as substance P may be released close to the synovial lining cells or joint cavity.

Key Words: sensory innervation • wheat germ agglutinin-horseradish peroxidase (WGA-HRP) • temporomandibular joint • synovial • anterograde tracing

REFERENCES

  • Adams JC (1981), Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775.[Medline] [Order article via Infotrieve]
  • Andres KH, von During M., Muszynski K., Schmidt RF (1987). Nerve fibers and their terminals of the dura mater encephali of the rat. Anat Embryol 175:289-301.[CrossRef][Medline] [Order article via Infotrieve]
  • Bar-Shavit Z., Goldman R., Stabinsky Y., Gottlieb P., Fridkin M., Teichberg VI, et al. (1980). Enhancement of phagocytosis-a newly found activity of substance P residing in its N-terminal tetrapeptide sequence. Biochem Biophys Res Commun 94:1445-1451.[CrossRef][Medline] [Order article via Infotrieve]
  • Broton JG, Hu JW, Sessle BJ (1988). Effect of temporomandibular joint stimulation on nociceptive and nonnociceptive neurons of the cat's trigeminal subnucleus caudalis (medullary dorsal horn). J Neurophysiol 59:1575-1589.[Abstract/Free Full Text]
  • Byers MR (1979). Dental sensory receptors. Int Rev Neurobiol 25:39-94.
  • Chan KY, Byers MR (1985a). Sensory nerve endings of incisive papilla of rat hard palate studied by peroxidase cytochemical methods. J Comp Neurol 234:192-200.[Medline] [Order article via Infotrieve]
  • Chan KY, Byers MR (1985b). Anterograde axonal transport and intercellular transfer of WGA-HRP in trigeminal-innervated sensory receptors of rat incisive papilla. J Comp Neurol 234:201-217.[Medline] [Order article via Infotrieve]
  • Dreessen D., Halata Z., Strasmann T. (1990). Sensory innervation of the temporomandibular joint in the mouse. Acta Anat 139:154-160.[Medline] [Order article via Infotrieve]
  • Frommer J., Monroe CW (1966). The morphology and distribution of nerve fibers and endings associated with the mandibular joint of the mouse. J Dent Res 45:1762-1766.
  • Heppelmann B., Messlinger K., Neiss WF, Schmidt RF (1990). Ultrastructural three-dimensional reconstruction of group III and group IV sensory nerve endings ("free nerve endings") in the knee joint capsule of the cat: evidence for multiple receptive sites. J Comp Neurol 292:103-116.[CrossRef][Medline] [Order article via Infotrieve]
  • Heym C., Common B., Klimaschewski L., Preissler U., Kummer W. (1993). Immunohistochemical evidence from co-localization and denervation studies for four types of substance P-containing nervous structures in the rat superior cervical ganglion. Anat Embryol 187:485-492.[Medline] [Order article via Infotrieve]
  • Hofelt T., Elfvin LG, Schultsberg M., Goldstein M., Nilsson G. (1977). On the occurrence of substance P-containing fibers in sympathetic ganglia: immunohistochemical evidence. Brain Res 132:29-41.[CrossRef][Medline] [Order article via Infotrieve]
  • Holmlund AB, Gynther GW, Reinholt FP (1992). Disk derangement and inflammatory changes in the posterior disk attachment of the temporomandibular joint. Oral Surg Oral Med Oral Pathol 73:9-12.[CrossRef][Medline] [Order article via Infotrieve]
  • Ichikawa H., Wakisaka S., Matsuo S., Akai M. ( 1989). Peptidergic innervation of the temporomandibular disk in the rat. Experientia 45:303-304.[Medline] [Order article via Infotrieve]
  • Johansson A., Isacsson G., Isberg A., Grandholm A. (1986). Distribution of substance P-like immunoreactive nerve fibers in temporomandibular joint soft tissues of monkey. Scand J Dent Res 94:225-230.[Medline] [Order article via Infotrieve]
  • Keller JH, Moffett BC Jr (1968). Nerve endings in the temporomandibular joint of the Rhesus macaque. Anat Rec 160:587-594.[Medline] [Order article via Infotrieve]
  • Kido MA, Kondo T., Ayasaka N., Terada Y., Tanaka T. (1991). The peripheral distribution of trigeminal nerve fibers in the rat temporomandibular joint studied by an anterograde axonal
  • transport method with wheat germ agglutinin-horseradish peroxidase. Arch Oral Biol 36:397-400.
  • Kido MA, Kiyoshima T., Kondo T., Ayasaka N., Moroi R., Terada Y., et al. (1993). Distribution of substance P and calcitonin gene-related peptide-like immunoreactive nerve fibers in the rat temporomandibular joint. J Dent Res 72:592-598.
  • Kruger L., Perl ER, Sedivec MJ (1981). Fine structure of myelinated mechanical nociceptor endings in cat hairy skin. J Comp Neurol 198:137-154.[CrossRef][Medline] [Order article via Infotrieve]
  • Kubo Y. ( 1987). The uptake of horseradish peroxidase in monkey temporomandibular joint synovium after occlusal alteration. J Dent Res 66:1049-1054.
  • Lee Y., Kawai Y., Shiosaka S., Takami K., Kiyama H., Hillyard CJ, et al. (1985). Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: immunohistochemical analysis. Brain Res 330:194-196.[CrossRef][Medline] [Order article via Infotrieve]
  • Lembeck F., Holzer P. (1979). Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn-Schmiedeberg's Arch Pharmacol 310:175-183.[CrossRef][Medline] [Order article via Infotrieve]
  • Levine JD, Clark R., Devor M., Helms C., Moskowitz MA, Basbaum AI (1984). Intraneuronal substance P contributes to the severity of experimental arthritis. Science 226:547-549.[Abstract/Free Full Text]
  • Marfurt CF, Turner DF (1983). Sensory nerve endings in rat orofacial region labeled by the anterograde and transganglionic transport of horseradish peroxidase: a new method for tracing peripheral nerve fibers. Brain Res 261:1-12.[Medline] [Order article via Infotrieve]
  • Mesulam MM (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106-117.[Abstract]
  • Murnane TW, Feagans WM (1970). Fine structure of synovial lining cells in the squamosal-mandibular joint of the rat. J Dent Res 49:1068-1073.
  • Robertson B., Aldskogius H. (1982). The use of anterogradely transported wheat germ agglutinin-horseradish peroxidase conjugate to visualize cutaneous sensory nerve endings. Brain Res 240:327-330.[Medline] [Order article via Infotrieve]
  • Romph JH, Capra NF, Gatipon GB (1979). Trigeminal nerve and temporomandibular joint of the cat: a horseradish peroxidase study. Exp Neurol 65:99-106.[Medline] [Order article via Infotrieve]
  • Thilander B. (1961). Innervation of the temporo-mandibular joint capsule in man. Trans R Sch Dent (Stockholm) 7(Ser 2):8-67.
  • Thilander B. (1964). Innervation of the temporomandibular disc in man. Acta Odontol Scand 22:151-156.[Medline] [Order article via Infotrieve]
  • Valtschanoff JG, Weinberg RJ, Rustioni A. (1992). Peripheral injury and anterograde transport of wheat germ agglutinin-horseradish peroxidase to the spinal cord. Neurosci 50:685-696.[CrossRef][Medline] [Order article via Infotrieve]
  • Weinberg RJ, Van Eyck SL (1991). A tetramethylbenzidine/tungstate reaction for horseradish peroxidase histochemistry. J Histochem Cytochem 39:1143-1148.[Abstract]
  • Weinberg RJ, Tracey DJ, Rustioni A. (1990). Extracellular labeling of unmyelinated dorsal terminals after WGA-HRP injections in spinal ganglia. Brain Res 523:351-355.[Medline] [Order article via Infotrieve]
  • Widenfalk B., Wiberg M. (1990). Origin of sympathetic and sensory innervation of the temporo-mandibular joint. A retrograde axonal tracing study in the rat. Neurosci Lett 109:30-35.[CrossRef][Medline] [Order article via Infotrieve]

Journal of Dental Research, Vol. 74, No. 7, 1353-1359 (1995)
DOI: 10.1177/00220345950740070601
Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?


This article has been cited by other articles:


Home page
 J. Neurophysiol.Home page
A. Tashiro, K. Okamoto, S. B. Milam, and D. A. Bereiter
Differential Effects of Estradiol on Encoding Properties of TMJ Units in Laminae I and V at the Spinomedullary Junction in Female Rats
J Neurophysiol, December 1, 2007; 98(6): 3242 - 3253.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
N. M. Flake, D. B. Bonebreak, and M. S. Gold
Estrogen and Inflammation Increase the Excitability of Rat Temporomandibular Joint Afferent Neurons
J Neurophysiol, March 1, 2005; 93(3): 1585 - 1597.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
S. Takeshita, H. Hirata, and D. A. Bereiter
Intensity Coding by TMJ-Responsive Neurons in Superficial Laminae of Caudal Medullary Dorsal Horn of the Rat
J Neurophysiol, November 1, 2001; 86(5): 2393 - 2404.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
B. E. Cairns, B. J. Sessle, and J. W. Hu
Characteristics of Glutamate-Evoked Temporomandibular Joint Afferent Activity in the Rat
J Neurophysiol, June 1, 2001; 85(6): 2446 - 2454.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
B. E. Cairns, B. J. Sessle, and J. W. Hu
Activation of Peripheral GABAA Receptors Inhibits Temporomandibular Joint-Evoked Jaw Muscle Activity
J Neurophysiol, April 1, 1999; 81(4): 1966 - 1969.
[Abstract] [Full Text] [PDF]

Home page
 JDRHome page
C.A. Casatti, L. Frigo, and J.A. Bauer
Origin of Sensory and Autonomic Innervation of the Rat Temporomandibular Joint: A Retrograde Axonal Tracing Study with the Fluorescent Dye Fast Blue
Journal of Dental Research, March 1, 1999; 78(3): 776 - 783.
[Abstract] [PDF]

Home page
 JDRHome page
T. Ibuki, M.A. Kido, T. Kiyoshima, Y. Terada, and T. Tanaka
An Ultrastructural Study of the Relationship between Sensory Trigeminal Nerves and Odontoblasts in Rat Dentin/Pulp as Demonstrated by the Anterograde Transport of Wheat Germ Agglutinin-Horseradish Peroxidase (WGA-HRP)
Journal of Dental Research, December 1, 1996; 75(12): 1963 - 1970.
[Abstract] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Kido, M.A.
Right arrow Articles by Tanaka, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kido, M.A.
Right arrow Articles by Tanaka, T.
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?