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. 1997 Nov;191(Pt 4):571–583. doi: 10.1046/j.1469-7580.1997.19140571.x

Encapsulated Ruffini-like endings in human lumbar facet joints

F VANDENABEELE 1,✉, J CREEMERS 1, I LAMBRICHTS 1, P LIPPENS 1, M JANS 1
PMCID: PMC1467724  PMID: 9449076

Abstract

The innervation of the human lumbar facet joint capsule was studied by light and electron microscopy. Small numbers of encapsulated corpuscular endings were identified in the dense fibrous layer. Clusters of 2 types of endings were found: small cylindrical corpuscles (type 1) and large fusiform corpuscles (type 2). The corpuscles were classified structurally as Ruffini-type endings. The 1st type was predominant and characterised by a compartmentalised receptor complex, a thin perineurial capsule and a narrow subcapsular space. The 2nd type was characterised by a thicker perineurial capsule, a ‘spindle-like’ receptive complex, and an extensive subcapsular space with capillaries and concentrically oriented fibroblast-like cells. Both types of endings were innervated mainly by thinly myelinated group III (A delta) and unmyelinated group IV (C) nerve fibres that branched and terminated in the receptor complex. Their sensory endings were intimately related to the collagen fibre bundles as multiple enlarged axonal segments (‘beads’) with ultrastructural features which were characteristic of receptive sites: an accumulation of mitochondria and vesicles, and ‘bare’ areas of axolemma lacking a Schwann cell investment but covered by a thin basal lamina. Some beads in the 2nd type of ending contained granular vesicles, 30–60 mm in diameter, resembling sympathetic nerve endings. Small diameter collagen fibrils situated within multilayered basal laminae were found among the multiple receptive sites in the receptive complex in both types of ending. Their possible functional significance in mechanoreception is discussed. Particular attention has been given to their apparent variable orientation to the mechanoreceptive site.

Keywords: Spine, mechanoreceptors

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Selected References

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  1. Abdel-Magied E. M., Taha A. A., King A. S. An ultrastructural investigation of a baroreceptor zone in the common carotid artery of the domestic fowl. J Anat. 1982 Oct;135(Pt 3):463–475. [PMC free article] [PubMed] [Google Scholar]
  2. Ahmed M., Bjurholm A., Kreicbergs A., Schultzberg M. Sensory and autonomic innervation of the facet joint in the rat lumbar spine. Spine (Phila Pa 1976) 1993 Oct 15;18(14):2121–2126. doi: 10.1097/00007632-199310001-00032. [DOI] [PubMed] [Google Scholar]
  3. Andres K. H., von Düring M., Schmidt R. F. Sensory innervation of the Achilles tendon by group III and IV afferent fibers. Anat Embryol (Berl) 1985;172(2):145–156. doi: 10.1007/BF00319597. [DOI] [PubMed] [Google Scholar]
  4. Ashton I. K., Ashton B. A., Gibson S. J., Polak J. M., Jaffray D. C., Eisenstein S. M. Morphological basis for back pain: the demonstration of nerve fibers and neuropeptides in the lumbar facet joint capsule but not in ligamentum flavum. J Orthop Res. 1992 Jan;10(1):72–78. doi: 10.1002/jor.1100100109. [DOI] [PubMed] [Google Scholar]
  5. Avramov A. I., Cavanaugh J. M., Ozaktay C. A., Getchell T. V., King A. I. The effects of controlled mechanical loading on group-II, III, and IV afferent units from the lumbar facet joint and surrounding tissue. An in vitro study. J Bone Joint Surg Am. 1992 Dec;74(10):1464–1471. [PubMed] [Google Scholar]
  6. Backenköhler U., Halata Z., Strasmann T. J. The sensory innervation of the shoulder joint of the mouse. Ann Anat. 1996 Apr;178(2):173–181. doi: 10.1016/S0940-9602(96)80040-9. [DOI] [PubMed] [Google Scholar]
  7. Beaman D. N., Graziano G. P., Glover R. A., Wojtys E. M., Chang V. Substance P innervation of lumbar spine facet joints. Spine (Phila Pa 1976) 1993 Jun 15;18(8):1044–1049. doi: 10.1097/00007632-199306150-00014. [DOI] [PubMed] [Google Scholar]
  8. Byers M. R., Dong W. K. Comparison of trigeminal receptor location and structure in the periodontal ligament of different types of teeth from the rat, cat, and monkey. J Comp Neurol. 1989 Jan 1;279(1):117–127. doi: 10.1002/cne.902790110. [DOI] [PubMed] [Google Scholar]
  9. Byers M. R. Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffini-like mechanoreceptors and free nerve endings. J Comp Neurol. 1985 Jan 22;231(4):500–518. doi: 10.1002/cne.902310408. [DOI] [PubMed] [Google Scholar]
  10. Cavanaugh J. M., el-Bohy A., Hardy W. N., Getchell T. V., Getchell M. L., King A. I. Sensory innervation of soft tissues of the lumbar spine in the rat. J Orthop Res. 1989;7(3):378–388. doi: 10.1002/jor.1100070310. [DOI] [PubMed] [Google Scholar]
  11. Chambers M. R., Andres K. H., von Duering M., Iggo A. The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q J Exp Physiol Cogn Med Sci. 1972 Oct;57(4):417–445. doi: 10.1113/expphysiol.1972.sp002177. [DOI] [PubMed] [Google Scholar]
  12. Freeman M. A., Wyke B. The innervation of the knee joint. An anatomical and histological study in the cat. J Anat. 1967 Jun;101(Pt 3):505–532. [PMC free article] [PubMed] [Google Scholar]
  13. Giles L. G., Harvey A. R. Immunohistochemical demonstration of nociceptors in the capsule and synovial folds of human zygapophyseal joints. Br J Rheumatol. 1987 Oct;26(5):362–364. doi: 10.1093/rheumatology/26.5.362. [DOI] [PubMed] [Google Scholar]
  14. Gillette R. G., Kramis R. C., Roberts W. J. Spinal projections of cat primary afferent fibers innervating lumbar facet joints and multifidus muscle. Neurosci Lett. 1993 Jul 9;157(1):67–71. doi: 10.1016/0304-3940(93)90644-z. [DOI] [PubMed] [Google Scholar]
  15. Grönblad M., Korkala O., Konttinen Y. T., Nederström A., Hukkanen M., Tolvanen E., Polak J. M. Silver impregnation and immunohistochemical study of nerves in lumbar facet joint plical tissue. Spine (Phila Pa 1976) 1991 Jan;16(1):34–38. doi: 10.1097/00007632-199101000-00006. [DOI] [PubMed] [Google Scholar]
  16. Halata Z., Badalamente M. A., Dee R., Propper M. Ultrastructure of sensory nerve endings in monkey (Macaca fascicularis) knee joint capsule. J Orthop Res. 1984;2(2):169–176. doi: 10.1002/jor.1100020208. [DOI] [PubMed] [Google Scholar]
  17. Halata Z., Haus J. The ultrastructure of sensory nerve endings in human anterior cruciate ligament. Anat Embryol (Berl) 1989;179(5):415–421. doi: 10.1007/BF00319583. [DOI] [PubMed] [Google Scholar]
  18. Halata Z., Munger B. L. Identification of the Ruffini corpuscle in human hairy skin. Cell Tissue Res. 1981;219(2):437–440. doi: 10.1007/BF00210162. [DOI] [PubMed] [Google Scholar]
  19. Halata Z., Munger B. L. The neuroanatomical basis for the protopathic sensibility of the human glans penis. Brain Res. 1986 Apr 23;371(2):205–230. doi: 10.1016/0006-8993(86)90357-4. [DOI] [PubMed] [Google Scholar]
  20. Halata Z., Munger B. L. The ultrastructure of Ruffini and Herbst corpuscles in the articular capsule of domestic pigeon. Anat Rec. 1980 Dec;198(4):681–692. doi: 10.1002/ar.1091980412. [DOI] [PubMed] [Google Scholar]
  21. Halata Z., Rettig T., Schulze W. The ultrastructure of sensory nerve endings in the human knee joint capsule. Anat Embryol (Berl) 1985;172(3):265–275. doi: 10.1007/BF00318974. [DOI] [PubMed] [Google Scholar]
  22. Halata Z. The ultrastructure of the sensory nerve endings in the articular capsule of the knee joint of the domestic cat (Ruffini corpuscles and Pacinian corpuscles). J Anat. 1977 Dec;124(Pt 3):717–729. [PMC free article] [PubMed] [Google Scholar]
  23. Haus J., Halata Z. Innervation of the anterior cruciate ligament. Int Orthop. 1990;14(3):293–296. doi: 10.1007/BF00178762. [DOI] [PubMed] [Google Scholar]
  24. Heppelmann B., Messlinger K., Neiss W. F., Schmidt R. F. 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. 1990 Feb 1;292(1):103–116. doi: 10.1002/cne.902920107. [DOI] [PubMed] [Google Scholar]
  25. Ide C. Nerve regeneration and Schwann cell basal lamina: observations of the long-term regeneration. Arch Histol Jpn. 1983 Apr;46(2):243–257. doi: 10.1679/aohc.46.243. [DOI] [PubMed] [Google Scholar]
  26. Johansson H., Sjölander P., Sojka P. Receptors in the knee joint ligaments and their role in the biomechanics of the joint. Crit Rev Biomed Eng. 1991;18(5):341–368. [PubMed] [Google Scholar]
  27. Kannari K., Sato O., Maeda T., Iwanaga T., Fujita T. A possible mechanism of mechanoreception in Ruffini endings in the periodontal ligament of hamster incisors. J Comp Neurol. 1991 Nov 8;313(2):368–376. doi: 10.1002/cne.903130211. [DOI] [PubMed] [Google Scholar]
  28. Kannari K. Sensory receptors in the periodontal ligament of hamster incisors with special reference to the distribution, ultrastructure and three-dimensional reconstruction of Ruffini endings. Arch Histol Cytol. 1990 Dec;53(5):559–573. doi: 10.1679/aohc.53.559. [DOI] [PubMed] [Google Scholar]
  29. Maeda T., Sato O., Kannari K., Takagi H., Iwanaga T. Immunohistochemical localization of laminin in the periodontal Ruffini endings of rat incisors: a possible function of terminal Schwann cells. Arch Histol Cytol. 1991 Jul;54(3):339–348. doi: 10.1679/aohc.54.339. [DOI] [PubMed] [Google Scholar]
  30. Maeda T., Sato O., Kobayashi S., Iwanaga T., Fujita T. The ultrastructure of Ruffini endings in the periodontal ligament of rat incisors with special reference to the terminal Schwann cells (K-cells). Anat Rec. 1989 Jan;223(1):95–103. doi: 10.1002/ar.1092230114. [DOI] [PubMed] [Google Scholar]
  31. McLain R. F. Mechanoreceptor endings in human cervical facet joints. Spine (Phila Pa 1976) 1994 Mar 1;19(5):495–501. doi: 10.1097/00007632-199403000-00001. [DOI] [PubMed] [Google Scholar]
  32. Mehta M., Parry C. B. Mechanical back pain and the facet joint syndrome. Disabil Rehabil. 1994 Jan-Mar;16(1):2–12. doi: 10.3109/09638289409166430. [DOI] [PubMed] [Google Scholar]
  33. Nitatori T. The fine structure of human Golgi tendon organs as studied by three-dimensional reconstruction. J Neurocytol. 1988 Feb;17(1):27–41. doi: 10.1007/BF01735375. [DOI] [PubMed] [Google Scholar]
  34. Ovalle W. K., Dow P. R. Comparative ultrastructure of the inner capsule of the muscle spindle and the tendon organ. Am J Anat. 1983 Mar;166(3):343–357. doi: 10.1002/aja.1001660308. [DOI] [PubMed] [Google Scholar]
  35. Pickar J. G., McLain R. F. Responses of mechanosensitive afferents to manipulation of the lumbar facet in the cat. Spine (Phila Pa 1976) 1995 Nov 15;20(22):2379–2385. doi: 10.1097/00007632-199511001-00002. [DOI] [PubMed] [Google Scholar]
  36. Sandoz P. A., Zenker W. Unmyelinated axons in a muscle nerve. Electron microscopic morphometry of the sternomastoid nerve in normal and sympathectomized rats. Anat Embryol (Berl) 1986;174(2):207–213. doi: 10.1007/BF00824336. [DOI] [PubMed] [Google Scholar]
  37. Sasamura T. Degeneration and regeneration of Ruffini corpuscles in the joint capsule. Nihon Seikeigeka Gakkai Zasshi. 1986 Nov;60(11):1157–1166. [PubMed] [Google Scholar]
  38. Sato A., Swenson R. S. Sympathetic nervous system response to mechanical stress of the spinal column in rats. J Manipulative Physiol Ther. 1984 Sep;7(3):141–147. [PubMed] [Google Scholar]
  39. Schenk I., Spaethe A., Halata Z. The structure of sensory nerve endings in the knee joint capsule of the dog. Ann Anat. 1996 Dec;178(6):515–521. doi: 10.1016/S0940-9602(96)80108-7. [DOI] [PubMed] [Google Scholar]
  40. Schoultz T. W., Swett J. E. The fine structure of the Golgi tendon organ. J Neurocytol. 1972 Jul;1(1):1–26. doi: 10.1007/BF01098642. [DOI] [PubMed] [Google Scholar]
  41. Schoultz T. W., Swett J. E. Ultrastructural organization of the sensory fibers innervating the Golgi tendon organ. Anat Rec. 1974 Jun;179(2):147–162. doi: 10.1002/ar.1091790202. [DOI] [PubMed] [Google Scholar]
  42. Shin H. S., Hulbert W. C., Biggs D. F. Observations on the fine structure of the baroreceptors and adrenergic innervation of the guinea-pig carotid sinus. J Morphol. 1987 Oct;194(1):65–74. doi: 10.1002/jmor.1051940106. [DOI] [PubMed] [Google Scholar]
  43. Sklenská A. Contribution to the ultrastructure of ghe golgi tendon organ. Folia Morphol (Praha) 1972;20(2):195–197. [PubMed] [Google Scholar]
  44. Strasmann T., Halata Z., Loo S. K. Topography and ultrastructure of sensory nerve endings in the joint capsules of the Kowari (Dasyuroides byrnei), an Australian marsupial. Anat Embryol (Berl) 1987;176(1):1–12. doi: 10.1007/BF00309746. [DOI] [PubMed] [Google Scholar]
  45. Vandenabeele F., Creemers J., Lambrichts I., Robberechts W. Fine structure of vesiculated nerve profiles in the human lumbar facet joint. J Anat. 1995 Dec;187(Pt 3):681–692. [PMC free article] [PubMed] [Google Scholar]
  46. Yamashita T., Cavanaugh J. M., el-Bohy A. A., Getchell T. V., King A. I. Mechanosensitive afferent units in the lumbar facet joint. J Bone Joint Surg Am. 1990 Jul;72(6):865–870. [PubMed] [Google Scholar]
  47. Yamashita T., Minaki Y., Ozaktay A. C., Cavanaugh J. M., King A. I. A morphological study of the fibrous capsule of the human lumbar facet joint. Spine (Phila Pa 1976) 1996 Mar 1;21(5):538–543. doi: 10.1097/00007632-199603010-00002. [DOI] [PubMed] [Google Scholar]
  48. Zimny M. L. Mechanoreceptors in articular tissues. Am J Anat. 1988 May;182(1):16–32. doi: 10.1002/aja.1001820103. [DOI] [PubMed] [Google Scholar]
  49. el-Bohy A., Cavanaugh J. M., Getchell M. L., Bulas T., Getchell T. V., King A. I. Localization of substance P and neurofilament immunoreactive fibers in the lumbar facet joint capsule and supraspinous ligament of the rabbit. Brain Res. 1988 Sep 20;460(2):379–382. doi: 10.1016/0006-8993(88)90386-1. [DOI] [PubMed] [Google Scholar]

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