Skip to main content
PMC home page
Journal of Anatomy logoLink to Journal of Anatomy
. 1979 May;128(Pt 3):523–552.

The structure and source of lingual proprioceptors in the monkey.

M J Fitzgerald, S R Sachithanandan
PMCID: PMC1232905  PMID: 157344

Abstract

The proprioceptive innervation of the tounge has been investigated in the Cynamolgus monkey by silver impregnation methods following unilateral section of lingual, hypoglossal, and cervical nerves. Muscle spindles were constantly present in the intrinsic and extrinsic muscles. They varied greatly in number, averaged half the length of lumbrical spindles, and showed an unusual arrangement of chain fibre nuclei. Other, inconstant proprioceptors included tendon endings, Ruffini endings, Pacinian corpuscles, paciniform and lamellated endings. Topologically, the endings other than spindles were extra-muscular, so that the overall pattern of proprioceptive innervation resembled that of skeletal muscle in general. Lingual nerve section was without apparent effect on the proprioceptors. Section of the hypoglossal nerve at its point of entry into the tongue caused severe depletiion of ipsilateral proprioceptors and of fusimotor nerves. In the anterior tongue there was evidence of transmedian overlap by efferent and afferent axons contained in the hypoglossal nerve. Hypoglossal section at the skull base caused degeneration of fusimotor nerves but not of proprioceptors. Section of (a), the connexion of C2-C3 ventral rami with the hypoglossal, together with section of (b), the ramus descendens hypoglossi, coused depletion of lingual proprioceptors; again there was evidence of transmedian overlap. Procedures (a) or (b) alone had a lesser effect. It was concluded that lingual proprioceptive afferent fibres occupy the distal hypoglossal nerve, leaving it in the ramus descendens and in the C2-C3 connexion to enter the spinal cord via nerves C2 and C3.

Full text

PDF
523

Images in this article

528Fig. 3
on p.528
528Fig. 4
on p.528
528Fig. 5
on p.528
528Fig. 6
on p.528
528Fig. 7
on p.528
528Fig. 8
on p.528
529Fig. 9
on p.529
529Fig. 10
on p.529
529Fig. 11
on p.529
529Fig. 12
on p.529
532Fig. 17
on p.532
532Figs. 18,20
on p.532
532Fig. 19
on p.532
533Fig. 21
on p.533
534Figs. 22-26
on p.534
535Fig. 27
on p.535
535Fig. 28
on p.535
535Fig. 29
on p.535
535Fig. 30
on p.535
536Fig. 31
on p.536
536Fig. 32
on p.536
536Fig. 33
on p.536
537Fig. 34
on p.537
539Fig. 35
on p.539
539Fig. 36
on p.539
539Fig. 37
on p.539
539Fig. 38
on p.539
539Fig. 39
on p.539

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ADAL M. N., BARKER D. INTRAMUSCULAR BRANCHING OF FUSIMOTOR FIBRES. J Physiol. 1965 Mar;177:288–299. doi: 10.1113/jphysiol.1965.sp007592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alexander R. W., Fitzgerald M. J. An example of transmedian neuromuscular innervation. J Dent Res. 1967 Jan-Feb;46(1):261–263. doi: 10.1177/00220345670460012201. [DOI] [PubMed] [Google Scholar]
  3. Banks R. W., Harker D. W., Stacey M. J. A study of mammalian intrafusal muscle fibres using a combined histochemical and ultrastructural technique. J Anat. 1977 Jul;123(Pt 3):783–796. [PMC free article] [PubMed] [Google Scholar]
  4. Banks R. W., James N. T. The fine structure of the guinea-pig muscle spindle. Z Zellforsch Mikrosk Anat. 1973;140(3):357–368. doi: 10.1007/BF00307023. [DOI] [PubMed] [Google Scholar]
  5. Bowman J. P., Combs C. M. Discharge patterns of lingual spindle afferent fibers in the hypoglossal nerve of the rhesus monkey. Exp Neurol. 1968 May;21(1):105–119. doi: 10.1016/0014-4886(68)90037-x. [DOI] [PubMed] [Google Scholar]
  6. Bowman J. P., Combs C. M. The cerebrocortical projection of hypoglossal afferents. Exp Neurol. 1969 Feb;23(2):291–301. doi: 10.1016/0014-4886(69)90063-6. [DOI] [PubMed] [Google Scholar]
  7. Bowman J. P. Muscle spindles in the intrinsic and extrinsic muscles of the rhesus monkey's (Macaca mulatta) tongue. Anat Rec. 1968 Aug;161(4):483–487. doi: 10.1002/ar.1091610410. [DOI] [PubMed] [Google Scholar]
  8. Boyd I. A., Gladden M. H., McWilliam P. N., Ward J. Control of dynamic and static nuclear bag fibres and nuclear chain fibres by gamma and beta axons in isolated cat muscle spindels. J Physiol. 1977 Feb;265(1):133–162. doi: 10.1113/jphysiol.1977.sp011709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Boyd I. A. The mechanical properties of dynamic nuclear bag fibres, static nuclear bag fibres and nuclear chain fibres in isolated cat muscle spindles. Prog Brain Res. 1976;44:33–50. [PubMed] [Google Scholar]
  10. Boyd J. D. The sensory component of the hypoglossal nerve in the rabbit. J Anat. 1941 Apr;75(Pt 3):330–345. [PMC free article] [PubMed] [Google Scholar]
  11. Burgess P. R., Clark F. J. Characteristics of knee joint receptors in the cat. J Physiol. 1969 Aug;203(2):317–335. doi: 10.1113/jphysiol.1969.sp008866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. COOPER S. Afferent impulses in the hypoglossal nerve on stretching the cat's tongue. J Physiol. 1954 Nov 29;126(2):32P–32P. [PubMed] [Google Scholar]
  13. COOPER S. Muscle spindles in the intrinsic muscles of the human tongue. J Physiol. 1953 Oct;122(1):193–202. doi: 10.1113/jphysiol.1953.sp004991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chouchkov H. N. Ultrastructure of Pacinian corpuscles after the section of nerve fibres. Z Mikrosk Anat Forsch. 1971;83(1):33–46. [PubMed] [Google Scholar]
  15. Daniel P. Spiral nerve endings in the extrinsic eye muscles of man. J Anat. 1946 Oct;80(Pt 4):189–193. [PMC free article] [PubMed] [Google Scholar]
  16. Downman C. B. Afferent fibres of the hypoglossal nerve. J Anat. 1939 Apr;73(Pt 3):387–395. [PMC free article] [PubMed] [Google Scholar]
  17. EKLUND G., SKOGLUND S. On the specificity of the Ruffini like joint receptors. Acta Physiol Scand. 1960 Jul 15;49:184–191. doi: 10.1111/j.1748-1716.1960.tb01942.x. [DOI] [PubMed] [Google Scholar]
  18. Egel R. T., Bowman J. P., Coombs C. M. Calibre spectra of the lingual and hypoglossal nerves of the rhesus monkey. J Comp Neurol. 1968 Oct;134(2):163–174. doi: 10.1002/cne.901340205. [DOI] [PubMed] [Google Scholar]
  19. FITZGERALD M. J. A GENERAL-PURPOSE SILVER TECHNIQUE FOR PERIPHERAL NERVE FIBERS IN FROZEN SECTIONS. Stain Technol. 1963 Nov;38:321–327. doi: 10.3109/10520296309061196. [DOI] [PubMed] [Google Scholar]
  20. FITZGERALD M. J., LAW M. E. The peripheral connexions between the lingual and hypoglossal nerves. J Anat. 1958 Apr;92(2):178–188. [PMC free article] [PubMed] [Google Scholar]
  21. Fitzgerald M. J., Alexander R. W. The intramscular ganglia of the cat's tongue. J Anat. 1969 Jul;105(Pt 1):27–46. [PMC free article] [PubMed] [Google Scholar]
  22. Fukuda Y., Iwama K. A relation between latencies of initial and late spike discharges of rat lateral geniculate cells to optic tract stimulation. Brain Res. 1972 Feb 25;37(2):322–325. doi: 10.1016/0006-8993(72)90678-6. [DOI] [PubMed] [Google Scholar]
  23. Gandevia S. C., McCloskey D. I. Joint sense, muscle sense, and their combination as position sense, measured at the distal interphalangeal joint of the middle finger. J Physiol. 1976 Sep;260(2):387–407. doi: 10.1113/jphysiol.1976.sp011521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Hanson J., Widén L. Afferent fibres in the hypoglossal nerve of cat. Acta Physiol Scand. 1970 May;79(1):24–36. doi: 10.1111/j.1748-1716.1970.tb04698.x. [DOI] [PubMed] [Google Scholar]
  26. Houk J., Henneman E. Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol. 1967 May;30(3):466–481. doi: 10.1152/jn.1967.30.3.466. [DOI] [PubMed] [Google Scholar]
  27. JANSEN J. K., RUDJORD T. ON THE SILENT PERIOD AND GOLGI TENDON ORGANS OF THE SOLEUS MUSCLE OF THE CAT. Acta Physiol Scand. 1964 Dec;62:364–379. doi: 10.1111/j.1748-1716.1964.tb10435.x. [DOI] [PubMed] [Google Scholar]
  28. James N. T. The histochemical demonstration of three types of intrafusal fibre in rat muscle spindles. Histochem J. 1971 Nov;3(6):457–462. doi: 10.1007/BF01014784. [DOI] [PubMed] [Google Scholar]
  29. Kawamura Y., Funakoshi M., Nishiyama T., Morimoto T. Auto-regulatory neuromechanism of the tongue muscle activity. Jpn J Physiol. 1967 Apr;17(2):123–134. doi: 10.2170/jjphysiol.17.123. [DOI] [PubMed] [Google Scholar]
  30. Krishnamurti A., Kanagasuntheram R., Vij S. Failure of reinnervation of Pacinian corpuscle after nerve crush. An electron microscopic study. Acta Neuropathol. 1973;23(4):338–341. doi: 10.1007/BF00687464. [DOI] [PubMed] [Google Scholar]
  31. Kubota K., Negishi T., Masegi T. Topological distribution of muscle spindles in the human tongue and its significance in proprioception. Bull Tokyo Med Dent Univ. 1975 Sep;22(3):235–242. [PubMed] [Google Scholar]
  32. LAW M. E. Lingual proprioception in pig, dog and cat. Nature. 1954 Dec 11;174(4441):1107–1108. doi: 10.1038/1741107b0. [DOI] [PubMed] [Google Scholar]
  33. Lewis P. R., Flumerfelt B. A., Shute C. C. The use of cholinesterase techniques to study topographical localization in the hypoglossal nucleus of the rat. J Anat. 1971 Nov;110(Pt 2):203–213. [PMC free article] [PubMed] [Google Scholar]
  34. MOUNTCASTLE V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol. 1957 Jul;20(4):408–434. doi: 10.1152/jn.1957.20.4.408. [DOI] [PubMed] [Google Scholar]
  35. MOUNTCASTLE V. B., POWELL T. P. Central nervous mechanisms subserving position sense and kinesthesis. Bull Johns Hopkins Hosp. 1959 Oct;105:173–200. [PubMed] [Google Scholar]
  36. Matthews P. B. Muscle afferents and kinaesthesia. Br Med Bull. 1977 May;33(2):137–142. doi: 10.1093/oxfordjournals.bmb.a071413. [DOI] [PubMed] [Google Scholar]
  37. McCloskey D. I. Differences between the senses of movement and position shown by the effects of loading and vibration of muscles in man. Brain Res. 1973 Oct 26;61:119–131. doi: 10.1016/0006-8993(73)90521-0. [DOI] [PubMed] [Google Scholar]
  38. Milburn A. The early development of muscle spindles in the rat. J Cell Sci. 1973 Jan;12(1):175–195. doi: 10.1242/jcs.12.1.175. [DOI] [PubMed] [Google Scholar]
  39. Morimoto T., Kawamura Y. Discharge patterns of hypoglossal afferents in a cat. Brain Res. 1971 Dec 24;35(2):539–542. doi: 10.1016/0006-8993(71)90496-3. [DOI] [PubMed] [Google Scholar]
  40. NYBERG-HANSEN R. ANATOMICAL DEMONSTRATION OF GAMMA MOTONEURONS IN THE CAT'S SPINAL CORD. Exp Neurol. 1965 Sep;13:71–81. doi: 10.1016/0014-4886(65)90006-3. [DOI] [PubMed] [Google Scholar]
  41. Nakamura Y., Goldberg L. J., Mizuno N., Clemente C. D. Masseteric reflex inhibition induced by afferent impulses in the hypoglossal nerve. Brain Res. 1970 Mar 3;18(2):241–255. doi: 10.1016/0006-8993(70)90326-4. [DOI] [PubMed] [Google Scholar]
  42. Peterson H. A., Winkelmann R. K., Coventry M. B. Nerve endings in the hip joint of the cat: their morphology, distrubution, and density. J Bone Joint Surg Am. 1972 Mar;54(2):333–343. [PubMed] [Google Scholar]
  43. RICHARDSON K. C. Studies on the structure of autonomic nerves in the small intestine, correlating the silver-impregnated image in light microscopy with the permanganate-fixed ultrastructure in electronmicrscopy. J Anat. 1960 Oct;94:457–472. [PMC free article] [PubMed] [Google Scholar]
  44. SAKLA F. B. MULTIPOLAR NERVE CELLS WITHIN THE LINGUAL GLOSSOPHARYNGEAL AND HYPOGLOSSAL NERVES IN THE ADULT HUMAN TONGUE. Indian J Med Sci. 1964 Apr;18:215–217. [PubMed] [Google Scholar]
  45. SAS J., APPELTAUER C. ATYPICAL MUSCLE SPINDLES IN THE EXTRINSIC EYE MUSCLES OF MAN. Acta Anat (Basel) 1963;55:311–322. doi: 10.1159/000142481. [DOI] [PubMed] [Google Scholar]
  46. STILWELL D. L., Jr Regional variations in the innervation of deep fasciae and aponeuroses. Anat Rec. 1957 Apr;127(4):635–653. doi: 10.1002/ar.1091270402. [DOI] [PubMed] [Google Scholar]
  47. STILWELL D. L., Jr The innervation of tendons and aponeuroses. Am J Anat. 1957 May;100(3):289–317. doi: 10.1002/aja.1001000302. [DOI] [PubMed] [Google Scholar]
  48. Sauerland E. K., Mizuno N. Hypoglossal nerve afferents: elicitation of a polysynaptic hypoglosso-laryngeal reflex. Brain Res. 1968 Aug 26;10(2):256–258. doi: 10.1016/0006-8993(68)90129-7. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Skavenski A. A. Inflow as a source of extraretinal eye position information. Vision Res. 1972 Feb;12(2):221–229. doi: 10.1016/0042-6989(72)90113-7. [DOI] [PubMed] [Google Scholar]
  51. Smith R. D., Marcarian H. Q., Niemer W. T. Direct projections from the masseteric nerve to the mesencephalic nucleus. J Comp Neurol. 1968 Aug;133(4):495–502. doi: 10.1002/cne.901330408. [DOI] [PubMed] [Google Scholar]
  52. Stacey M. J. Free nerve endings in skeletal muscle of the cat. J Anat. 1969 Sep;105(Pt 2):231–254. [PMC free article] [PubMed] [Google Scholar]
  53. TARKHAN A. A., EL-MALEK S. A. On the presence of sensory nerve cells on the hypoglossal nerve. J Comp Neurol. 1950 Oct;93(2):219–228. doi: 10.1002/cne.900930204. [DOI] [PubMed] [Google Scholar]
  54. WOHLFART G., HENRIKSSON K. G. Observations on the distribution, number and innervation of Golgi musculotendinous organs. Acta Anat (Basel) 1960;41:192–204. doi: 10.1159/000141617. [DOI] [PubMed] [Google Scholar]
  55. Weddell G., Harpman J. A., Lambley D. G. The innervation of the musculature of the tongue. J Anat. 1940 Jan;74(Pt 2):255–267. [PMC free article] [PubMed] [Google Scholar]
  56. Wong W. C., Kanagasuntheram R. Early and late effects of median nerve injury on Meissner's and Pacinian corpuscles of the hand of the macaque (M. fascicularis). J Anat. 1971 May;109(Pt 1):135–142. [PMC free article] [PubMed] [Google Scholar]
  57. Woźniak W., Young P. A. Nerve cells in the extracranial portion of the hypoglossal nerve in human fetuses. Anat Rec. 1968 Dec;162(4):517–522. doi: 10.1002/ar.1091620414. [DOI] [PubMed] [Google Scholar]
  58. Zapata P., Torrealba G. Mechanosensory units in the hypoglossal nerve of the cat. Brain Res. 1971 Sep 24;32(2):349–367. doi: 10.1016/0006-8993(71)90329-5. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES