Extraocular muscle proprioceptors and proprioception

Progress in Retinal and Eye Research

Volumn 18, Issue 3, 1999, Pages 269-291

  Ruskell, Gordon L ^a  

^a CITY UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANATOMY; ARTICLE; BRAIN CORTEX; CAT; DEPTH PERCEPTION; EFFERENT NERVE; EXTRAOCULAR MUSCLE; HUMAN; MONKEY; MUSCLE SPINDLE; MUSCLE SPINDLE AFFERENT NERVE; NERVE ENDING; NERVE LESION; NONHUMAN; PRIORITY JOURNAL; PROPRIOCEPTION; TENDON RECEPTOR; VISION;

EID: 0033032517     PISSN: 13509462     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1350-9462(98)00029-9     Document Type: Review

References (136)

1. Abrahams, V. C. (1979) Proprioceptive influences from eye muscle receptors on cells of the superior colliculus. In Control of Posture and Movement. Progress in Brain Research Vol. 50. (ed. R. Granit and O. Pompeiano), pp. 325-334. Elsevier/North-Holland, Amsterdam.
2. Alvarado-Mallart M. R., Batini C., Buisseret-Delmas C., Corvisier J. Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport. Exp. Brain Res. 23:1975;167-179.
3. Alvarado-Mallart M. R., Pinçon-Raymond M. The palisade endings of cat extraocular muscles: a light and electron microscope study. Tissue Cell. 11:1979;567-584.
4. Ashton J. A., Boddy A., Dean S. R., Milleret C., Donaldson I. M. L. Afferent signals from cat extraocular muscles in the medial vestibular nucleus, the nucleus prepositus hypoglossi and adjacent brainstem structures. Neurosci. 26:1988;131-146.
5. Bach-y-Rita P., Murata K. Extraocular proprioceptive responses in the VI nerve of the cat. Quart. J. Exp. Physiol. 49:1964;408-415.
6. Bach-y-Rita P., Ito F. Properties of stretch receptors in cat extraocular muscles. J. Physiol. 186:1966;663-688.
7. Baker R., Precht W., Llinas R. Mossy fibre climbing projections of extraocular afferents to the cerebellum. Brain Res. 38:1972;440-445.
8. Barker, D. (1974) The morphology of muscle receptors. In Muscle Receptors. Handbook of Sensory Physiology, Vol.III/2 (C. C. Hunt ed), pp. 1-190.
9. Batini C., Buisseret P., Buisseret-Delmas C. Trigeminal pathway of the extrinsic eye muscle afferents in cat. Brain Res. 85:1975;74-78.
10. Batini C., Buisseret P., Kado R. T. Extraocular proprioceptive and trigeminal projections to the Purkinje cells of the cerebellar cortex. Arch. Ital. Biol. 112:1974;1-17.
11. Batini, C. and Horcholle-Bossavit, G. (1979) Extraocular muscle afferents and visual input interactions in the superior colliculus of the cat. In Reflex Control of Posture and Movement. Progress in Brain Research, Vol. 50 (ed. R. Granit and O. Pompeiano), pp. 335-344. Elsevier/North-Holland, Amsterdam.
12. Billig I., Buisseret-Delmas C., Buisseret P. Identification of nerve endings in cat extraocular muscles. Anat. Rec. 248:1997;566-575.
13. Blumer R., Lukas J. R., Wasicky R., Mayr R. Presence and structure of innervated myotendinous cylinders in sheep extraocular muscles. Neurosci. Lett. 248:1998;49-52.
14. Bock O., Kommerell G. Visual localization after strabismus surgery is compatible with the "outflow" theory. Vision Res. 26:1986;1825-1829.
15. Bonavolontà A. Richerche comparative nei musculo estrinseci dell'occhio nell'uomo e altri mammiferi. 2. Gli organi musculo-tendinei di Golgi. Quad. Anat. Pract. Ser. XI:1956;153-166.
16. Bortolami R., Lucchi M. L., Pettorossi V. E., Callegari E., Manni E. Localization and somatotopy of sensory cells innervating the extraocular muscles of lamb, pig and cat. Histochemical and electrophysiological investigation. Arch. Ital. Biol. 125:1987;1-15.
17. Bortolami R., Calzi L., Lucchi M. L., Giardino L., Callegari E., Manni E., Pettorossi V. E., Barazzoni A. M., Lalatta Costerbosa G. Peripheral territory and neuropeptides of the trigeminal ganglion neurons centrally projecting through the oculomotor nerve demonstrated by fluorescent double retrograde double-labeling combined with immunocytochemistry. Brain Res. 547:1991;82-88.
18. Bridgeman B., Stark L. Ocular proprioception and efference copy in registering visual direction. Vis. Res. 31:1991;1903-1913.
19. Brindley G. S., Merton P. A. The absence of position sense in the human eye. J. Physiol. 153P:1960;127-130.
20. Brindley G. S., Goodwin G. M., Kulikowski J. J., Leighton D. Stability of vision with a paralysed eye. J. Physiol. 258P:1976;65-66.
21. Browne J. S. The responses of muscle spindles in sheep extraocular muscles. J. Physiol. 251:1975;483-496.
22. Bruenech J. R. Tendon receptors in human extraocular muscles. Vis. Res. 35:1995;S322.
23. Bruenech, P. J. and Ruskell, G. L. (1998) The incidence and form of myotendinous nerve endings in infant and adult human extraocular muscles. In preparation.
24. Brzezinski D. K. Untersuchungen zur Histochemie der Muskelspindeln. II. Mitteilung: Zur Topochemie und Funktion des Spindelraumes und der Spindelkapsel. Acta Histochem. 12:1961;277-288.
25. Buisseret P., Maffei L. Extraocular proprioception projections to the visual cortex. Exp. Brain Res. 28:1977;421-426.
26. Buisseret-Delmas C. Parcours trigéminal des fibres sensorielles provenant des muscles extrinsèques de l'oeil chez le chat. Arch. Ital. Biol. 114:1976;341-356.
27. Buisseret-Delmas C., Buisseret P. Central projections of extraocular muscle afferents in the cat. Neurosci. Lett. 109:1990;48-53.
28. Buzzard E. F. The occurrence of muscle spindles in human ocular muscles. Proc. Roy. Soc. Med. 1:1908;83-87.
29. Campos E. C., Chiesi C., Bolzani R. Abnormal spatial localization in patients with herpes zoster ophthalmicus. Arch. Ophthalmol. 104:1986;1176-1177.
30. Cannon S. C., Robinson D. A. Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J. Neurophysiol. 57:1987;1383-1409.
31. Carpenter, R. H. S. (1988) Movement of the Eyes. (2nd ed), Pion, London, p. 306.
32. Ciaccio G. V. Sur les plaques nerveuses finales dans les tendons des vertébrés. Arch. Ital. Biol. 14:1891;31-57.
33. Cilimbaris P. A. Histologische Untersuchungen über die Muskelspindeln der Augenmuskeln. Arch. Mikr. Anat. 75:1910;692-747.
34. Cooper S., Daniel P. M. Muscle spindles in human extrinsic eye muscles. Brain. 72:1949;1-24.
35. Cooper S., Daniel P. M., Whitteridge D. Afferent impulses in the oculomotor nerve, from the extrinsic eye muscles. J. Physiol. 113:1951;463-474.
36. Cooper S., Daniel P. M., Whitteridge D. Muscle spindles and other sensory endings in the extrinsic eye muscles: the physiology and anatomy of these receptors and of their connexions with the brain-stem. Brain. 78:1955;564-583.
37. Cooper S., Fillenz M. Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of these muscles. J. Physiol. 127:1955;400-413.
38. Daniel P. M. Spiral nerve endings in the extrinsic eye muscles. J. Anat. 80:1946;189-193.
39. Dengis C. A., Steinbach M. J., Kraft S. P. Registered eye position: short- and long-term effects of botulinum toxin injected into eye muscle. Exp. Brain Res. 119:1998;475-482.
40. Dogiel A. S. Die Endigungen der sensiblen Nerven in den Augenmuskeln und deren Sehnen beim Menschen und den Säugetieren. Arch Mikr. Anat Entwick. 68:1906;501-526.
41. Donaldson I. M. L., Long A. C. Interaction between extraocular proprioceptive and visual signals in the superior colliculus of the cat. J. Physiol. 298:1980;85-110.
42. Donaldson I. M. L., Dixon R. A. Excitation of units in the lateral geniculate nucleus and contiguous nuclei of the cat by stretch of extrinsic ocular muscles. Exp. Brain Res. 38:1980;245-255.
43. Duhamel J.-R., Colby C. L., Goldberg M. E. The updating of the representation of visual space in parietal cortex by intended eye movements. Science. 255:1992;90-92.
44. Durston J. H. J. Histochemistry of primate extraocular muscles and the changes of denervation. Br. J. Ophthalmol. 58:1974;196-216.
45. Edwards S. B., Ginsburgh C. L., Henkel C. K., Stein B. E. Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neurol. 184:1979;309-330.
46. Fillenz M. Responses in the brain stem of the cat to stretch of extrinsic ocular muscles. J. Physiol. 128:1955;182-199.
47. Fuchs A. F., Kornhuber H. H. Extraocular muscle afferents to the cerebellum of the cat. J. Physiol. 200:1969;713-722.
48. Gauthier G. M., Mommay D., Vercher J.-L. Ocular muscle proprioception and visual localization of targets in man. Brain. 113:1990;1857-1871.
49. Gauthier G. M., Vercher J.-L., Blouin J. Egocentric visual target position and velocity coding: role of ocular muscle proprioception. Ann. Biomed. Engin. 23:1995;423-435.
50. Gentle A., Ruskell G. L. Pathway of the primary afferent nerve fibres serving proprioception in monkey extraocular muscles. Ophthal. Physiol. Opt. 17:1997;225-231.
51. Golgi C. Sui Nervi dei tendini dell'uomo e di altri vertebrati. Un nuovo organo nervoso terminale muscolo-tendineo. Mem. Reale Accad. Sci. Torino Ser. II. 32:1880;361-385.
52. Graves A. L., Trotter Y., Frégnac Y. Role of extraocular muscle proprioception in the development of depth perception in cats. J. Neurophysiol. 58:1987;816-831.
53. Greene T., Jampel R. Muscle spindles in the extraocular muscles of the macaque. J. Comp. Neurol. 126:1966;547-550.
54. Guthrie B. L., Porter J. D., Sparks D. L. Corollary discharge provides accurate eye position information to the oculomotor system. Science. 221:1983;1193-1195.
55. Harker D. W. The structure and innervation of sheep superior rectus and levator palpebrae extraocular muscles. Invest. Ophthalmol. 11:1972;970-979.
56. Helmholtz H. von (1866) Handbuch der physiologischen Optik. Voss, Leipzig. English translation from: A Treatise on Physiological Optics (ed. J. P. C. Southall) Edn. 3, Vol. 3 (1963). Dover, New York.
57. Helmholtz H. von (1866) Handbuch der physiologischen Optik. Voss, Leipzig. English translation from: A Treatise on Physiological Optics (ed. J. P. C. Southall) Edn. 3, Vol. 3 (1963). Dover, New York.
58. Huber G. C. Sensory nerve terminations in the tendons of the extrinsic eye-muscles of the cat. J. Comp. Neurol. 10:1900;152-158.
59. Hunt, C. C. (1974) The physiology of muscle receptors. In Muscle Receptors. Handbook of Sensory Physiology, Vol. III/2 (ed. C. C. Hunt), pp. 191-234. Springer Verlag, Berlin.
60. Inoue T. A study on the muscle spindle in the human ocular muscles. Acta Med. Fukuoka. 28:1958;235.
61. Irvine S. R., Ludvigh E. J. Is ocular proprioceptive sense concerned in vision? Arch. Ophthalmol. 15:1937;1037-1049.
62. Jami L. Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiol. Rev. 72:1992;623-666.
63. Keller E. L., Robinson D. A. Absence of a stretch reflex in extraocular muscles of the monkey. J. Neurophysiol. 34:1972;908-919.
64. Lal R., Friedlander M. J. Effect of passive eye position changes on retinogeniculate transmission in the cat. J. Neurophysiol. 63:1990;502-522.
65. Lal R., Friedlander M. J. effect of passive eye movements on retinogeniculate transmission in the cat. J. Neurophysiol. 63:1990;523-538.
66. Lewis R. F., Zee D. S. Abnormal spatial localization with trigeminal-oculomotor synkinesis. Evidence for proprioceptive effect. Brain. 116:1993;1105-1118.
67. Lewis R. F., Zee D. S., Gaymard B. M., Guthrie B. L. Extraocular muscle proprioception functions in the control of ocular alignment and eye movement conjugacy. J. Neurophysiol. 72:1994;1028-1031.
68. Ludvigh E. Possible role of proprioception in the extraocular muscles. Arch. Ophthalmol. 48:1952;436-440.
69. Ludvigh E. Control of ocular movements and visual interpretation of environment. Arch. Ophthalmol. 48:1952;442-448.
70. Lukas J. R., Blumer R., Aigner M., Denk M., Baumgartner I., Mayr R. Propriozeption aus äusseren Augenmuskeln des Menschen: zur morphologie ihrer Muskelspindeln. Klin. Monats. Augenheilk. 211:1997;183-187.
71. Lukas J. R., Aigner M., Blumer R., Heinzl H., Mayr R. Number and distribution of neuromuscular spindles in human extraocular muscles. Invest. Ophthalmol. Vis. Sci. 35:1994;4317-4327.
72. Maier A., DeSantis M., Eldred E. The occurrence of muscle spindles in extraocular muscles of various vertebrates. J. Morph. 143:1975;397-408.
73. Manni E., Bortolami R., Desole C. Eye muscle proprioception and the semilunar ganglion. Exp. Neurol. 16:1966;226-236.
74. Manni E., Bortolami R., Desole C. Peripheral pathway of eye muscle proprioception. Exp. Neurol. 22:1968;1-12.
75. Manni E., Palmieri G., Marini R. Peripheral pathway of the proprioceptive afferents from the lateral rectus muscle of the eye. Exp. Neurol. 30:1971;46-53.
76. Manni E., Bortolami R., Pettorossi V. E., Callegari E. Trigeminal afferent fibres in the trunk of the oculomotor nerve of lambs. Exp. Neurol. 50:1976;465-476.
77. Manni E., Bortolami R., Pettorossi V. E., Lucchi M. L., Callegari E., Draicchio F. Influence of oculomotor nerve afferents on central endings of primary trigeminal fibers. Arch. Ital. Biol. 126:1987;29-39.
78. Manni E., Dracchio F., Pettorossi V. E., Carobi C., Grassi S., Bortolami R., Lucchi M. L. On the nature of afferent fibers of oculomotor nerve. Arch. Ital. Biol. 127:1989;99-108.
79. Marchi V. Ueber die Terminalorgane der Nerven (Golgi's Nervenkorperchen) in den sehnen der Augenmuskeln. Graefes Arch. Ophthalmol. 28:1882;203-212.
80. Maruo T. Electromyographical studies on stretch reflex in human extraocular muscle. Japan J. Ophthalmol. 8:1964;96-111.
81. Marini R., Bortolami R. Somatotopic representation of eye muscle proprioception within the superior colliculus of the lamb. Exp. Neurol. 69:1980;226-238.
82. Matsushita M., Ikeda M., Okado N. The cells of origin of the trigemino-thalamic, trigemino-spinal and trigemino-cerebellar projections in the cat. Neurosci. 7:1982;1439-1454.
83. Matthews P. B. C. Where does Sherrington's "muscular sense" originate? Muscles, joints, corollary discharges? Ann. Rev. Neurosci. 5:1982;189-218.
84. McCouch G. P., Adler F. H. Extraocular reflexes. Am. J. Physiol. 100:1932;78-88.
85. Merrillees N. C. R., Sunderland S., Hayhow W. Neuromuscular spindles in the extraocular muscles of man. Anat. Rec. 108:1950;23-30.
86. Merton P. A. The accuracy of directing the eyes in the dark. J. Physiol. 156:1961;555-577.
87. Mukuno K., Nomura T. Fine structure of the muscle spindles in the human extraocular muscles. Acta Soc. Ophthalmol. Jap. 73:1969;2119-2127.
88. Nelson J. S., Meredith A., Stein B. E. Does an extracular proprioceptive signal reach the superior colliculus? J. Neurophysiol. 62:1989;1360-1374.
89. Newsome W. T., Wurtz R. H., Komatsu H. Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J. Neurophysiol. 60:1988;604-620.
90. Nitatori T. The fine structure of human Golgi tendon organs as studied by three-dimensional reconstruction. J. Neurocytol. 17:1988;27-41.
91. Ogasawara K., Onodera S., Shiwa T., Ninomiya S., Tazawa Y. Projections of extraocular muscle primary afferent neurons to the trigeminal sensory complex in cats as studied with the transganglionic transport of horseradish peroxidase. Neurosci. Lett. 73:1987;242-246.
92. Optican L. M., Zee D. S., Chu F. C. Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements. J. Neurophysiol. 54:1985;110-122.
93. Padykula H. S., Gauthier G. F. The ultrastructure of the neuromuscular junctions of mammalian red, white and intermediate skeletal muscle fibres. J. Cell Biol. 46:1970;27-41.
94. Porter J. D. Brainstem terminations of extraocular muscles primary afferent neurons in the monkey. J. Comp. Neurol. 247:1986;133-143.
95. Porter J. D., Donaldson I. M. L. The anatomical substrate for cat extraocular muscle proprioception. Neurosci. 43:1991;473-482.
96. Porter J. D., Guthrie B. L., Sparks D. L. Innervation of monkey extraocular muscles: localization of sensory and motor neurons by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 218:1983;208-219.
97. Porter J. D., Spencer R. F. Localization and morphology of cat extraocular muscle afferent neurones identified by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 204:1982;56-64.
98. Richmond B. R., Wurtz R. H. Vision during saccadic eye movements. II. A corollary discharge to monkey superior colliculus. J. Neurophysiol. 43:1980;1156-1167.
99. Richmond F. J. R., Johnston W. S. W., Baker R. S., Steinbach M. J. Palisade endings in human extraocular muscles. Invest. Ophthalmol. Vis. Sci. 25:1984;471-476.
100. Robbins N. Plasticity at the mature neuromuscular junction. Trends Neurosci. 3:1980;120-121.
101. Ruskell G. L. The fine structure of innervated myotendinous cylinders in extraocular muscles of rhesus monkeys. J. Neurocytol. 7:1978;693-708.
102. Ruskell G. L. The incidence and variety of Golgi tendon organs in extraocular muscles of the rhesus monkey. J. Neurocytol. 8:1979;639-653.
103. Ruskell G. L. Fibre analysis of the nerve to the inferior oblique muscle in monkeys. J. Anat. 137:1983;445-455.
104. Ruskell G. L. Spiral nerve endings in human extraocular muscles terminate in motor end plates. J. Anat. 139:1984;33-44.
105. Ruskell G. L. The tentorial nerve in monkeys is a branch of the cavernous plexus. J. Anat. 157:1988;67-77.
106. Ruskell G. L. The fine structure of human extraocular muscle spindles and their potential proprioceptive capacity. J. Anat. 167:1989;199-214.
107. Ruskell G. L. Golgi tendon organs in the proximal tendon of sheep extraocular muscles. Anat. Rec. 227:1990;25-31.
108. Ruskell G. L. Primate extraocular myotendinous nerve endings project directly to the brainstem in monkeys. Ophthal. Res. 29(Suppl. 1):1997;149.
109. Ruskell, G. L. and Kjellevold-Haugen, I.-B. (1998) Apical myotendonous nerve terminals of extraocular muscles in cynomolgus monkeys. Ophthal. Res., in press.
110. Ruskell G. L., Simons T. Trigeminal nerve pathways to the cerebral arteries in monkeys. J. Anat. 155:1987;23-37.
111. Ruskell G. L., Wilson J. Spiral nerve endings and dapple motor end plates in monkey extraocular muscles. J. Anat. 136:1983;85-95.
112. Saigal R. P., Karamanlidis A. N., Voogt J., Magnana O., Michaloudi H. Secondary trigeminocerebellar projections in sheep studied with the horseradish peroxidase method. J. Comp. Neurol. 189:1980;537-553.
113. Sas J., Appeltauer C. Atypical muscle spindles in the extrinsic eye muscles of man. Acta Anat. 55:1963;311-322.
114. Scalzi A., Price M. Ultrastructure of muscle spindles from the extraocular muscles of sheep. J. Cell. Biol. 47:1970;80a.
115. Sherif M. F., Papadopoulos N. J., Albert E. N. Fiber contribution from the mesencephalic nucleus of the trigeminal nerve to the trochlear nerve in the cat: a histological quantitative study. Anat. Rec. 201:1981;669-678.
116. Sherrington C. S. Note on the knee-jerk and the correlation of action of antagonistic muscles. Proc. Roy. Soc. Lond. 52:1893;556-564.
117. Sherrington C. S. On the proprio-ceptive system, especially in its reflex aspect. Brain. 29:1906;467-482.
118. Sherrington C. S. Observations on the sensual rôle of the proprioceptive nerve-supply of the extrinsic ocular muscles. Brain. 41:1918;332-343.
119. Sivananasingham P. Peripheral pathway of proprioceptive fibres from feline extra-ocular muscles. Acta Anat. 100:1978;173-184.
120. Skavenski A. A. Inflow as a source of extraretinal eye position information. Vis. Res. 12:1972;221-229.
121. Sodi A., Corsi M., Faussone Pellegrini M. S., Salvi G. Fine structure of the receptors at the myotendinous junction of human extraocular muscles. Histol. Histopath. 3:1988;103-113.
122. Stibbe E. P. Sensory components of the motor nerves of the eye. J. Anat. 64:1929;P112-113.
123. Steinbach M. J., Smith D. R. Spatial localization after strabismus surgery: evidence for inflow. Science. 213:1981;1407-1409.
124. Steinbach M. J. Inflow as a long-term calibrator of eye position in humans. Acta Psychologica. 63:1986;297-306.
125. Tanaka H., Sugita Y., Moriya M., Saito H.-A. Analysis of object motion in the ventral part of the medial superior temporal area of the macaque visual cortex. J. Neurophysiol. 69:1993;128-142.
126. Sperry R. W. Neural basis for the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43:1950;482-489.
127. Tozer F. M., Sherrington C. S. Receptors and afferents of the third, fourth, and sixth cranial nerves. Proc. Roy. Soc. Lond. Ser. B. 82:1910;450-457.
128. van Donkelaar P., Gauthier G. M., Blouin J., Vercher J. L. The role of ocular muscle proprioception during modifications in smooth pursuit output. Vis. Res. 37:1997;769-774.
129. Ventre-Dominey J., Dominey P. F., Sindou M. Extraocular proprioception is required for spatial localization in man. Neuroreport. 7:1996;1531-1535.
130. Voss H. Beiträge zur mikroskopischen Anatomie der Augenmuskeln das Menschen. Anat. Anz. 104:1957;345-355.
131. Walker M. F., Fitzgibbon E. J., Goldberg M. E. Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. J. Neurophysiol. 73:1995;1988-2003.
132. Whitteridge D. A separate afferent nerve supply from extraocular muscles of the goat. Quart. J. Exper, Physiol. 40:1955;331-336.
133. Wiberg M., Blomqvist A. The projection to the mesencephalon from the dorsal column nuclei. An anatomical study in the cat. Brain Res. 311:1984;225-244.
134. Wiberg M., Westman J., Blomqvist A. Somatosensory projection to the mesencephalon: an anatomical study in the monkey. J. Comp. Neurol. 264:1987;92-117.
135. Winckler G. L'innervation proprioceptive des muscles extrinsèques du globe oculaire chez L'homme. C.R. Ass. Anat. 43:1956;848-857.
136. Zaki W. Le nerf pathétique chez l'homme. Arch. Anat. Histol. Embryol. 43:1960;105-120.