Age-Related Changes in the Oculomotor System

  • J. Richard Bruenech
Part of the Aging Medicine book series (AGME)


This chapter aims to review the most important parameters in oculomotor control and provide information regarding the functional implications of the age-related changes taking place in the oculomotor system. Age-related changes in muscle fibers such as loss of myofilaments and reduction in mitochondrial content will change the length tension curve of the muscle, making the relationship between the degree of contraction and development of muscle force (i.e., the degree of eye rotation), less predictable. Changes in the pattern of innervation is also likely to interfere with muscle dynamics and thus create an additional variable parameter in the length tension curve. The so-called fibrillen-structure fibers were found to be most affected. These muscle fibers may have more functions than previously assumed. The reduction in ocular motility observed in elderly patients may be caused by age-related changes, either directly through a reduced oculorotatory capacity or indirectly through a reduced ability to manipulate the angle of insertion of the distal tendon during eye rotation.


oculomotor system Motor unit Nerve fibers Sensory receptors age related changes 


  1. 1.
    Jenkyn LR, Reeves AG, Warren T, Whiting RK, Clayton RJ, Moore WW, Rizzo A, Tuzun IM, Bonnett JC, Culpepper (1985) Neurologic signs in senescence. Arch Neurol 42:1154PubMedGoogle Scholar
  2. 2.
    Kokemon E, Bossemeyer RW Jr, Barney J, Williams WJ. (1977) Neurological manifestations of aging. J Gerontol 32:411Google Scholar
  3. 3.
    Loeser RF, Delbono O (2003) Aging of the muscles and joints. In: Hazzard WR, Blass JP, Halter JB, Ouslander JG, Tinetti ME (eds) Principles of Geriatric Medicine & Gerontology, 5th ed. McGraw-Hill, PUBLICATION CITY, p 905–919Google Scholar
  4. 4.
    Pakkar A, Cummings JL (2003) Mental status and neurologic examination in the elderly. In: Hazzard WR, Blass JP, Halter JB, Ouslander JG, Tinetti ME (eds) Principles of Geriatric Medicine & Gerontology, 5th ed. McGraw-Hill PUBLICATION CITY, p 111–119Google Scholar
  5. 5.
    Tinetti ME (1986) Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc 34:119PubMedGoogle Scholar
  6. 6.
    Collins CC (1971) Orbital mechanics. In: Bech-y-Rita P, Collins CC, Hyde JE (eds) The control of eye movements. Academic Press, PUBLICATION CITY, p 285–325Google Scholar
  7. 7.
    Ruskell GL (1999) Extraocular muscle proprioceptors and proprioception. Prog Retin Eye Res 18:126–128CrossRefGoogle Scholar
  8. 8.
    Breinin GM (1957) Electromyographic. Evidence of ocular muscle proprioception in man. Arch Ophthalmol 176–180Google Scholar
  9. 9.
    Keller EL, Robinson DA (1971) Absence of a stretch reflex in extraocular muscle of monkey. J Neurophysiol 34:908–919PubMedGoogle Scholar
  10. 10.
    Demer JL, Miller JM, Poukems V, Vinters HV, Glasgow BJ (1995) Evidence for fibromuscular pulleys of the recti muscles. Invest Ophth Vis Sci 36:1125–1136Google Scholar
  11. 11.
    Clarc RA, Isenberg SJ (2001) The range of ocular movements decreases with ageing. J AAPOS 5:26–30CrossRefGoogle Scholar
  12. 12.
    Büttner U, Büttner-Ennever JA (1988) Present concepts of oculomotor organization. In: Büttner-Ennever (ed) Neuroanatomy of the oculomotor system. Elsevier 1–23Google Scholar
  13. 13.
    Robinson D (1975b) How the oculomotor system repairs itself. Invest Ophthalmol 14:413–415Google Scholar
  14. 14.
    Heines DE, Mihailoff GA, Bloedel JR (2006) The Cerebellum. In: Heines DE (ed) Fundamental Neuroscience for Basic and Clinical Applications, 3rd ed. Elsevier p 432–449Google Scholar
  15. 15.
    Ito M (1982) Cerebellar control of the vestibulo-ocular reflex-around the flocculus hypothesis. Annu Rev Neurosci 5:275–296PubMedCrossRefGoogle Scholar
  16. 16.
    Lisberger SG (1998) Physiologic basis for motor learning in the vestibule-ocular reflex. Otolaryngol Head Neck Surg. 119: 43–48PubMedCrossRefGoogle Scholar
  17. 17.
    Anderson TJ, Jenkins IH, Brooks DJ, Hawken MB, Frackowiak RSJ, Kennard C (1994) Cortical control of saccades and fixation in man: A PET study. Brain 117: 1073–1084PubMedCrossRefGoogle Scholar
  18. 18.
    Horn AKE, Buttner U, Buttner-Ennever JA (YEAR) Brainstem and cerebellar structures for eye movement. PUBLISHER, CITYGoogle Scholar
  19. 19.
    Kerber KA, Enrietto JA, Jacobsen KM, Baloh RW (1998) Disequilibrium in older people-A prospective study. Neurology 51: 574–580PubMedGoogle Scholar
  20. 20.
    Balaban CD (1999) Vestibular autonomic regulation (including motion sickness and mechanisms of vomiting) 12:29–33Google Scholar
  21. 21.
    Brandt T, Dieterich M (1999) The vestibular cortex:Its location, function and disorders. Ann N Y Acad Sci 871:293–312PubMedCrossRefGoogle Scholar
  22. 22.
    Matthews PBC (1991) The human stretch reflex and the motor cortex. Trends Neurosci 14:87–91PubMedCrossRefGoogle Scholar
  23. 23.
    Ruskell GL (1989) The fine structure of human extraocular muscle spindles and their potential proprioceptive capacity. J Anat 167:199–214PubMedGoogle Scholar
  24. 24.
    Collins CC (1971) Orbital mechanics. In: Bach-y-Rita P, Collins CC, and Hyde JE (eds) The Control of Eye Movements Academic Press, New York, p 285–325Google Scholar
  25. 25.
    Breinin GM (1957) Electromyographic evidence of ocular muscle proprioception in man. Arch Ophthal 57:176–180Google Scholar
  26. 26.
    Keller EL, Robinson DA (1971) Absence of a stretch reflex in extraocular muscle of the monkey. J Neurophys 34:908–919Google Scholar
  27. 27.
    Bruenech JR, Ruskell GL (2001) Muscle spindles in extraocular muscles of human infants. Cel Tiss Org 169:388–394CrossRefGoogle Scholar
  28. 28.
    Ruskell GL (1983) Fibre analysis of the nerve to the inferior oblique muscle in monkeys. J Anat 137: 445–455PubMedGoogle Scholar
  29. 29.
    Miller NR (1985) Central trigeminal pathways of the extraocular muscle spindles. In: Miller NR (ed) Walsh & Hoyt's Clinical Neuro-Ophthalmology Williams & Wilkins, Baltimore, p 1030–1032Google Scholar
  30. 30.
    Campos EC, Chiesi C, Bolzani R (1986) Abnormal spatial localisation in patients with herpes zoster ophthalmicus. Arch Ophthal 104:1176–1177PubMedGoogle Scholar
  31. 31.
    Steinbach MJ, Smith DR (1981) Spatial localisation after strabismus surgery. Evidence for inflow. Sci 213:1407–1409Google Scholar
  32. 32.
    Richmond FJR, Johnson WSW, Baker RS, Steinbach MJ (1984) Palisade endings in human extraocular muscles. Invest Ophthal and Vis Sci 25: 471–476Google Scholar
  33. 33.
    Ruskell GL (1978) The fine structure of innervated myotendinous cylinders in extraocular muscles of rhesus monkeys. J Neurocyt 7: 693–708CrossRefGoogle Scholar
  34. 34.
    Bruenech JR, Ruskell GL (2000) Myotendinous nerve endings in human infant and adult extraocular muscles. Anat Rec 260:132–140PubMedCrossRefGoogle Scholar
  35. 35.
    Sodi A, Corsi M, Faussone Pellegrini MS, Salvi G (1988) Fine structure of the receptors at the myotendinous junction of human extraocular muscles. Histol Histopathol 3:103–113PubMedGoogle Scholar
  36. 36.
    Eberhorn AC, Horn AKE, Fischer P, Buttner-Ennever JA (2005) Proprioception and palisade endings in extraocular eye muscles Ann NY Acad.Sci 1039:1–8PubMedCrossRefGoogle Scholar
  37. 37.
    Bruenech JR, I-B Kjellevold Haugen (2005) The structural organization of the distal insertion of human extraocular muscles (EOM). Ophthalmic Res 37:2164–98Google Scholar
  38. 38.
    Kjellevold Haugen IB, Bruenech JR (2005) Sensory receptors in extraocular muscles (EOM) and their potential role in oculomotor control. Ophthalmic Res 37:2163–98Google Scholar
  39. 39.
    Kjellevold Haugen I-B, Bruenech JR (2006) Age-related neuromuscular changes in human extraocular muscles. In: Gomez de Liano R (ed) 30th European Strabismological Association Meeting Transactions. Taylor & Francis, Killarney, Ireland, p 141–144Google Scholar
  40. 40.
    Kelders WPA, Kleinrensink GJ, van der Geest JN, Feenstra L, deZeeuwMiller CI, Frens MA (1985) Compensatory increase of the cervico-ocular reflex with age in healthy humans. In: Miller NR (ed) Walsh and Hoyt's Clinical Neuro-Ophthalmology. Williams & Wilkins, CITYGoogle Scholar
  41. 41.
    Mulch G, Petermann W (1979) Influence of age on results of vestibular function tests. Review of literature and presentation of caloric test results. Ann Oto Rhinol Laryngol 88:1–17Google Scholar
  42. 42.
    Paige GD (1994) Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic and vestibular control of eye movements with ageing. Exp Brain Res 98:355–372PubMedCrossRefGoogle Scholar
  43. 43.
    Huaman AG, Sharpe JA (1993) Vertical saccades in senescence. Invest Ophthalmol Vis Sci 34:2588–2595PubMedGoogle Scholar
  44. 44.
    Yang Q, Kapoula (2006) The control of vertical saccades in aged subjects Exp Brain Res 171:67–77Google Scholar
  45. 45.
    Yang Q, Kapoula. (2006) Aging does not affect the accuracy of vertical saccades nor the quality of their binocular coordination. Neurobiol Aging [Need publication data here].Google Scholar
  46. 46.
    Kjellevold Haugen I-B, Bruenech JR (2005) Histological analysis of the efferent innervation of human extraocular muscles. In: De Faber, J-T (ed) 29th European Strabismological Association Meeting Transactions, Izmir, Turkey, June 1–4, 2004, Taylor & Francis, CITYGoogle Scholar
  47. 47.
    Eggers HM (1982) Functional anatomy of the extraocular muscles. In: Jakobiec FA (ed) Ocular Anatomy, Embryology and Teratology. Harper & Row, Oxford, p 783–824Google Scholar
  48. 48.
    Sevel D (1981) A reappraisal of the origin of the human extraocular muscles. Ophthal 88:1330–1338Google Scholar
  49. 49.
    Gamble H.J, Fenton J, Allsopp G (1978) Electron microscope observations on human fetal striated muscle. J Anatomy 126:567–589Google Scholar
  50. 50.
    Bruenech JR, Kjellevold Haugen IB (2006) Morphological variations in human extraocular muscles and their functional implications. Acta Ophthal Scan vol 84, Suppl 239Google Scholar
  51. 51.
    Miller JE Ageing changes in extraocular muscle. In: Lennerstrand G, Bach-Y-Rita P (eds) Basic Mechanisms of Ocular Motility and their Clinical implications. Pergamon, Oxford, p 47–61Google Scholar
  52. 52.
    Bruenech JR (2000) Neuroanatomical organization of human extraocular muscles review of the effector organ of the oculomotor system. PUBLISHER, CITY, p 1–58Google Scholar
  53. 53.
    Locket NA (1968) The dual nature of human extraocular muscles. Br Ort Jour 25:2–11Google Scholar
  54. 54.
    Nunomura S, Hizawa K, Ii K, Sano T (1984) A histochemical study on fibre types in human extraocular muscles. Biomedical Research 5:295–302Google Scholar
  55. 55.
    Peachey L (1971) The structure of the extraocular muscle fibres in mammals. In: Bach-y-Rita P, Collins CC, Hyde JE (eds) The Control of Eye Movements. Academic Press, New York, 47–66Google Scholar
  56. 56.
    Scott AB, (1973) Collins CC, Division of labour in human extraocular muscles. Arch Ophthal 90:319–322PubMedGoogle Scholar
  57. 57.
    Mühlendyck H, and Ali SS (1978) Histological and ultrastructural studies on the ringbands in human extraocular muscles. Graefes Arch Clin Exp Ophthalmol 208:177–191CrossRefGoogle Scholar
  58. 58.
    Ringel SR, Wilson B, Barden MT, Kaiser KK (1987) Histochemistry of human extraocular muscle. Arch Ophthal 96:1067–1072Google Scholar
  59. 59.
    McKelvie P, Friling R, Davey K, Kowal L (1999) Changes as the result of aging in extraocular muscles: a post-mortem study. Aust N Z J Ophthalmol 27:420–425PubMedCrossRefGoogle Scholar
  60. 60.
    Scelsi R, Scelsi L, Poggi P (2002) Microcirculatory Changes and Disuse Are Cause of Damage to Muscle Fibres During Aging. Basic App Myol 12(5):193–199Google Scholar
  61. 61.
    Berard-Badier M, Pellissier JF, Toga M, Mouillac N, Berard PV (1978) Ultrastructural studies of extraocular muscles in ocular motility disorders. II. Morphological analysis of 38 biopsies. Albrecht Von Graefes Arch Klin Exp Ophthalmol 208 (1–3):193–205PubMedCrossRefGoogle Scholar
  62. 62.
    Ruskell GL (1984) Sheathing of muscle fibres at neuromuscular junctions and at extra-junctional loci in human extra-ocular muscles. J Anat 138(1):33–44PubMedGoogle Scholar
  63. 63.
    Ruskell GL, Kjellevold Haugen IB, Bruenech JR, van der Werf F (2005) Double insertions of extraocular muscles in humans and the pulley theory. J Anat 206:295–306PubMedCrossRefGoogle Scholar
  64. 64.
    Demer JL (2000) Evidence for active control of rectus extraocular muscle pulleys. Invest. Ophthalmol. Vis Sci 41:1280–1290PubMedGoogle Scholar
  65. 65.
    Oh SY, Poukens V, Demer JL (2001) Quantitative analysis of rectus extraocular muscle layers in monkey and humans. Invest Ophthalmol Vis Sci 42:10–16PubMedGoogle Scholar
  66. 66.
    Miller JM (2007) Understanding and Misunderstanding Extraocular Muscle Pulleys. J Vis vol 7, num 11, art 10, p 1–15CrossRefGoogle Scholar
  67. 67.
    Demer JL (2006) Current concepts of mechanical and neural factors in ocular motility. Cur Opin Neurol 19:4–13. 25CrossRefGoogle Scholar
  68. 68.
    Quaia C, Optican LM (1998) Commutative saccadic generator is sufficient to control a 3-D ocular plant with pulleys. J Neurophysiol 79:3197–3215PubMedGoogle Scholar
  69. 69.
    Clark RA, Demer JL (2002) Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging Am J Ophthalmol 132(6):872–8Google Scholar
  70. 70.
    McClung JR, Allman BL, Dimitrova DM, Goldberg SJ (2006) Extraocular connective tissues: A role in human eye movements? Invest Ophthalmol Vis Sci 47:202–205PubMedCrossRefGoogle Scholar
  71. 71.
    McLoon LK, Thorstenson KM, Solomon A, Lewis MP (2007) Myogenic precursor cells in craniofacial muscles. Oral Dis March 13(2):134–40CrossRefGoogle Scholar
  72. 72.
    McNeer KW, Spencer RF (1981) The histopathology of human strabismic extraocular muscle. In: Lennerstrand G, Zee DS, and Keller EL (eds) Functional Basis of Ocular Motility Disorders. Pergamon, Oxford, p 27–38Google Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • J. Richard Bruenech
    • 1
  1. 1.Biomedical Research UnitBuskerud University CollegeKongsbergNorway

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