The Oculomotor Systems Ability to Adapt to Structural Changes Caused by the Process of Senescence: A Review

Jan Richard Bruenech, Inga-Britt Kjellevold Haugen, Ulla Bak, Marianne Maagaard, Frans VanderWerf

Abstract


Age-related binocular vision anomalies are frequently encountered during clinical examination of mature patients. Observations of both concomitant and incomitant restrictions in eye motility indicate that all oculomotor system levels are implicated, from cortical neurons down to extraocular muscles. The system can make adaptations in response to changes induced by growth and ageing, which it does by monitoring and adjusting its own performance. This adaptive mechanism, which is important for maintaining motility, spatial orientation, and perceptual stability, seems to rely on extra-retinal information about eye position in relation to the head and trunk. Receptors in the extraocular muscles and the vestibular system, assumed to contribute to this type of information, also undergo age-related changes. This may compromise their ability to assist in the adaptive process and in potential calibrations of other neural systems. Furthermore, recent observations of a dual, common, final pathway and double insertions of distal extraocular muscles suggest that muscle and tendon receptors may facilitate other, still unresolved, functions in the visual system. Consequently, age-related changes in certain mechanoreceptors may have more severe implications for ocular motility and visual functions than previously assumed. This review aims to detail some of the most frequent neurogenic and myogenic age-related changes that take place in the human oculomotor system and relevant pre-motor structures. It will also address clinical implications of these changes and the potential adaptive mechanism they initiate.

Keywords


Adaptation; ageing; extraocular muscles; muscle pulley; neural integrator

References


Abadi, R.V. (2002). Mechanisms underlying nystagmus. J R Soc Med., 95(5), 231-234. doi:10.1258/jrsm.95.5.231

Abel, L. A., Schmidt, D., Dell’Osso, L. F., & Daroff, R. B. (1978). Saccadic system plasticity in humans. Ann Neurol., 4(4), 313-318. doi:10.1002/ana.410040405

Alvarado-Mallart, R. M., & Pinçon-Raymond, M. (1979). The palisade endings of cat extraocular muscles: a light and electron microscope study. Tissue Cell, 11(3), 567-584. doi:10.1016/0040-8166(79)90063-6

Andersen, R. A., Shenoy, K. V., Crowell, J. A., & Bradley, D . C. (2000). Neural mechanisms for self-motion perception in area MST. Int Rev Neurobiol., 44, 219-233. doi:10.1016/S0074-7742(08)60744-8

Anderson, T. J., Jenkins, I. H., Brooks, D. J., Hawken, M. B., Frackowiak, R. S., & Kennard, C. (1994). Cortical control of saccades and fixation in man. A PET study. Brain, 117(Pt5), 1073-1084. doi:10.1093/brain/117.5.1073

Angelaki, D. E., & Hess, B. J. (2005). Self-motion-induced eye movements: effects on visual acuity and navigation. Nat Rev Neurosci., 6(12), 966-976. doi:10.1038/nrn1804

Annese, J., Gazzaniga, M. S., & Toga, A. W. (2005). Localization of the human cortical visual area MT based on computer aided histological analysis. Cereb Cortex, 15(7), 1044-1053. doi:10.1093/cercor/bhh205

Arnold, D. B., Robinson, D. A., & Leigh, R. J. (1999). Nystagmus induced by pharmacological inactivation of the brainstem ocular motor integrator in monkey. Vision Res., 39(25), 4286-4295. doi:10.1016/S0042-6989(99)00142-X

Arnold, D. B., & Robinson, D. A. (1997). The oculomotor integrator: testing of a neural network model. Exp Brain Res., 113(1), 57-74. doi:10.1007/BF02454142

Bahcelioglu, M., Elmas, C., Kurkcuoglu, A., Calguner, E., Erdogan, D., Kadioglu, D., & Gözil, R. (2008). Age-related immunohistochemical and ultrastructural changes in rat oculomotor nerve. Anat Histol Embryol., 37(4), 279-284. doi:10.1111/j.1439-0264.2008.00841.x

Balaban, C. D. (1999). Vestibular autonomic regulation (including motion sickness and the mechanism of vomiting). Curr Opin Neurol., 12(1), 29-33.

Baloh, R. W., Enrietto, J., Jacobson, K. M., & Lin, A. (2001). Age-related changes in vestibular function: a longitudinal study. Ann NY & Acad Sci., 942, 210-219. doi:10.1111/j.1749-6632.2001.tb03747.x

Barton, J. J., Simpson, T., Kiriakopoulos, E., Stewart, C., Crawley, A., Guthrie, B., Wood, M., & Mikulis, D. (1996). Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception. Ann Neurol., 40(3), 387-398. doi:10.1002/ana.410400308

Becker, W., & Fuchs, A. F. (1969). Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. Vision Res., 9(10), 1247-1258. doi:10.1016/0042-6989(69)90112-6

Becker, W., & Klein, H. M. (1973). Accuracy of saccadic eye movements and maintenance of eccentric eye positions in the dark. Vision Res.,13(6), 1021-1034. doi:10.1016/0042-6989(73)90141-7

Berard-Badier, M., Pellissier, J. F., Toga, M., Mouillac, N., & Berard, P. V. (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), 193-205. doi:10.1007/BF00406993

Blanke, O., & Seeck, M. (2003). Direction of saccadic and smooth eye movements induced by electrical stimulation of the human frontal eye field: effect of orbital position. Exp Brain Res., 150(2), 174-183. doi:10.1007/s00221-003-1395-7

Blumer, R., Konakci, K. Z., Pomikal, C., Wieczorek, G., Lucas, J. R., & Streicher, J. (2009). Palisade Endings: cholinergic sensory organs or effector organs? Invest Ophthalmol Vis Sci., 50(3), 1176-1186. doi:10.1167/iovs.08-2748

Brandt, T., & Dieterich, M. (1999). The vestibular cortex. Its locations, functions, and disorders. Ann N Y Acad Sci., 871, 293-312. doi:10.1111/j.1749-6632.1999.tb09193.x

Brenner, E., Smeets, J. B., & van den Berg, A. V. (2001). Smooth eye movements and spatial localisation. Vision Res., 41(17), 2253-2259. doi:10.1016/S0042-6989(01)00018-9

Brodal, P. (1982). Further observations on the cerebellar projections from the pontine nuclei and the nucleus reticularis tegmenti pontis in the rhesus monkey. J Comp Neurol., 204(1), 44–55. doi:10.1002/cne.902040106

Bruenech, J. R. (2008). Age-related changes in the human oculomotor system. In: C. A. P. Cavallotti & L. Cerulli (Eds.). Age-related changes of the human eye.(pp. 343-373). New York: Springer, Humana Press. doi:10.1007/978-1-59745-507-7_20

Bruenech, J. R., & Kjellevold Haugen, I. B. (2007a). Morphological variations found in human extraocular muscles and their functional implications. Acta Ophthalmol Scand., 84(Suppl 239).

Bruenech, J. R, & Kjellevold Haugen, I. B. (2007b). Neuromuscular principles in the visual system and their potential role in visual discomfort. In: Dainoff (Ed.). Ergonomic and health aspect, Beijing (pp. 10-18), ISBN: 978-3-540-73332-4. Berlin: Springer.

Bruenech, J. R., & Kjellevold Haugen, I. B. (2005a). Structural organization of the distal insertion of human extraocular muscles (EOM). Ophthalmic Res., 37, 2164(98).

Bruenech, J. R, & Kjellevold Haugen, I. B. (2005b). The neuroanatomical basis for fine tuning of eye movements during close work. In: G. Salvendy (Ed.). Human Computer International 2005, U.S. CD, Vol 1, ISBN: O-8058-5807-5 [CD], New Jersey: Lawrence Erlbaum Associates Inc.

Bruenech, J. R, & Ruskell, G. L. (2001). Muscle spindles in extraocular muscles of human infants. Cells Tissues Organs, 169(4), 388-394. doi:10.1159/000047906

Bruenech, J. R., & Ruskell, G. L. (2000). Myotendinous nerve endings in human infant and adult extraocular muscles. Anat Rec., 260(2), 132-140. doi:10.1002/1097-0185(20001001)

Butler, K. M., Zacks, R. T., & Henderson, J. M. (1999). Suppression of reflexive saccades in younger and older adults: age comparisons on an antisaccade task. Mem Cognit., 27(4), 584-591. doi:10.3758/BF03211552

Büttner-Ennever, J. A. (2007). Anatomy of the oculomotor system. In: A. Straube & U. Büttner (Eds.). Neuro-Ophthalmology. Dev Ophthalmol, vol40, (pp. 1-14). doi:10.1159/000100345

Büttner-Ennever, J. A., Horn, A. K., Scherberger, H., & D'Ascanio, P. (2001). Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys. J Comp Neurol., 438(3), 318-335. doi:10.1002/cne.1318

Büttner, U., & Büttner-Ennever, J. A. (2006). Present concepts of oculomotor organization. Prog Brain Res., 151, 1-42. doi:10.1016/S0079-6123(05)51001-X

Campos, E. C., Chiesi, C., Bolzani R. (1986). Abnormal spatial localization in patients with herpez zoster ophthalmicus. Evidence for the presence of proprioceptive information. Arch Ophthalmol., 104(8), 1176-1177.

Clark, R. A., & Demer, J. L. (2002). Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging. Am J Ophthalmol., 134(6), 872-878. doi:10.1016/S0002-9394(02)01695-1

Clark, R. A., & Demer, J. L. (2009). Posterior inflection of weakened lateral rectus path: connective tissue factors reduce response to lateral rectus recession. Am J Ophthalmol., 147(1), 127-133. doi:10.1016/j.ajo.2008.07.029

Clark, R. A., & Isenberg, S. J. (2001). The range of ocular movements decreases with aging. J AAPOS., 5(1), 26-30. doi:10.1067/mpa.2001.111016

Collins, C. C. (1971). Orbital mechanics. In: P. Bach-y-Rita, C. C. Collins, J. E. Hyde (Eds.). The Control of Eye Movements (pp. 185-325). New York: Academic Press.

Culham, J. C., Brandt, S. A., Cavanagh, P., Kanwisher, N. G., Dale, A. M., & Tootell, R. B. (1998). Cortical fMRI activation produced by attentive tracking of moving targets. J Neurophysiol., 80(5), 2657-2670.

De Zeeuw, C. I., Chorev, E., Devor, A., Manor, Y., Van Der Giessen, R. S., De Jeu, M. T., Hoogenraad, C. C., Bijman, J., Ruigrok, T. J., French, P., Jaarsma, D., Kistler, W. M., Meier, C., Petrasch-Parwez, E., Dermietzel, R., Sohl, G., Gueldenagel, M., Willecke, K., & Yarom, Y. (2003). Deformation of network connectivity in the inferior olive of connexin 36-deficient mice is compensated by morphological and electrophysiological changes at the single neuron level. J Neurosci., 23(11), 4700-4711.

De Zeeuw, C. I., van Alphen, A. M., Koekkoek, S. K., Buharin, E., Coesmans, M. P., Morpurgo, M. M., & van den Burg, J. (1998). Recording eye movements in mice: A new approach to investigate the molecular basis of cerebellar control of motor learning and motor timing. Otolaryng Head Neck Surg., 119(3), 193-203. doi:10.1016/S0194-5998(98)70054-3

Dean, P. (1996). Motor unit recruitment in a distributed model of extraocular muscle. J Neurophysiol., 76(2), 727-742.

Demer, J. L. (2006). Current concepts of mechanical and neural factors in ocular motility. Curr Opin Neurol., 19(1), 4-13.

Demer, J. L., Miller, J. M., Poukens, V., Vinters, H. V., & Glasgow, B. J. (1995). Evidence for fibromuscular pulleys of the recti muscles. Invest Ophthalmol Vis Sci., 36(6), 1125-1136.

Demer, J. L., Oh, S. Y., & Poukens, V. (2000). Evidence for active control of rectus extraocular muscle pulleys. Invest Ophthalmol Vis Sci., 41(6), 1280-1290.

Dukelow, S. P., DeSouza, J. F., Culham, J. C., van den Berg, A. V., Menon, R. S., & Vilis, T. (2001). Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. J Neurophysiol., 86(4), 1991-2000.

Eberhorn, A. C, Horn, A. K., Fisher, P., & Büttner-Ennever, J. A. (2005). Proprioception and palisade endings in extraocular eye muscles. Ann NY Acad Sci., 1039, 1-8. doi:10.1196/annals.1325.001

Flügel-Koch, C., Neuhuber, W. L., Kaufman, P. L., & Lütjen-Drecoll, E. (2009). Morphologic indication for proprioception in the human ciliary muscle. Invest Ophthalmol Vis Sci., 50(12), 5529-5536. doi:10.1167/iovs.09-3783

Gamlin, P. D, & Yoon, K. (2000). An area for vergence eye movement in primate frontal cortex. Nature, 407(6807), 1003-1007. doi:10.1038/35039506

Garbutt, S., Han, Y., Kumar, A. N., Harwood, M., Harris, C. M., & Leigh, R. J. (2003). Vertical optokinetic nystagmus and saccades in normal human subjects. Invest Ophthalmol Vis Sci., 44(9), 3833-3841. doi:10.1167/iovs.03-0066

Grosbras, M. H., Lobel, E., Van de Moortele, P. F., LeBihan, D., & Berthoz, A. (1999). An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. Cereb Cortex, 9(7), 705-711. doi:10.1093/cercor/9.7.705

Haines, D. E., Mihailoff, G. A., & Bloedel, J. R. (2006). The Cerebellum. In: D. E. Haines (Ed.). Fundamental Neuroscience for Basic and Clinical Applications, 3rd ed. (pp. 432-449). New York: Elsevier.

Hayakawa, Y., Nakajima, T., Takagi, M., Fukuhara, N., & Abe, H. (2002). Human cerebellar activation in relation to saccadic eye movements: a functional magnetic resonance imaging study. Ophthalmologica, 216(6), 399-405. doi:10.1159/000067551

Helmholtz, H. 1866 (1962). In: Handbuch der Physiologishen Optik, Vol 3. Leipzig: Voss.

Henn, V., Lang, W., Hepp, K., & Reisine, H. (1984). Experimental gaze palsies in monkeys and their relation to human pathology. Brain, 107(Pt 2), 619-636. doi:10.1093/brain/107.2.619

Heron, G., Charman, W. N., & Schor, C. M. (2001). Age Changes in the interactions between the accommodation and vergence systems. Optom Vis Sci., 78(10), 754-762.

Huaman, A. G., & Sharpe, J. A. (1993). Vertical saccades in senescence. Invest Ophthalmol Vis Sci., 34(8), 2588-2595.

Ito, M. (1982). Cerebellar control of the vestibulo-ocular reflex-around the flocculus hypothesis. Annu Rev Neurosci., 5, 275-297. doi:10.1146/annurev.ne.05.030182.001423

Jenkyn, L. R., Reeves, A. G., Warren, T., Whiting, R. K., Clayton, R. J., Moore, W. W., Rizzo, A., Tuzun, I. M., Bonnett, J. C., & Culpepper, B. W. (1985). Neurologic signs in senescence. Arch Neurol., 42(12), 1154-1157.

Kelders, W. P., Kleinrensink, G. J., van der Geest, J. N., Feenstra, L., de Zeeuw, C. I., & Frens, M. A. (2003). Compensatory increase of the cervico-ocular reflex with age in healthy humans. J Physiol., 553(Pt1), 311-317. doi:10.1113/jphysiol.2003.049338

Keller, E. L., & Robinson, D. A. (1971). Absence of a stretch reflex in extraocular muscles of the monkey. J Neurophysiol., 34(5), 908-919.

Kerber, K. A., Enrietto, J. A., Jacobson, K. M., & Baloh, R. W. (1998). Disequilibrium in older people: a prospective study. Neurology, 51(2), 574-580.

Khosrovani, S., Van Der Giessen, R. S., De Zeeuw, C. I., & De Jeu, M. T. (2007). In vivo mouse inferior olive neurons exhibit heterogeneous subthreshold oscillations and spiking patterns. Proc Natl Acad Sci USA, 104(40), 15911-15916. doi:10.1073/pnas.0702727104

King, W. M., Fuchs, A. F., & Magnin, M. (1981). Vertical eye movement-related responses of neurons in midbrain near intestinal nucleus of Cajal. J Neurophysiol., 46(3), 549-562.

Kis, A. C., Singh, V. W., & Niemeier, M. (2009). Short- and long-term plasticity of eye position information: examining perceptual, attentional, and motor influences on perisaccadic perception. J Vis., 9(6)11, 1-21.

Kjellevold Haugen, I. B., & Bruenech, J. R. (2006). Age-related neuromuscular changes in human extraocular muscles. In: R. Gomez de Liano (Ed.). 30th European Strabismological Association Meeting Transactions, Killarney, Co Kerry, Ireland, 2005 (pp. 141-144). ISBN: 84-609-9035-4, Spain.

Kjellevold Haugen, I. B., & Bruenech, J. R. (2005a). Histological analysis of the efferent innervation of human extraocular muscles. In: J. T. De Faber JT (Ed.) 29th European Strabismological Association Meeting Transactions, Izmir, Turkey, 2004 (pp. 91-94). ISBN: 0415372119, Publisher Taylor & Francis.

Kjellevold Haugen, I. B., & Bruenech, J. R. (2005b). Neuroanatomical studies of oculomotor control. In: G. Salvendy (Ed.). Human Computer International 2005, U.S. CD, Vol 1, ISBN: O-8058-5807-5 [CD], New Jersey: Lawrence Erlbaum Associates Inc.

Kokmen, E., Bossemeyer, R. W. Jr., Barney, J., & Williams, W. J. (1977). Neurological manifestations of aging. J Gerontol., 32(4), 411-419. doi:10.1093/geronj/32.4.411

Kommerell, G., Oliver, D. H., & Theopold, H. (1976). Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. Invest Ophthalmol., 15(8), 657-660.

Kono, R., Poukens, V., & Demer, J. L. (2002). Quantitative analysis of the structure of the human extraocular muscle pulley system. Invest Ophthalmol Vis Sci., 43(9), 2923-2932.

Koornneef, L. (1977). Details of the orbital connective tissue system in the adult. Acta Morphol Neerl Scand., 15(1), 1-34.

Krauzlis, R. J. (2004). Recasting the smooth pursuit eye movement system. J Neurophysiol., 91(2), 591-603. doi:10.1152/jn.00801.2003

Langaas, T., Riddel, P. M., Svarverud, E., Ystenæs, A. E., Langeggen, I., & Bruenech, J. R. (2008). Variability of the accommodation response in early onset myopia. Optm Vis Sci., 85(1), 37-48. doi:10.1097/OPX.0b013e31815ed6e9

Langer, T., Kaneko, C. R., Scudder, C. A., & Fuchs, A. F. (1986). Afferents to the abducens nucleus in the monkey and cat. J Comp Neurol., 245(3), 379-400.

Leigh, R. J., & Zee, D. S. (Eds.). (2006). The Neurology of Eye Movements. Oxford, UK: Oxford University Press.

Lennerstrand, G. (2007). Strabismus and eye muscle function. Acta Ophthalmol Scand., 85(7), 711-723. doi:10.1111/j.1600-0420.2007.00853.x

Lienbacher, K., Mustari, M., Ying, H. S., Büttner-Ennever, J. A., & Horn, A. K. (2011). Do palisade endings in extraocular muscles arise from neurons in the motor nuclei? Invest Ophthalmol Vis Sci., 52(5), 2510-2519. doi:10.1167/iovs.10-6008

Loeser, R. F. Jr., & Delbono, O. (2009). Aging of the muscles and joints. In: J. B. Halter, J. G. Ouslander, M. E. Tinetti, S. Studenski, K. P. High, S. Asthana, W. R. Hazzard, N. F. Wollard (Eds.). Hazzard's geriatric medicine and gerontology, 6th ed. (pp. 1355-1368). New York: McGraw-Hill Medical.

Ma, T. P., Graybiel, A. M., & Wurtz, R. H. (1991). Location of saccade-related neurons in the macaque superior colliculus. Exp Brain Res., 85(1), 21-35. doi:10.1007/BF00229983

Machado, L., & Rafal, R. D. (2004). Control of fixation and saccades in humans with chronic lesions of oculomotor cortex. Neuropsychology, 18(1), 115-123. doi:10.1037/0894-4105.18.1.115

Matsuo, S., Bergeron, A., & Guitton, D. (2004). Evidence for Gaze Feedback to the Cat Superior Colliculus: Discharges Reflect Gaze Trajectory Perturbations J. Neurosci., 24(11), 2760-2773. doi:10.1523/JNEUROSCI.5120-03.2004

Matthews, P. B. (1991). The human stretch reflex and the motor cortex. Trends Neurosci., 14(3), 87-91. doi:10.1016/0166-2236(91)90064-2

May, P. J. (2006). The mammalian superior colliculus: laminar structure and connections. Prog Brain Res., 151, 321-378. doi:10.1016/S0079-6123(05)51011-2

McClung, J. R., Allman, B. L., Dimitrova, D. M., & Goldberg, S. J. (2006). Extraocular connective tissues: a role in human eye movements? Invest Ophthalmol Vis Sci., 47(1), 202–205. doi:10.1167/iovs.05-0860

McKelvie, P., Friling, R., Davey, K., & Kowal, L. (1999). Changes as the result of ageing in extraocular muscles: a post-mortem study. Aust NZ J Ophthalmol., 27(6), 420-425. doi:10.1046/j.1440-1606.1999.00244.x

McLoon, L. K. (2009). A new role for satellite cells: control of reinnervation after muscle injury by semaphorin 3A. Focus on “Possible implication of satellite cells in regenerative motoneuritogenesis: HGF upregulates neural chemorepellent Sema3A during myogenic differentiation”. Am J Physiol Cell Physiol., 297(2), C227-230. doi:10.1152/ajpcell.00256.2009

Miller, J. E. (1975). Aging changes in extraocular muscles. In: G. Lennerstrand, P. Bach-Y-Rita (Eds.). Basic Mechanisms of Ocular Motility and Clinical implications (pp. 47-61). Oxford: Pergamon Press.

Miller, J. M. (1989). Functional anatomy of normal human rectus muscles. Vision Res., 29(2), 223-240. doi:10.1016/0042-6989(89)90126-0

Miller, J. M. (2007). Understanding and misunderstanding extraocular muscle pulleys. J Vis., 7(11)10, 1-15. doi:10.1167/7.11.10

Miller, N. R. (1985). Central trigeminal pathways of the extraocular muscle spindles. In: N. R. Miller (Ed.). Walsh & Hoyt's Clinical Neuro-Ophthalmology (pp. 1030-1032). Baltimore: Williams & Wilkins.

Misslisch, H., Tweed, D., Fetter, M., Sievering, D., & Koenig, E. (1994). Rotational kinematics of the human vestibuloocular reflex. III. Listing's law. J Neurophysiol., 72(5), 2490-2502.

Mühlendyck, H., & Ali, S. S. (1978). Histological and ultrastructural studies on the ringbands in human extraocular muscles. Albrecht Von Graefes Arch Klin Exp Ophthalmol., 208(1-3), 177-191. doi:10.1007/BF00406992

Mulch, G., & Petermann, W. (1979). Influence of age on results of vestibular function tests. Review of literature and presentation of caloric test results. Ann Otol Rhinol Laryngol Suppl., 88(2 Pt 2 Suppl 56), 1-17.

Munoz, D. P, & Everling, S. (2004). Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci., 5(3), 218-228. doi:10.1038/nrn1345

Oh, S. Y., Poukens, V., & Demer, J. L. (2001). Quantitative analysis of rectus extraocular muscle layers in monkey and humans. Invest Ophthalmol Vis Sci., 42(1), 10-16.

Optican, L. M. (2005). Sensorimotor transformation for visually guided saccades. Ann NY Acad Sci., 1039, 132-148. doi:10.1196/annals.1325.013

Page, W. K., & Duffy, C. J. (1999). MST neuronal response to heading direction during pursuit eye movements. J Neurophysiol., 81(2), 596-610.

Paige, G. D. (1994). Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging. Exp Brain Res., 98(2), 355-372. doi:10.1007/BF00228423

Park, S. E., Sa, H. S., & Oh, S. Y. (2009). Innervated myotendinous cylinders alterations in human extraocular muscles in patients with strabismus. Korean J Ophthalmol., 23(2), 93-99. doi:10.3341/kjo.2009.23.2.93

Pulaski, P. D., Zee, D. S., & Robinson, D. A. (1981). The behavior of the vestibulo-ocular reflex at high velocities of head rotation. Brain Res., 222(1), 159-165. doi:10.1016/0006-8993(81)90952-5

Quaia, C., & Optican, L. M. (1998). Commutative saccadic generator is sufficient to control a 3-D ocular plant with pulleys. J Neurophysiol., 79(6), 3197-3215.

Ramachandran, R., & Lisberger, S. G. (2005). Normal performance and expression of learning in the vestibulo-ocular reflex (VOR) at high frequencies. J Neurophysiol., 93(4), 2028-2038. doi:10.1152/jn.00832.2004

Rambold, H., Neumann, G., Sander, T., & Helmchen, C. (2006). Age-related changes of vergence under natural viewing conditions. Neurobiol Aging, 27(1), 163-172. doi:10.1016/j.neurobiolaging.2005.01.002

Richmond, F. J., Johnson, W. S., Baker, R. S., & Steinbach, M. J. (1984). Palisade endings in human extraocular muscles. Invest Ophthalmol Vis Sci., 25(4), 471-476.

Richter, H. O., Bänziger, Y., Abdi, S., & Forsman, M. (2010). Stabilization of gaze: a relationship between ciliary muscle contraction and trapezius muscle activity. Vision Res., 50(23), 2559-2569. doi:10.1016/j.visres.2010.08.021

Robinson, D. A. (1978). The functional behavior of the peripheral ocular motor apparatus: a review. In: G. Kommerell (Ed.). Disorders of Ocular Motility: Neurophysiological and clinical aspects (pp. 43-61). Munich: JF Bergman-Verlag.

Robinson, F. R., & Fuchs, A. F. (2001). The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci., 24, 981-1004. doi:10.1146/annurev.neuro.24.1.981

Rosano, C., Krisky, C. M., Welling, J. S., Eddy, W. F., Luna, B., Thulborn K. R., & Sweeney, J. A. (2002). Pursuit and saccadic eye movement subregions in human frontal eye field: a high-resolution fMRI investigation. Cereb Cortex, 12(2), 107-115. doi:10.1093/cercor/12.2.107

Ruskell, G. L. (1999). Extraocular muscle proprioceptors and proprioception. Prog Retin Eye Res., 18(3), 269-291. doi:10.1016/S1350-9462(98)00029-9

Ruskell, G. L., Kjellevold Haugen, I. B., Bruenech, J. R., & van der Werf, F. (2005). Double insertions of extraocular muscles in humans and the pulley theory. J Anat., 206(3), 295-306. doi:10.1111%2Fj.1469-7580.2005.00383.x

Ruskell, G. L. (1984). Sheathing of muscle fibres at neuromuscular junctions and at extra-junctional loci in human extra-ocular muscles. J Anat., 138(Pt1), 33-44.

Ruskell, G. L. (1989). The fine structure of human extraocular muscle spindles and their potential proprioceptive capacity. J Anat., 167, 199-214.

Ruskell, G. L. (1978). The fine structure of innervated myotendinous cylinders in extraocular muscles of rhesus monkeys. J Neurocytol., 7(6), 693-708. doi:10.1007/BF01205145

Sahin, E., & DePinho, R. A. (2010). Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature, 464(7288), 520-528. doi:10.1038/nature08982

Sakai, K., Rowe, J. B., & Passingham, R. E. (2002). Active maintenance in prefrontal area 46 creates distractor-resistant memory. Nat Neurosci., 5(5), 479-484. doi:10.1038/nn846

Scelsi, R., Scelsi, L., & Poggi, P. (2002). Microcirculatory changes and disuse are cause to damage to muscle fibres during aging. Basic Appl Myol., 12(5), 193-199.

Sharma, S., Ray, B., Bhardwaj, D., Dwivedi, A. K., & Roy, T. S. (2009). Age changes in the human oculomotor nerve-a stereological study. Ann Anat., 191(3), 260-266. doi:10.1016/j.aanat.2009.02.008

Sherrington, C. S. (1918). Observations on the sensual role of the proprioceptive nerve supply of the extrinsic ocular muscles. Brain, 41, 332-343. doi:10.1093/brain/41.3-4.332

Shipp, S., de Jong, B. M., Zihl, J., Frackowiak, R. S., & Zeki, S. (1994). The brain activity related to residual motion vision in a patient with bilateral lesion of v5. Brain, 117(Pt5), 1023-1038. doi:10.1093/brain/117.5.1023

Siebeck, R., & Krüger, P. (1955) [The histological structure of the extrinsic ocular muscles as an indication of their function]. [Article in German] Albrecht Von Graefes Arch Ophthalmol., 156(6), 636-652.

Simonsz, H. J., Harting, F., de Waal, B. J., & Verbeeten, B. W. (1985). Sideways displacement and curved path of recti eye muscles. Arch Ophthalmol., 103(1), 124-128.

Sodi, A., Corsi, M., Faussone Pellegrini, M. S., & Salvi, G. (1988). Fine structure of the receptors at the myotendinous junction of human extraocular muscles. Histol Histopathol., 3(2), 103-113.

Sommer, M. A., & Wurtz, R. H. (2004). What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J Neurophysiol., 91(3), 1403-1423. doi:10.1152/jn.00740.2003

Sommer, M. A., & Wurtz, R. H. (2008). Visual perception and corollary discharge. Perception, 37(3), 408-418.

Steinbach, M. J., & Smith, D. R. (1981). Spatial localization after strabismus surgery: evidence for inflow. Science, 213(4514), 1407-1409. doi:10.1126/science.7268444

Tanaka, M., & Lisberger, S. G. (2001). Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex. Nature, 409, 191-194. doi:10.1038/35051582

Tusa, R. J., Mustari, M. J., Das, V. E., & Boothe, R. G. (2002). Animal models for visual deprivation-induced strabismus and nystagmus. Ann NY Acad Sci., 956, 346-360. doi:10.1111/j.1749-6632.2002.tb02833.x

Ugolini, G., Klam, F., Doldan Dans, M., Dubayle, D., Brandi, A. M., Büttner-Ennever, J., & Graf, W. (2006). Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: differences in monosynaptic input to “slow” and “fast” abducens motoneurons. J Comp Neurol., 498(6), 762-785. doi:10.1002/cne.21092

Vivo, J., Morales, J. L., Díz, A., Galisteo, A. M., Monterde, J. G., Agüera, E., & Miró, F. (2006). Structural and ultrastructural study of the intracranial portion of the oculomotor, trochlear and abducent nerves in dog. Anat Histol Embryol., 35(3), 184-189. doi:10.1111/j.1439-0264.2005.00658.x

Voogd, J., & Wylie, D. R. (2004). Functional and anatomical organization of floccular zones: a preserved feature in vertebrates. J Comp Neurol., 470(2), 107-112. doi:10.1002/cne.11022

Waespe, W., Cohen, B., & Raphan, T. (1983). Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Exp Brain Res., 50(1), 9-33. doi:10.1007/BF00238229

Wahlberg, M., Lindskoog Pettersson, A., Rosén, R., Nilsson, M., Unsbo, P., & Brautaset, R. (2011). Clinical importance of spherical and chromatic aberration on the accommodative response in contact lens wear. J Modern Optics,Vol58(19-20),1696-1702. doi:10.1080/09500340.2011.565374

Wurtz, R. H. (2008). Neuronal mechanisms of visual stability. Vision Res., 48(20), 2070-2089. doi:10.1016/j.visres.2008.03.021

Xing, J., & Andersen, R. A. (2000). Models of the posterior parietal cortex which perform multimodal integration and represent space in several coordinate frames. J Cogn Neurosci., 12(4), 601-614. doi:10.1162/089892900562363

Yang, Q., & Kapoula, Z. (2006). The control of vertical saccades in aged subjects. Exp Brain Res., 171(1), 67-77. doi:10.1007/s00221-005-0249-x

Zivotofsky, A. Z., Rottach, K. G., Averbuch-Heller, L., Kori, A. A., Thomas, C. W., Dell’Osso, L. F., & Leigh, R. J. (1996). Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion. J Neurophysiol., 76(6), 3617-3632. doi:10.1016/S0042-6989(97)00288-5


Full Text: PDF

DOI: 10.5384/sjovs.vol5i1p1-14