1932

Abstract

Disrupting binocular vision in infancy leads to strabismus and oftentimes to a variety of associated visual sensory deficits and oculomotor abnormalities. Investigation of this disorder has been aided by the development of various animal models, each of which has advantages and disadvantages. In comparison to studies of binocular visual responses in cortical structures, investigations of neural oculomotor structures that mediate the misalignment and abnormalities of eye movements have been more recent, and these studies have shown that different brain areas are intimately involved in driving several aspects of the strabismic condition, including horizontal misalignment, dissociated deviations, A and V patterns of strabismus, disconjugate eye movements, nystagmus, and fixation switch. The responses of cells in visual and oculomotor areas that potentially drive the sensory deficits and also eye alignment and eye movement abnormalities follow a general theme of disrupted calibration, lower sensitivity, and poorer specificity compared with the normally developed visual oculomotor system.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-111815-114335
2016-10-14
2024-05-07
Loading full text...

Full text loading...

/deliver/fulltext/vision/2/1/annurev-vision-111815-114335.html?itemId=/content/journals/10.1146/annurev-vision-111815-114335&mimeType=html&fmt=ahah

Literature Cited

  1. Adams DL, Economides JR, Horton JC. 2015. Contrasting effects of strabismic amblyopia on metabolic activity in superficial and deep layers of striate cortex. J. Neurophysiol. 113:3337–44 [Google Scholar]
  2. Adams DL, Economides JR, Sincich LC, Horton JC. 2013. Cortical metabolic activity matches the pattern of visual suppression in strabismus. J. Neurosci. 33:3752–59 [Google Scholar]
  3. Agaoglu MN, Joshi AC, Agaoglu S, Das VE. 2014a. Abducens neurons responses in monkeys with strabismus. Investig. Ophthalmol. Vis. Sci. 55:2572 [Google Scholar]
  4. Agaoglu MN, LeSage SK, Joshi AC, Das VE. 2014b. Spatial patterns of fixation-switch behavior in strabismic monkeys. Investig. Ophthalmol. Vis. Sci. 55:1259–68 [Google Scholar]
  5. Agaoglu MN, Pullela M, Degler BA, Joshi AC, Agaoglu S. et al. 2015a. Neural plasticity following surgical correction of strabismus in monkeys Presented at Annu. Meet. Soc. Neurosci., Oct. 19, Chicago
  6. Agaoglu S, Agaoglu MN, Das VE. 2015b. Motion information via the nonfixating eye can drive optokinetic nystagmus in strabismus. Investig. Ophthalmol. Vis. Sci. 56:6423–32 [Google Scholar]
  7. Anderson BC, Christiansen SP, Grandt S, Grange RW, McLoon LK. 2006. Increased extraocular muscle strength with direct injection of insulin-like growth factor-I. Investig. Ophthalmol. Vis. Sci. 47:2461–67 [Google Scholar]
  8. Berg KT, Hunter DG, Bothun ED, Antunes-Foschini R, McLoon LK. 2012. Extraocular muscles in patients with infantile nystagmus: adaptations at the effector level. Arch. Ophthalmol. 130:343–49 [Google Scholar]
  9. Birch EE. 2013. Amblyopia and binocular vision. Prog. Retin. Eye Res. 33:67–84 [Google Scholar]
  10. Boothe RG, Brown RJ. 1996. What happens to binocularity in primate strabismus?. Eye 10:199–208 [Google Scholar]
  11. Boothe RG, Dobson V, Teller DY. 1985. Postnatal development of vision in human and nonhuman primates. Annu. Rev. Neurosci. 8:495–545 [Google Scholar]
  12. Brodsky MC. 2007. Dissociated horizontal deviation: clinical spectrum, pathogenesis, evolutionary underpinnings, diagnosis, treatment, and potential role in the development of infantile esotropia (an American Ophthalmological Society thesis). Trans. Am. Ophthalmol. Soc. 105272–93 [Google Scholar]
  13. Chino YM, Shansky MS, Jankowski WL, Banser FA. 1983. Effects of rearing kittens with convergent strabismus on development of receptive-field properties in striate cortex neurons. J. Neurophysiol. 50:265–86 [Google Scholar]
  14. Chino YM, Smith EL 3rd, Hatta S, Cheng H. 1997. Postnatal development of binocular disparity sensitivity in neurons of the primate visual cortex. J. Neurosci. 17:296–307 [Google Scholar]
  15. Christiansen SP, Harral RL 3rd, Brown H. 1996. Extraocular muscle fiber morphometry following combined recession–resection procedures in rabbits. J. Pediatr. Ophthalmol. Strabismus 33:247–50 [Google Scholar]
  16. Christiansen SP, McLoon LK. 2006. The effect of resection on satellite cell activity in rabbit extraocular muscle. Investig. Ophthalmol. Vis. Sci. 47:605–13 [Google Scholar]
  17. Christiansen SP, Peterson D, To T, Youle R, McLoon L. 2002. Long-term effects of ricin-mAb 35 on extraocular muscles of rabbits: potential treatment for strabismus. Investig. Ophthalmol. Vis. Sci. 43:679–85 [Google Scholar]
  18. Crawford ML. 2000. Animal models in strabismus: sensory aspects of a comitant strabismus. Advances in Strabismus Research: Basic and Clinical Aspects G Lennerstrand, J Ygge 121–30 London: Portland Press [Google Scholar]
  19. Crawford ML, Blake R, Cool SJ, von Noorden GK. 1975. Physiological consequences of unilateral and bilateral eye closure in macaque monkeys: some further observations. Brain Res. 84:150–54 [Google Scholar]
  20. Crawford ML, Harwerth RS, Chino YM, Smith EL 3rd. 1996. Binocularity in prism-reared monkeys. Eye 10:161–66 [Google Scholar]
  21. Crawford ML, Smith EL 3rd, Harwerth RS, von Noorden GK. 1984. Stereoblind monkeys have few binocular neurons. Investig. Ophthalmol. Vis. Sci. 25:779–81 [Google Scholar]
  22. Crawford ML, von Noorden GK. 1979a. Concomitant strabismus and cortical eye dominance in young rhesus monkeys. Trans. Ophthalmol. Soc. U. K. 99:369–74 [Google Scholar]
  23. Crawford ML, von Noorden GK. 1979b. The effects of short-term experimental strabismus on the visual system in Macaca mulatta. Investig. Ophthalmol. Vis. Sci. 18:496–505 [Google Scholar]
  24. Crawford ML, von Noorden GK. 1980. Optically induced concomitant strabismus in monkeys. Investig. Ophthalmol. Vis. Sci. 19:1105–9 [Google Scholar]
  25. Cullen KE, Van Horn MR. 2011. The neural control of fast versus slow vergence eye movements. Eur. J. Neurosci. 33:2147–54 [Google Scholar]
  26. Cynader M, Hoffmann KP. 1981. Strabismus disrupts binocular convergence in cat nucleus of the optic tract. Brain Res. 227:132–36 [Google Scholar]
  27. Das VE. 2008. Investigating mechanisms of strabismus in nonhuman primates. J. AAPOS 12:324–25 [Google Scholar]
  28. Das VE. 2009. Alternating fixation and saccade behavior in nonhuman primates with alternating occlusion-induced exotropia. Investig. Ophthalmol. Vis. Sci. 50:3703–10 [Google Scholar]
  29. Das VE. 2012. Responses of cells in the midbrain near-response area in monkeys with strabismus. Investig. Ophthalmol. Vis. Sci. 53:3858–64 [Google Scholar]
  30. Das VE, Fu LN, Mustari MJ, Tusa RJ. 2005. Incomitance in monkeys with strabismus. Strabismus 13:33–41 [Google Scholar]
  31. Das VE, Mustari MJ. 2007. Correlation of cross-axis eye movements and motoneuron activity in non-human primates with “A” pattern strabismus. Investig. Ophthalmol. Vis. Sci. 48:665–74 [Google Scholar]
  32. Das VE, Ono S, Tusa RJ, Mustari MJ. 2004. Conjugate adaptation of saccadic gain in non-human primates with strabismus. J. Neurophysiol. 91:1078–84 [Google Scholar]
  33. Demer JL. 2001. Clarity of words and thoughts about strabismus. Am. J. Ophthalmol. 132:757–59 [Google Scholar]
  34. Demer JL, Poukens V, Ying H, Shan X, Tian J, Zee DS. 2010. Effects of intracranial trochlear neurectomy on the structure of the primate superior oblique muscle. Investig. Ophthalmol. Vis. Sci. 51:3485–93 [Google Scholar]
  35. Distler C, Hoffmann KP. 1996. Retinal slip neurons in the nucleus of the optic tract and dorsal terminal nucleus in cats with congenital strabismus. J. Neurophysiol. 75:1483–94 [Google Scholar]
  36. Economides JR, Adams DL, Horton JC. 2012. Perception via the deviated eye in strabismus. J. Neurosci. 32:10286–95 [Google Scholar]
  37. Economides JR, Adams DL, Horton JC. 2014. Eye choice for acquisition of targets in alternating strabismus. J. Neurosci. 34:14578–88 [Google Scholar]
  38. Economides JR, Adams DL, Horton JC. 2016. Variability of ocular deviation in strabismus. JAMA Ophthalmol. 134:63–69 [Google Scholar]
  39. Economides JR, Adams DL, Jocson CM, Horton JC. 2007. Ocular motor behavior in macaques with surgical exotropia. J. Neurophysiol. 98:3411–22 [Google Scholar]
  40. Fenstemaker SB, Kiorpes L, Movshon JA. 2001. Effects of experimental strabismus on the architecture of macaque monkey striate cortex. J. Comp. Neurol. 438:300–17 [Google Scholar]
  41. Fu L, Tusa RJ, Mustari MJ, Das VE. 2007. Horizontal saccade disconjugacy in strabismic monkeys. Investig. Ophthalmol. Vis. Sci. 48:3107–14 [Google Scholar]
  42. Fuchs AF, Kaneko CR, Scudder CA. 1985. Brainstem control of saccadic eye movements. Annu. Rev. Neurosci. 8:307–37 [Google Scholar]
  43. Gamlin P, Zhang H. 1996. Effects of muscimol blockade of the posterior fastigial nucleus on vergence and ocular accommodation in the primate Presented at Annu. Meet. Soc. Neurosci., Washington, DC
  44. Ghasia FF, Shaikh AG. 2013. Pattern strabismus: Where does the brain's role end and the muscle's begin?. J. Ophthalmol. 2013:301256 [Google Scholar]
  45. Ghasia FF, Shaikh AG, Jacobs J, Walker MF. 2015. Cross-coupled eye movement supports neural origin of pattern strabismus. Investig. Ophthalmol. Vis. Sci. 56:2855–66 [Google Scholar]
  46. Ghasia FF, Tychsen L. 2014. Horizontal and vertical optokinetic eye movements in macaque monkeys with infantile strabismus: directional bias and crosstalk. Investig. Ophthalmol. Vis. Sci. 55:265–74 [Google Scholar]
  47. Ghasia FF, Wilmot G, Ahmed A, Shaikh AG. 2016. Strabismus and micro-opsoclonus in Machado-Joseph disease. Cerebellum 15491–97
  48. Govindan M, Mohney BG, Diehl NN, Burke JP. 2005. Incidence and types of childhood exotropia: a population-based study. Ophthalmology 112:104–8 [Google Scholar]
  49. Greenberg AE, Mohney BG, Diehl NN, Burke JP. 2007. Incidence and types of childhood esotropia: a population-based study. Ophthalmology 114:170–74 [Google Scholar]
  50. Guyton DL. 2000. Dissociated vertical deviation: etiology, mechanism, and associated phenomena. Costenbader lecture. J. AAPOS 4:131–44 [Google Scholar]
  51. Guyton DL. 2006. The 10th Bielschowsky Lecture. Changes in strabismus over time: the roles of vergence tonus and muscle length adaptation. Binocul. Vis. Strabismus Q. 21:81–92 [Google Scholar]
  52. Guyton DL, Cheeseman EW Jr., Ellis FJ, Straumann D, Zee DS. 1998. Dissociated vertical deviation: an exaggerated normal eye movement used to damp cyclovertical latent nystagmus. Trans. Am. Ophthalmol. Soc. 96:389–424; discussion 424–29 [Google Scholar]
  53. Harrison AR, Anderson BC, Thompson LV, McLoon LK. 2007. Myofiber length and three-dimensional localization of NMJs in normal and botulinum toxin treated adult extraocular muscles. Investig. Ophthalmol. Vis. Sci. 48:3594–601 [Google Scholar]
  54. Harwerth RS, Smith EL 3rd, Boltz RL, Crawford ML, von Noorden GK. 1983. Behavioral studies on the effect of abnormal early visual experience in monkeys: spatial modulation sensitivity. Vis. Res. 23:1501–10 [Google Scholar]
  55. Harwerth RS, Smith EL 3rd, Duncan GC, Crawford ML, von Noorden GK. 1986. Multiple sensitive periods in the development of the primate visual system. Science 232:235–38 [Google Scholar]
  56. Horton JC, Hocking DR, Adams DL. 1999. Metabolic mapping of suppression scotomas in striate cortex of macaques with experimental strabismus. J. Neurosci. 19:7111–29 [Google Scholar]
  57. Hoyt CS, Good WV. 1995. Acute onset concomitant esotropia: When is it a sign of serious neurological disease?. Br. J. Ophthalmol. 79:498–501 [Google Scholar]
  58. Hubel DH, Wiesel TN. 1965. Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28:1041–59 [Google Scholar]
  59. Hubel DH, Wiesel TN. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206:419–36 [Google Scholar]
  60. Joshi AC, Das VE. 2011. Responses of medial rectus motoneurons in monkeys with strabismus. Investig. Ophthalmol. Vis. Sci. 52:6697–705 [Google Scholar]
  61. Joshi AC, Das VE. 2013. Muscimol inactivation of caudal fastigial nucleus and posterior interposed nucleus in monkeys with strabismus. J. Neurophysiol. 110:1882–91 [Google Scholar]
  62. Judge SJ, Cumming BG. 1986. Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. J. Neurophysiol. 55:915–30 [Google Scholar]
  63. Kapoula Z, Bucci MP, Eggert T, Garraud L. 1997. Impairment of the binocular coordination of saccades in strabismus. Vis. Res. 37:2757–66 [Google Scholar]
  64. Kheradmand A, Zee DS. 2011. Cerebellum and ocular motor control. Front. Neurol. 2:53 [Google Scholar]
  65. King WM, Fuchs AF, Magnin M. 1981. Vertical eye movement-related responses of neurons in midbrain near intestinal nucleus of Cajal. J. Neurophysiol. 46:549–62 [Google Scholar]
  66. King WM, Zhou W. 2000. New ideas about binocular coordination of eye movements: Is there a chameleon in the primate family tree?. Anat. Rec. 261:153–61 [Google Scholar]
  67. Kiorpes L. 1992. Effect of strabismus on the development of vernier acuity and grating acuity in monkeys. Vis. Neurosci. 9:253–59 [Google Scholar]
  68. Kiorpes L. 2006. Visual processing in amblyopia: animal studies. Strabismus 14:3–10 [Google Scholar]
  69. Kiorpes L. 2015. Visual development in primates: neural mechanisms and critical periods. Dev. Neurobiol. 75:1080–90 [Google Scholar]
  70. Kiorpes L, Boothe RG, Carlson MR, Alfi D. 1985. Frequency of naturally occurring strabismus in monkeys. J. Pediatr. Ophthalmol. Strabismus 22:60–64 [Google Scholar]
  71. Kiorpes L, Kiper DC, O'Keefe LP, Cavanaugh JR, Movshon JA. 1998. Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. J. Neurosci. 18:6411–24 [Google Scholar]
  72. Kiorpes L, Walton PJ, O'Keefe LP, Movshon JA, Lisberger SG. 1996. Effects of early-onset artificial strabismus on pursuit eye movements and on neuronal responses in area MT of macaque monkeys. J. Neurosci. 16:6537–53 [Google Scholar]
  73. Kumagami T, Zhang B, Smith EL 3rd, Chino YM. 2000. Effect of onset age of strabismus on the binocular responses of neurons in the monkey visual cortex. Investig. Ophthalmol. Vis. Sci. 41:948–54 [Google Scholar]
  74. Leigh RJ, Zee DS. 2015. The Neurology of Eye Movements New York: Oxford Univ. Press
  75. Levi DM. 2006. Visual processing in amblyopia: human studies. Strabismus 14:11–19 [Google Scholar]
  76. Levi DM. 2013. Linking assumptions in amblyopia. Vis. Neurosci. 30:277–87 [Google Scholar]
  77. Levi DM, Knill DC, Bavelier D. 2015. Stereopsis and amblyopia: a mini-review. Vis. Res. 114:17–30 [Google Scholar]
  78. Luschei ES, Fuchs AF. 1972. Activity of brain stem neurons during eye movements of alert monkeys. J. Neurophysiol. 35:445–61 [Google Scholar]
  79. Maruko I, Zhang B, Tao X, Tong J, Smith EL 3rd, Chino YM. 2008. Postnatal development of disparity sensitivity in visual area 2 (V2) of macaque monkeys. J. Neurophysiol. 100:2486–95 [Google Scholar]
  80. May PJ, Porter JD, Gamlin PD. 1992. Interconnections between the primate cerebellum and midbrain near-response regions. J. Comp. Neurol. 315:98–116 [Google Scholar]
  81. Mays LE. 1984. Neural control of vergence eye movements: convergence and divergence neurons in midbrain. J. Neurophysiol. 51:1091–108 [Google Scholar]
  82. McLoon LK, Anderson BC, Christiansen SP. 2006. Increasing muscle strength as a treatment for strabismus: sustained release of insulin-like growth factor-1 in rabbit extraocular muscle. J. AAPOS 10:424–29 [Google Scholar]
  83. McLoon LK, Christiansen SP. 2003. Increasing extraocular muscle strength with insulin-like growth factor II. Investig. Ophthalmol. Vis. Sci. 44:3866–72 [Google Scholar]
  84. Miller JM, Scott AB, Danh KK, Strasser D, Sane M. 2013. Bupivacaine injection remodels extraocular muscles and corrects comitant strabismus. Ophthalmology 120:2733–40 [Google Scholar]
  85. Mori T, Matsuura K, Zhang B, Smith EL 3rd, Chino YM. 2002. Effects of the duration of early strabismus on the binocular responses of neurons in the monkey visual cortex (V1). Investig. Ophthalmol. Vis. Sci. 43:1262–69 [Google Scholar]
  86. Murakami S, Noda H, Warabi T. 1991. Converging eye movements evoked by microstimulation of the fastigial nucleus of macaque monkeys. Neurosci. Res. 10:106–17 [Google Scholar]
  87. Mustari MJ, Ono S. 2011. Neural mechanisms for smooth pursuit in strabismus. Ann. N. Y. Acad. Sci. 1233:187–93 [Google Scholar]
  88. Mustari MJ, Ono S, Vitorello KC. 2008. How disturbed visual processing early in life leads to disorders of gaze-holding and smooth pursuit. Prog. Brain Res. 171:487–95 [Google Scholar]
  89. Mustari MJ, Tusa RJ, Burrows AF, Fuchs AF, Livingston CA. 2001. Gaze-stabilizing deficits and latent nystagmus in monkeys with early-onset visual deprivation: role of the pretectal NOT. J. Neurophysiol. 86:662–75 [Google Scholar]
  90. Narasimhan A, Tychsen L, Poukens V, Demer JL. 2007. Horizontal rectus muscle anatomy in naturally and artificially strabismic monkeys. Investig. Ophthalmol. Vis. Sci. 48:2576–88 [Google Scholar]
  91. Noda H, Sugita S, Ikeda Y. 1990. Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J. Comp. Neurol. 302:330–48 [Google Scholar]
  92. O'Dell C, Boothe RG. 1997. The development of stereoacuity in infant rhesus monkeys. Vis. Res. 37:2675–84 [Google Scholar]
  93. Oh SY, Clark RA, Velez F, Rosenbaum AL, Demer JL. 2002. Incomitant strabismus associated with instability of rectus pulleys. Investig. Ophthalmol. Vis. Sci. 43:2169–78 [Google Scholar]
  94. Ohtsuka K, Maekawa H, Sawa M. 1993. Convergence paralysis after lesions of the cerebellar peduncles. Ophthalmologica 206:143–48 [Google Scholar]
  95. Ono S, Das VE, Mustari MJ. 2012. Conjugate adaptation of smooth pursuit during monocular viewing in strabismic monkeys with exotropia. Investig. Ophthalmol. Vis. Sci. 53:2038–45 [Google Scholar]
  96. Optican LM, Zee DS, Chu FC. 1985. Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements. J. Neurophysiol. 54:110–22 [Google Scholar]
  97. Patel VR, Zee DS. 2015. The cerebellum in eye movement control: nystagmus, coordinate frames and disconjugacy. Eye 29:191–95 [Google Scholar]
  98. Pirdankar OH, Das VE. 2016. Influence of target parameters on fixation stability in normal and strabismic monkeys. Investig. Ophthalmol. Vis. Sci. 57:108795 [Google Scholar]
  99. Quaia C, Shan X, Tian J, Ying H, Optican LM. et al. 2008. Acute superior oblique palsy in the monkey: effects of viewing conditions on ocular alignment and modelling of the ocular motor plant. Prog. Brain Res. 171:47–52 [Google Scholar]
  100. Quick MW, Boothe RG. 1989. Measurement of binocular alignment in normal monkeys and in monkeys with strabismus. Investig. Ophthalmol. Vis. Sci. 30:1159–68 [Google Scholar]
  101. Quick MW, Boothe RG. 1992. A photographic technique for measuring horizontal and vertical eye alignment throughout the field of gaze. Investig. Ophthalmol. Vis. Sci. 33:234–46 [Google Scholar]
  102. Quick MW, Tigges M, Gammon JA, Boothe RG. 1989. Early abnormal visual experience induces strabismus in infant monkeys. Investig. Ophthalmol. Vis. Sci. 30:1012–17 [Google Scholar]
  103. Richards M, Wong A, Foeller P, Bradley D, Tychsen L. 2008. Duration of binocular decorrelation predicts the severity of latent (fusion maldevelopment) nystagmus in strabismic macaque monkeys. Investig. Ophthalmol. Vis. Sci. 49:1872–78 [Google Scholar]
  104. Robinson FR, Fuchs AF. 2001. The role of the cerebellum in voluntary eye movements. Annu. Rev. Neurosci. 24:981–1004 [Google Scholar]
  105. Schoeff K, Chaudhuri Z, Demer JL. 2013. Functional magnetic resonance imaging of horizontal rectus muscles in esotropia. J. AAPOS 17:16–21 [Google Scholar]
  106. Scholl B, Tan AY, Priebe NJ. 2013. Strabismus disrupts binocular synaptic integration in primary visual cortex. J. Neurosci. 33:17108–22 [Google Scholar]
  107. Scott AB. 1981. Botulinum toxin injection of eye muscles to correct strabismus. Trans. Am. Ophthalmol. Soc. 79:734–70 [Google Scholar]
  108. Scott AB. 1994. Change of eye muscle sarcomeres according to eye position. J. Pediatr. Ophthalmol. Strabismus 31:85–88 [Google Scholar]
  109. Scott AB, Magoon EH, McNeer KW, Stager DR. 1990. Botulinum treatment of childhood strabismus. Ophthalmology 97:1434–38 [Google Scholar]
  110. Scott AB, Miller JM, Shieh KR. 2009. Treating strabismus by injecting the agonist muscle with bupivacaine and the antagonist with botulinum toxin. Trans. Am. Ophthalmol. Soc. 107:104–9 [Google Scholar]
  111. Scott AB, Rosenbaum A, Collins CC. 1973. Pharmacologic weakening of extraocular muscles. Investig. Ophthalmol. 12:924–27 [Google Scholar]
  112. Shan X, Hamasaki I, Tian J, Ying HS, Tamargo RJ, Zee DS. 2011. Vertical alignment in monkeys with unilateral IV section: effects of prolonged monocular patching and trigeminal deafferentation. Ann. N. Y. Acad. Sci. 1233:78–84 [Google Scholar]
  113. Shan X, Tian J, Ying HS, Quaia C, Optican LM. et al. 2007a. Acute superior oblique palsy in monkeys: I. Changes in static eye alignment. Investig. Ophthalmol. Vis. Sci. 48:2602–11 [Google Scholar]
  114. Shan X, Tian J, Ying HS, Walker MF, Guyton D. et al. 2008. The effect of acute superior oblique palsy on torsional optokinetic nystagmus in monkeys. Investig. Ophthalmol. Vis. Sci. 49:1421–28 [Google Scholar]
  115. Shan X, Ying HS, Tian J, Quaia C, Walker MF. et al. 2007b. Acute superior oblique palsy in monkeys: II. Changes in dynamic properties during vertical saccades. Investig. Ophthalmol. Vis. Sci. 48:2612–20 [Google Scholar]
  116. Simonsz HJ, Kolling GH. 2011. Best age for surgery for infantile esotropia. Eur. J. Paediatr. Neurol. 15:205–8 [Google Scholar]
  117. Smith EL 3rd, Bennett MJ, Harwerth RS, Crawford ML. 1979. Binocularity in kittens reared with optically induced squint. Science 204:875–77 [Google Scholar]
  118. Smith EL 3rd, Chino YM, Ni J, Cheng H, Crawford ML, Harwerth RS. 1997. Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. J. Neurophysiol. 78:1353–62 [Google Scholar]
  119. Steinbach MJ, Kirshner EL, Arstikaitis MJ. 1987. Recession versus marginal myotomy surgery for strabismus: effects on spatial localization. Investig. Ophthalmol. Vis. Sci. 28:1870–72 [Google Scholar]
  120. Steinbach MJ, Smith DR. 1981. Spatial localization after strabismus surgery: evidence for inflow. Science 213:1407–9 [Google Scholar]
  121. Steinbach MJ, Smith DR, Crawford JS. 1988. Egocentric localization changes following unilateral strabismus surgery. J. Pediatr. Ophthalmol. Strabismus 25:115–18 [Google Scholar]
  122. Takagi M, Tamargo R, Zee DS. 2003. Effects of lesions of the cerebellar oculomotor vermis on eye movements in primate: binocular control. Prog. Brain Res. 142:19–33 [Google Scholar]
  123. Takagi M, Zee DS, Tamargo RJ. 1998. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J. Neurophysiol. 80:1911–31 [Google Scholar]
  124. Takagi M, Zee DS, Tamargo RJ. 2000. Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J. Neurophysiol. 83:2047–62 [Google Scholar]
  125. Tian J, Shan X, Zee DS, Ying H, Tamargo RJ. et al. 2007. Acute superior oblique palsy in monkeys: III. Relationship to Listing's law. Investig. Ophthalmol. Vis. Sci. 48:2621–25 [Google Scholar]
  126. Tusa RJ, Mustari MJ, Burrows AF, Fuchs AF. 2001. Gaze-stabilizing deficits and latent nystagmus in monkeys with brief, early-onset visual deprivation: eye movement recordings. J. Neurophysiol. 86:651–61 [Google Scholar]
  127. Tusa RJ, Mustari MJ, Das VE, Boothe RG. 2002. Animal models for visual deprivation-induced strabismus and nystagmus. Ann. N. Y. Acad. Sci. 956:346–60 [Google Scholar]
  128. Tychsen L, Boothe RG. 1996. Latent fixation nystagmus and nasotemporal asymmetries of motion visually evoked potentials in naturally strabismic primate. J. Pediatr. Ophthalmol. Strabismus 33:148–52 [Google Scholar]
  129. Tychsen L, Burkhalter A. 1997. Nasotemporal asymmetries in V1: ocular dominance columns of infant, adult, and strabismic macaque monkeys. J. Comp. Neurol. 388:32–46 [Google Scholar]
  130. Tychsen L, Lisberger SG. 1986. Maldevelopment of visual motion processing in humans who had strabismus with onset in infancy. J. Neurosci. 6:2495–508 [Google Scholar]
  131. Tychsen L, Richards M, Wong A, Foeller P, Bradley D, Burkhalter A. 2010. The neural mechanism for latent (fusion maldevelopment) nystagmus. J. Neuroophthalmol. 30:276–83 [Google Scholar]
  132. Tychsen L, Richards M, Wong A, Foeller P, Burhkalter A. et al. 2008. Spectrum of infantile esotropia in primates: behavior, brains, and orbits. J. AAPOS 12:375–80 [Google Scholar]
  133. Tychsen L, Wong AM, Foeller P, Bradley D. 2004. Early versus delayed repair of infantile strabismus in macaque monkeys: II. Effects on motion visually evoked responses. Investig. Ophthalmol. Vis. Sci. 45:821–27 [Google Scholar]
  134. Tychsen L, Yildirim C, Anteby I, Boothe R, Burkhalter A. 2000. Macaque monkey as an ocular motor and neuroanatomic model of human infantile strabismus. Advances in Strabismus Research: Basic and Clinical Aspects, ed. G Lennerstrand, J Ygge 103–20 London: Portland Press [Google Scholar]
  135. Van Horn MR, Waitzman DM, Cullen KE. 2013. Vergence neurons identified in the rostral superior colliculus code smooth eye movements in 3D space. J. Neurosci. 33:7274–84 [Google Scholar]
  136. van Leeuwen AF, Collewijn H, de Faber JT, van der Steen J. 2001. Saccadic binocular coordination in alternating exotropia. Vis. Res. 41:3425–35 [Google Scholar]
  137. Versino M, Hurko O, Zee DS. 1996. Disorders of binocular control of eye movements in patients with cerebellar dysfunction. Brain 119:1933–50 [Google Scholar]
  138. von Noorden GK, Campos EC. 2002. Binocular Vision and Ocular Motility: Theory and Management of Strabismus St. Louis, MO: Mosby
  139. Walton MM, Mustari MJ. 2015. Abnormal tuning of saccade-related cells in pontine reticular formation of strabismic monkeys. J. Neurophysiol. 114:857–68 [Google Scholar]
  140. Walton MM, Mustari MJ, Willoughby CL, McLoon LK. 2015. Abnormal activity of neurons in abducens nucleus of strabismic monkeys. Investig. Ophthalmol. Vis. Sci. 56:10–19 [Google Scholar]
  141. Walton MM, Ono S, Mustari MJ. 2013. Stimulation of pontine reticular formation in monkeys with strabismus. Investig. Ophthalmol. Vis. Sci. 54:7125–36 [Google Scholar]
  142. Walton MM, Ono S, Mustari M. 2014. Vertical and oblique saccade disconjugacy in strabismus. Investig. Ophthalmol. Vis. Sci. 55:275–90 [Google Scholar]
  143. Wensveen JM, Smith EL 3rd, Hung LF, Harwerth RS. 2011. Brief daily periods of unrestricted vision preserve stereopsis in strabismus. Investig. Ophthalmol. Vis. Sci. 52:4872–79 [Google Scholar]
  144. Wiesel TN, Hubel DH. 1965. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28:1029–40 [Google Scholar]
  145. Williams AS, Hoyt CS. 1989. Acute comitant esotropia in children with brain tumors. Arch. Ophthalmol. 107:376–78 [Google Scholar]
  146. Willoughby CL, Christiansen SP, Mustari MJ, McLoon LK. 2012. Effects of the sustained release of IGF-1 on extraocular muscle of the infant non-human primate: adaptations at the effector organ level. Investig. Ophthalmol. Vis. Sci. 53:68–75 [Google Scholar]
  147. Willoughby CL, Fleuriet J, Walton MM, Mustari MJ, McLoon LK. 2015. Adaptability of the immature ocular motor control system: unilateral IGF-1 medial rectus treatment. Investig. Ophthalmol. Vis. Sci. 56:3484–96 [Google Scholar]
  148. Wong AM, Foeller P, Bradley D, Burkhalter A, Tychsen L. 2003. Early versus delayed repair of infantile strabismus in macaque monkeys: I. Ocular motor effects. J. AAPOS 7:200–9 [Google Scholar]
  149. Zhang B, Bi H, Sakai E, Maruko I, Zheng J. et al. 2005. Rapid plasticity of binocular connections in developing monkey visual cortex (V1). PNAS 102:9026–31 [Google Scholar]
  150. Zhang H, Gamlin P. 1996. Single unit activity within the posterior fastigial nucleus during vergence and accommodation in the alert primate Presented at Annu. Meet. Soc. Neurosci., Washington, DC
  151. Zhang H, Gamlin PD. 1998. Neurons in the posterior interposed nucleus of the cerebellum related to vergence and accommodation. I. Steady-state characteristics. J. Neurophysiol. 79:1255–69 [Google Scholar]
  152. Zhang Y, Mays LE, Gamlin PD. 1992. Characteristics of near response cells projecting to the oculomotor nucleus. J. Neurophysiol. 67:944–60 [Google Scholar]
  153. Zhou W, King WM. 1998. Premotor commands encode monocular eye movements. Nature 393:692–95 [Google Scholar]
/content/journals/10.1146/annurev-vision-111815-114335
Loading
/content/journals/10.1146/annurev-vision-111815-114335
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error