Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Eye movements in patients with neurodegenerative disorders

Nature Reviews Neurology volume 9, pages 74–85 (2013)Cite this article

Subjects

Abstract

The neural pathways and brain regions involved in eye movements during ocular fixation and gaze control include the cerebrum, brainstem and cerebellum, and abnormal eye movements can indicate the presence of neurodegeneration. In some patients, oculomotor signs are key to making a diagnosis. Careful clinical examination of eye movements in patients with neurodegenerative disorders is, therefore, an invaluable adjunct to neurological and cognitive assessments. Eye movement recordings in the laboratory are generally not necessary for diagnostic purposes, but can be a useful addition to the clinical examination. Laboratory recordings of eye movements can provide valuable information about disease severity, progression or regression in neurodegenerative disease, and hold particular promise for objective evaluation of the efficacy of putative neuroprotective and neurorestorative therapies. For example, aspects of saccade performance can be tested to probe both motor and cognitive aspects of oculomotor behaviour. This Review describes the oculomotor features of the major age-related movement disorders, including Parkinson disease, Huntington disease, dementia and other neurodegenerative disorders. Findings in presymptomatic individuals and changes associated with disease progression are discussed.

Key Points

  • Careful clinical examination of eye movements is a useful adjunct in the diagnosis of many neurodegenerative disorders; laboratory eye movement recordings do not usually provide diagnostic clues

  • Different saccadic paradigms and laboratory recordings precisely reflect cognitive and motor characteristics of neurodegenerative disorders and may be useful biomarkers of disease severity and progression, especially in dementia

  • Clinical oculomotor examination in Parkinson disease indicates subtle saccadic hypometria and mildly impaired smooth pursuit, whereas laboratory recordings show voluntary saccadic abnormalities that correlate with cognitive status

  • Atypical parkinsonian disorders are associated with distinctive features: slowed saccades in progressive supranuclear palsy, positional and head-shaking downbeat nystagmus in multiple system atrophy, and saccadic apraxia in corticobasal syndrome

  • Specific oculomotor hallmarks that aid diagnosis in spinocerebellar ataxia (SCA) are very slowed saccades in SCA2 and SCA7, positional downbeat nystagmus in SCA6, and hypoactive vestibulo-ocular reflex in Friedreich ataxia

  • Future work is needed to explore the robustness and repeatability of laboratory eye movement recordings in healthy controls and disease states

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Variation in the extent of motor and cognitive impairment and the role of eye movement assessments in age-related neurodegenerative disorders.
Figure 2: Task-specific saccade hypometria in a patient with Parkinson disease.
Figure 3: Patterns of eye movement abnormalities in parkinsonian disorders.
Figure 4: Horizontal saccade abnormalities in a patient with spinocerebellar ataxia type 2.

Similar content being viewed by others

References

  1. Bridgeman, B. Conscious vs unconscious processes: the case of vision. Theory Psychology 2, 73–88 (1992).

    Article  Google Scholar 

  2. Deubel, H. & Schneider, W. X. Delayed saccades, but not delayed manual aiming movements, require visual attention shifts. Ann. NY Acad. Sci. 1004, 289–296 (2003).

    Article  PubMed  Google Scholar 

  3. Aarsland, D. in Cognitive Impairment and Dementia in Parkinson's Disease (ed. Emre, M.) 5–14 (Oxford University Press, Oxford, 2010).

  4. Anderson, T. et al. Oculomotor function in multiple system atrophy: clinical and laboratory features in 30 patients. Mov. Disord. 23, 977–984 (2008).

    Article  PubMed  Google Scholar 

  5. Chen, A. L. et al. The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis. Front. Neurol. 1, 147 (2010).

    PubMed  PubMed Central  Google Scholar 

  6. Hellmuth, J. et al. Multicenter validation of a bedside antisaccade task as a measure of executive function. Neurology 78, 1824–1831 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Garbutt, S. et al. Oculomotor function in frontotemporal lobar degeneration, related disorders and Alzheimer's disease. Brain 131, 1268–1281 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Tabrizi, S. J. et al. Biological and clinical manifestations of Huntington's disease in the longitudinal TRACK-HD study: cross-sectional analysis of baseline data. Lancet Neurol. 8, 791–801 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Tabrizi, S. J. et al. Potential endpoints for clinical trials in premanifest and early Huntington's disease in the TRACK-HD study: analysis of 24 month observational data. Lancet Neurol. 11, 42–53 (2012).

    Article  PubMed  Google Scholar 

  10. Tabrizi, S. J. et al. Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. Lancet Neurol. 10, 31–42 (2011).

    Article  PubMed  Google Scholar 

  11. Munoz, D. P., Dorris, M. C., Pare, M. & Everling, S. On your mark, get set: brainstem circuitry underlying saccadic initiation. Can. J. Physiol. Pharmacol. 78, 934–944 (2000).

    Article  CAS  PubMed  Google Scholar 

  12. Deubel, H. in Attention and Performance XVII: Cognitive Regulation of Performance (eds Gopher, D. & Koriat, A.) 697–721 (MIT Press, Cambridge, MA, 1999).

    Google Scholar 

  13. Liu, P. & Basso, M. A. Substantia nigra stimulation influences monkey superior colliculus neuronal activity bilaterally. J. Neurophysiol. 100, 1098–1112 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Terao, Y. et al. Initiation and inhibitory control of saccades with the progression of Parkinson's disease—changes in three major drives converging on the superior colliculus. Neuropsychologia 49, 1794–1806 (2011).

    Article  PubMed  Google Scholar 

  15. MacAskill, M. R. et al. The influence of motor and cognitive impairment upon visually-guided saccades in Parkinson's disease. Neuropsychologia 50, 3338–3347 (2012).

    Article  PubMed  Google Scholar 

  16. Bronstein, A. M. & Kennard, C. Predictive ocular motor control in Parkinson's disease. Brain 108, 925–940 (1985).

    Article  PubMed  Google Scholar 

  17. Crawford, T. J., Goodrich, S., Henderson, L. & Kennard, C. Predictive responses in Parkinson's disease: manual keypresses and saccadic eye movements to regular stimulus events. J. Neurol. Neurosurg. Psychiatry 52, 1033–1042 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ventre, J., Zee, D. S., Papageorgiou, H. & Reich, S. Abnormalities of predictive saccades in hemi-Parkinson's disease. Brain 115, 1147–1165 (1992).

    Article  PubMed  Google Scholar 

  19. O'Sullivan, S. S. et al. Clinical outcomes of progressive supranuclear palsy and multiple system atrophy. Brain 131, 1362–1372 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Chambers, J. M. & Prescott, T. J. Response times for visually guided saccades in persons with Parkinson's disease: a meta-analytic review. Neuropsychologia 48, 887–899 (2010).

    Article  PubMed  Google Scholar 

  21. Mosimann, U. P. et al. Saccadic eye movement changes in Parkinson's disease dementia and dementia with Lewy bodies. Brain 128, 1267–1276 (2005).

    Article  PubMed  Google Scholar 

  22. Matsumoto, H. et al. Small saccades restrict visual scanning area in Parkinson's disease. Mov. Disord. 26, 1619–1626 (2011).

    Article  PubMed  Google Scholar 

  23. Clark, U. S., Neargarder, S. & Cronin-Golomb, A. Visual exploration of emotional facial expressions in Parkinson's disease. Neuropsychologia 48, 1901–1913 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Anastasopoulos, D., Ziavra, N., Savvidou, E., Bain, P. & Bronstein, A. M. Altered eye-to-foot coordination in standing parkinsonian patients during large gaze and whole-body reorientations. Mov. Disord. 26, 2201–2211 (2011).

    Article  PubMed  Google Scholar 

  25. Carpenter, M. G. & Bloem, B. R. A new twist on turning movements in Parkinson's disease patients. Mov. Disord. 26, 2151–2153 (2011).

    Article  PubMed  Google Scholar 

  26. Lohnes, C. A. & Earhart, G. M. Saccadic eye movements are related to turning performance in Parkinson disease. J. Parkinsons Dis. 1, 109–118 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hely, M. A., Reid, W. G., Adena, M. A., Halliday, G. M. & Morris, J. G. The Sydney multicenter study of Parkinson's disease: the inevitability of dementia at 20 years. Mov. Disord. 23, 837–844 (2008).

    Article  PubMed  Google Scholar 

  28. Pinkhardt, E. H. et al. Eye movement impairments in Parkinson's disease: possible role of extradopaminergic mechanisms. BMC Neurol. 12, 5 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  29. van Stockum, S., MacAskill, M. R., Anderson, T. J. & Dalrymple-Alford, J. C. Don't look now or look away: two sources of saccadic disinhibition in Parkinson's disease? Neuropsychologia 46, 3108–3115 (2008).

    Article  PubMed  Google Scholar 

  30. Perneczky, R. et al. Saccadic latency in Parkinson's disease correlates with executive function and brain atrophy, but not motor severity. Neurobiol. Dis. 43, 79–85 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Nakashima, H. et al. An autopsied case of dementia with Lewy bodies with supranuclear gaze palsy. Neurol. Res. 25, 533–537 (2003).

    Article  PubMed  Google Scholar 

  32. Kapoula, Z. et al. Spread deficits in initiation, speed and accuracy of horizontal and vertical automatic saccades in dementia with lewy bodies. Front. Neurol. 1, 138 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Gilman, S. et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71, 670–676 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rascol, O. et al. Square wave jerks in parkinsonian syndromes. J. Neurol. Neurosurg. Psychiatry 54, 599–602 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Linder, J., Wenngren, B. I., Stenlund, H. & Forsgren, L. Impaired oculomotor function in a community-based patient population with newly diagnosed idiopathic parkinsonism. J. Neurol. 259, 1206–1214 (2012).

    Article  PubMed  Google Scholar 

  36. Rascol, O. et al. Abnormal ocular movements in Parkinson's disease. Evidence for involvement of dopaminergic systems. Brain 112, 1193–1214 (1989).

    Article  PubMed  Google Scholar 

  37. Stell, R. & Bronstein, A. M. in Movement Disorders 3 (eds Marsden, C. D. & Fahn, S.) 88–113 (Butterworth-Heinemann Ltd, Oxford, 1994).

  38. Arpa, J. et al. Electro-oculogram in multiple system and late onset cerebellar atrophies. Rev. Neurol. 23, 969–974 (1995).

    CAS  PubMed  Google Scholar 

  39. Rascol, O. J., Clanet, M., Senard, J. M., Montastruc, J. L. & Rascol, A. Vestibulo-ocular reflex in Parkinson's disease and multiple system atrophy. Adv. Neurol. 60, 395–397 (1993).

    CAS  PubMed  Google Scholar 

  40. Lee, J. Y. et al. Perverted head-shaking and positional downbeat nystagmus in patients with multiple system atrophy. Mov. Disord. 24, 1290–1295 (2009).

    Article  PubMed  Google Scholar 

  41. Williams, D. R. et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. Brain 128, 1247–1258 (2005).

    Article  PubMed  Google Scholar 

  42. Williams, D. R., Holton, J. L., Strand, K., Revesz, T. & Lees, A. J. Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov. Disord. 22, 2235–2241 (2007).

    Article  PubMed  Google Scholar 

  43. Williams, D. R. & Lees, A. J. Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol. 8, 270–279 (2009).

    Article  PubMed  Google Scholar 

  44. Troost, B. T. & Daroff, R. B. The ocular motor defects in progressive supranuclear palsy. Ann. Neurol. 2, 397–403 (1977).

    Article  CAS  PubMed  Google Scholar 

  45. Bhidayasiri, R. et al. Pathophysiology of slow vertical saccades in progressive supranuclear palsy. Neurology 57, 2070–2077 (2001).

    Article  CAS  PubMed  Google Scholar 

  46. Vidailhet, M. et al. Eye movements in parkinsonian syndromes. Ann. Neurol. 35, 420–426 (1994).

    Article  CAS  PubMed  Google Scholar 

  47. Rivaud-Pechoux, S. et al. Longitudinal ocular motor study in corticobasal degeneration and progressive supranuclear palsy. Neurology 54, 1029–1032 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. Boxer, A. L. et al. Saccade abnormalities in autopsy-confirmed frontotemporal lobar degeneration and Alzheimer disease. Arch. Neurol. 69, 509–517 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Litvan, I. et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47, 1–9 (1996).

    Article  CAS  PubMed  Google Scholar 

  50. Garbutt, S. et al. Abnormalities of optokinetic nystagmus in progressive supranuclear palsy. J. Neurol. Neurosurg. Psychiatry 75, 1386–1394 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Steele, J. C. Progressive supranuclear palsy. Brain 95, 693–704 (1972).

    CAS  PubMed  Google Scholar 

  52. Altiparmak, U. E., Eggenberger, E., Coleman, A. & Condon, K. The ratio of square wave jerk rates to blink rates distinguishes progressive supranuclear palsy from Parkinson disease. J. Neuroophthalmol. 26, 257–259 (2006).

    Article  PubMed  Google Scholar 

  53. Rivaud-Pechoux, S., Vidailhet, M., Brandel, J. P. & Gaymard, B. Mixing pro- and antisaccades in patients with parkinsonian syndromes. Brain 130, 256–264 (2007).

    Article  CAS  PubMed  Google Scholar 

  54. Vidailhet, M. et al. Saccades and antisaccades in parkinsonian syndromes. Adv. Neurol. 80, 377–382 (1999).

    CAS  PubMed  Google Scholar 

  55. Wadia, P. M. & Lang, A. E. The many faces of corticobasal degeneration. Parkinsonism Relat. Disord. 13 (Suppl. 3), S336–S340 (2007).

    Article  PubMed  Google Scholar 

  56. Ling, H. et al. Does corticobasal degeneration exist? A clinicopathological re-evaluation. Brain 133, 2045–2057 (2010).

    Article  PubMed  Google Scholar 

  57. Vidailhet, M. & Rivaud-Pechoux, S. Eye movement disorders in corticobasal degeneration. Adv. Neurol. 82, 161–167 (2000).

    CAS  PubMed  Google Scholar 

  58. Rottach, K. G., Riley, D. E., DiScenna, A. O., Zivotofsky, A. Z. & Leigh, R. J. Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes. Ann. Neurol. 39, 368–377 (1996).

    Article  CAS  PubMed  Google Scholar 

  59. Murray, R. et al. Cognitive and motor assessment in autopsy-proven corticobasal degeneration. Neurology 68, 1274–1283 (2007).

    Article  CAS  PubMed  Google Scholar 

  60. Lasker, A. G., Zee, D. S., Hain, T. C., Folstein, S. E. & Singer, H. S. Saccades in Huntington's disease: slowing and dysmetria. Neurology 38, 427–431 (1988).

    Article  CAS  PubMed  Google Scholar 

  61. Lasker, A. G. & Zee, D. S. Ocular motor abnormalities in Huntington's disease. Vision Res. 37, 3639–3645 (1997).

    Article  CAS  PubMed  Google Scholar 

  62. Peltsch, A., Hoffman, A., Armstrong, I., Pari, G. & Munoz, D. P. Saccadic impairments in Huntington's disease. Exp. Brain Res. 186, 457–469 (2008).

    Article  CAS  PubMed  Google Scholar 

  63. Golding, C. V., Danchaivijitr, C., Hodgson, T. L., Tabrizi, S. J. & Kennard, C. Identification of an oculomotor biomarker of preclinical Huntington disease. Neurology 67, 485–487 (2006).

    Article  CAS  PubMed  Google Scholar 

  64. Rupp, J. et al. Comparison of vertical and horizontal saccade measures and their relation to gray matter changes in premanifest and manifest Huntington disease. J. Neurol. 259, 267–276 (2012).

    Article  PubMed  Google Scholar 

  65. Winograd-Gurvich, C. T. et al. Hypometric primary saccades and increased variability in visually-guided saccades in Huntington's disease. Neuropsychologia 41, 1683–1692 (2003).

    Article  CAS  PubMed  Google Scholar 

  66. Leigh, R. J., Newman, S. A., Folstein, S. E., Lasker, A. G. & Jensen, B. A. Abnormal ocular motor control in Huntington's disease. Neurology 33, 1268–1275 (1983).

    Article  CAS  PubMed  Google Scholar 

  67. Blekher, T. et al. Saccades in presymptomatic and early stages of Huntington disease. Neurology 67, 394–399 (2006).

    Article  CAS  PubMed  Google Scholar 

  68. Patel, S. S., Jankovic, J., Hood, A. J., Jeter, C. B. & Sereno, A. B. Reflexive and volitional saccades: biomarkers of Huntington disease severity and progression. J. Neurol. Sci. 313, 35–41 (2012).

    Article  PubMed  Google Scholar 

  69. Henderson, T. et al. Inhibitory control during smooth pursuit in Parkinson's disease and Huntington's disease. Mov. Disord. 26, 1893–1899 (2011).

    Article  PubMed  Google Scholar 

  70. Turner, T. H. et al. Behavioral measures of saccade latency and inhibition in manifest and premanifest Huntington's disease. J. Mot. Behav. 43, 295–302 (2011).

    Article  PubMed  Google Scholar 

  71. Hicks, S. L., Robert, M. P., Golding, C. V., Tabrizi, S. J. & Kennard, C. Oculomotor deficits indicate the progression of Huntington's disease. Prog. Brain Res. 171, 555–558 (2008).

    Article  PubMed  Google Scholar 

  72. Rupp, J. et al. Progression in prediagnostic Huntington disease. J. Neurol. Neurosurg. Psychiatry 81, 379–384 (2010).

    Article  PubMed  Google Scholar 

  73. Rupp, J. et al. Abnormal error-related antisaccade activation in premanifest and early manifest Huntington disease. Neuropsychology 25, 306–318 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Antoniades, C. A., Xu, Z., Mason, S. L., Carpenter, R. H. & Barker, R. A. Huntington's disease: changes in saccades and hand-tapping over 3 years. J. Neurol. 257, 1890–1898 (2010).

    Article  CAS  PubMed  Google Scholar 

  75. Josephs, K. A. Frontotemporal dementia and related disorders: deciphering the enigma. Ann. Neurol. 64, 4–14 (2008).

    Article  CAS  PubMed  Google Scholar 

  76. Burrell, J. R., Hornberger, M., Carpenter, R. H., Kiernan, M. C. & Hodges, J. R. Saccadic abnormalities in frontotemporal dementia. Neurology 78, 1816–1823 (2012).

    Article  CAS  PubMed  Google Scholar 

  77. Currie, J., Ramsden, B., McArthur, C. & Maruff, P. Validation of a clinical antisaccadic eye movement test in the assessment of dementia. Arch. Neurol. 48, 644–648 (1991).

    Article  CAS  PubMed  Google Scholar 

  78. Abel, L. A., Unverzagt, F. & Yee, R. D. Effects of stimulus predictability and interstimulus gap on saccades in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 13, 235–243 (2002).

    Article  PubMed  Google Scholar 

  79. Boxer, A. L. et al. Medial versus lateral frontal lobe contributions to voluntary saccade control as revealed by the study of patients with frontal lobe degeneration. J. Neurosci. 26, 6354–6363 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Crawford, T. J. et al. Inhibitory control of saccadic eye movements and cognitive impairment in Alzheimer's disease. Biol. Psychiatry 57, 1052–1060 (2005).

    Article  PubMed  Google Scholar 

  81. Shafiq-Antonacci, R., Maruff, P., Masters, C. & Currie, J. Spectrum of saccade system function in Alzheimer disease. Arch. Neurol. 60, 1272–1278 (2003).

    Article  PubMed  Google Scholar 

  82. Fletcher, W. A. & Sharpe, J. A. Saccadic eye movement dysfunction in Alzheimer's disease. Ann. Neurol. 20, 464–741 (1986).

    Article  CAS  PubMed  Google Scholar 

  83. Yang, Q., Wang, T., Su, N., Xiao, S. & Kapoula, Z. Specific saccade deficits in patients with Alzheimer's disease at mild to moderate stage and in patients with amnestic mild cognitive impairment. Age (Dordr.) http://dx.doi.org/10.1007/s11357-012-9420-z.

  84. Yang, Q. et al. Long latency and high variability in accuracy-speed of prosaccades in Alzheimer's disease at mild to moderate stage. Dement. Geriatr. Cogn. Dis. Extra 1, 318–329 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Schewe, H. J., Uebelhack, R. & Vohs, K. Abnormality in saccadic eye movement in dementia. Eur. Psychiatry 14, 52–53 (1999).

    Article  CAS  PubMed  Google Scholar 

  86. Donaghy, C. et al. Slow saccades in bulbar-onset motor neurone disease. J. Neurol. 257, 1134–1140 (2010).

    Article  PubMed  Google Scholar 

  87. Donaghy, C., Thurtell, M. J., Pioro, E. P., Gibson, J. M. & Leigh, R. J. Eye movements in amyotrophic lateral sclerosis and its mimics: a review with illustrative cases. J. Neurol. Neurosurg. Psychiatry 82, 110–116 (2011).

    Article  PubMed  Google Scholar 

  88. Ohki, M. et al. Ocular abnormalities in amyotrophic lateral sclerosis. Acta Otolaryngol. Suppl. 511, 138–142 (1994).

    Article  CAS  PubMed  Google Scholar 

  89. Averbuch-Heller, L., Helmchen, C., Horn, A. K., Leigh, R. J. & Buttner-Ennerver, J. A. Slow vertical saccades in motor neuron disease: correlation of structure and function. Ann. Neurol. 44, 641–648 (1998).

    Article  CAS  PubMed  Google Scholar 

  90. Leveille, A., Kiernan, J., Goodwin, J. A. & Antel, J. Eye movements in amyotrophic lateral sclerosis. Arch. Neurol. 39, 684–686 (1982).

    Article  CAS  PubMed  Google Scholar 

  91. McCluskey, L. F. et al. Amyotrophic lateral sclerosis-plus syndrome with TAR DNA-binding protein-43 pathology. Arch. Neurol. 66, 121–124 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Shaunak, S. et al. Oculomotor function in amyotrophic lateral sclerosis: evidence for frontal impairment. Ann. Neurol. 38, 38–44 (1995).

    Article  CAS  PubMed  Google Scholar 

  93. Donaghy, C. et al. Ocular fixation instabilities in motor neurone disease. A marker of frontal lobe dysfunction? J. Neurol. 256, 420–426 (2009).

    Article  CAS  PubMed  Google Scholar 

  94. Orr, H. T. & Zoghbi, H. Y. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30, 575–621 (2007).

    Article  CAS  PubMed  Google Scholar 

  95. Yabe, I. et al. Positional vertigo and macroscopic downbeat positioning nystagmus in spinocerebellar ataxia type 6 (SCA6). J. Neurol. 250, 440–443 (2003).

    Article  PubMed  Google Scholar 

  96. Gomez, C. M. et al. Spinocerebellar ataxia type 6: gaze-evoked and vertical nystagmus, Purkinje cell degeneration, and variable age of onset. Ann. Neurol. 42, 933–950 (1997).

    Article  CAS  PubMed  Google Scholar 

  97. Buttner, N. et al. Oculomotor phenotypes in autosomal dominant ataxias. Arch. Neurol. 55, 1353–1357 (1998).

    Article  CAS  PubMed  Google Scholar 

  98. Bour, L. J., van Rootselaar, A. F., Koelman, J. H. & Tijssen, M. A. Oculomotor abnormalities in myoclonic tremor: a comparison with spinocerebellar ataxia type 6. Brain 131, 2295–2303 (2008).

    Article  CAS  PubMed  Google Scholar 

  99. Marelli, C. et al. SCA15 due to large ITPR1 deletions in a cohort of 333 white families with dominant ataxia. Arch. Neurol. 68, 637–643 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Velazquez-Perez, L. et al. Saccade velocity is controlled by polyglutamine size in spinocerebellar ataxia 2. Ann. Neurol. 56, 444–447 (2004).

    Article  PubMed  Google Scholar 

  101. Wadia, N. et al. A clinicogenetic analysis of six Indian spinocerebellar ataxia (SCA2) pedigrees. The significance of slow saccades in diagnosis. Brain 121, 2341–2355 (1998).

    Article  PubMed  Google Scholar 

  102. Geiner, S., Horn, A. K., Wadia, N. H., Sakai, H. & Buttner-Ennever, J. A. The neuroanatomical basis of slow saccades in spinocerebellar ataxia type 2 (Wadia-subtype). Prog. Brain Res. 171, 575–581 (2008).

    Article  CAS  PubMed  Google Scholar 

  103. Fahey, M. C. et al. Vestibular, saccadic and fixation abnormalities in genetically confirmed Friedreich ataxia. Brain 131, 1035–1045 (2008).

    Article  PubMed  Google Scholar 

  104. Burk, K. et al. Autosomal dominant cerebellar ataxia type I: oculomotor abnormalities in families with SCA1, SCA2, and SCA3. J. Neurol. 246, 789–797 (1999).

    Article  CAS  PubMed  Google Scholar 

  105. Hubner, J. et al. Eye movement abnormalities in spinocerebellar ataxia type 17 (SCA17). Neurology 69, 1160–1168 (2007).

    Article  CAS  PubMed  Google Scholar 

  106. Enevoldson, T. P., Sanders, M. D. & Harding, A. E. Autosomal dominant cerebellar ataxia with pigmentary macular dystrophy. A clinical and genetic study of eight families. Brain 117, 445–460 (1994).

    Article  PubMed  Google Scholar 

  107. Oh, A. K., Jacobson, K. M., Jen, J. C. & Baloh, R. W. Slowing of voluntary and involuntary saccades: an early sign in spinocerebellar ataxia type 7. Ann. Neurol. 49, 801–804 (2001).

    Article  CAS  PubMed  Google Scholar 

  108. Thurtell, M. J. et al. Two patients with spinocerebellar ataxia type 7 presenting with profound binocular visual loss yet minimal ophthalmoscopic findings. J. Neuroophthalmol. 29, 187–191 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Velazquez-Perez, L. et al. Saccade velocity is reduced in presymptomatic spinocerebellar ataxia type 2. Clin. Neurophysiol. 120, 632–635 (2009).

    Article  CAS  PubMed  Google Scholar 

  110. Iacono, W. G. & Lykken, D. T. Two-year retest stability of eye tracking performance and a comparison of electro-oculographic and infrared recording techniques: evidence of EEG in the electro-oculogram. Psychophysiology 18, 49–55 (1981).

    Article  CAS  PubMed  Google Scholar 

  111. Roy-Byrne, P., Radant, A., Wingerson, D. & Cowley, D. S. Human oculomotor function: reliability and diurnal variation. Biol. Psychiatry 38, 92–97 (1995).

    Article  CAS  PubMed  Google Scholar 

  112. Blekher, T. et al. Test-retest reliability of saccadic measures in subjects at risk for Huntington disease. Invest. Ophthalmol. Vis. Sci. 50, 5707–5711 (2009).

    Article  PubMed  Google Scholar 

  113. Rivaud-Péchoux, S. et al. Improvement of memory guided saccades in parkinsonian patients by high frequency subthalamic nucleus stimulation. J. Neurol. Neurosurg. Psychiatry 68, 381–384 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Sauleau, P. et al. Subthalamic stimulation improves orienting gaze movements in Parkinson's disease. Clin. Neurophysiol. 119, 1857–1863 (2008).

    Article  PubMed  Google Scholar 

  115. Temel, Y., Visser-Vandewalle, V. & Carpenter, R. H. Saccadometry: a novel clinical tool for quantification of the motor effects of subthalamic nucleus stimulation in Parkinson's disease. Exp. Neurol. 216, 481–489 (2009).

    Article  PubMed  Google Scholar 

  116. Temel, Y., Visser-Vandewalle, V. & Carpenter, C. Saccadic latency during electrical stimulation of the human subthalamic nucleus. Curr. Biol. 18, R412–R414 (2008).

    Article  CAS  PubMed  Google Scholar 

  117. Pinkhardt, E. H. & Kassubek, J. Ocular motor abnormalities in Parkinsonian syndromes. Parkinsonism Relat. Disord. 17, 223–230 (2011).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine, University of Otago Christchurch, 2 Riccarton Avenue, Christchurch, 8011, New Zealand

    Tim J. Anderson

  2. New Zealand Brain Research Institute, 66 Stewart Street, Christchurch, 8011, New Zealand

    Michael R. MacAskill

Authors
  1. Tim J. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael R. MacAskill
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T. J. Anderson and M. R. MacAskill contributed equally to researching data for the article, discussion of the content, writing the article, and to review and/or editing of the manuscript before submission.

Corresponding author

Correspondence to Tim J. Anderson.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anderson, T., MacAskill, M. Eye movements in patients with neurodegenerative disorders. Nat Rev Neurol 9, 74–85 (2013). https://doi.org/10.1038/nrneurol.2012.273

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrneurol.2012.273

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing