Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-669899f699-7xsfk Total loading time: 0 Render date: 2025-05-05T01:56:27.592Z Has data issue: false hasContentIssue false

Chapter 11 - Oculomotor and Visual-Vestibular Disturbances in Parkinson’s Disease

Published online by Cambridge University Press:  05 March 2022

By
Adolfo M. Bronstein ,
Tim Anderson ,
Diego Kaski ,
Michael MacAskill  and
Aasef Shaikh
Edited by
Néstor Gálvez-Jiménez ,
Amos D. Korczyn  and
Ramón Lugo-Sanchez
Néstor Gálvez-Jiménez
Affiliation:
Florida International University
Amos D. Korczyn
Affiliation:
Tel-Aviv University
Ramón Lugo-Sanchez
Affiliation:
Cleveland Clinic
Get access

Summary

In this chapter we will describe how Parkinson’s disease (PD) affects patients’ eye movements, both bedside and laboratory, preceded by brief review of the anatomo-physiological substrate of eye movements. We will provide a practical summary of how to use the eye movement examination to aid the differential diagnosis of the parkinsonian syndromes, in particular idiopathic PD from multiple system atrophy (MSA), progressive supranuclear palsy (PSP), and corticobasal syndrome (CBS). A sub-section will describe how deep brain stimulation (DBS) also influences eye movements in PD. Despite a plethora of eye movement laboratory studies in PD it is still relatively unknown what the eye movements of these patients are like in real life. Given that the eyes move in order to see better, does the akinesia of PD impose visual deprivation or delays during ecological whole-body movements?.

Type
Chapter
Information
Non-motor Parkinson's Disease , pp. 115 - 129
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Book purchase

Temporarily unavailable

References

Leigh, RJ, Zee, DS. The Neurology of Eye Movements, 5th Ed. Oxford University Press; 2015, xx, 1109.Google Scholar
Hikosaka, O, Takikawa, Y, Kawagoe, R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 2000; 80(3): 953–978.Google Scholar
Terao, Y, Fukuda, H, Ugawa, Y, Hikosaka, O. New perspectives on the pathophysiology of Parkinson’s disease as assessed by saccade performance: a clinical review. Clin Neurophysiol 2013; 124(8): 1491–1506.Google Scholar
Buttner, U, Buttner-Ennever, JA. Present concepts of oculomotor organization. Prog Brain Res 2006; 151: 1–42.Google Scholar
Hellmuth, J, Mirsky, J, Heuer, HW, et al. Multicenter validation of a bedside antisaccade task as a measure of executive function. Neurology 2012; 78(23): 1824–1831.CrossRefGoogle ScholarPubMed
Schindlbeck, KA, Schonfeld, S, Naumann, W, et al. Characterization of diplopia in non-demented patients with Parkinson’s disease. Parkinsonism Relat Disord 2017; 45: 1–6.Google Scholar
Corin, MS, Elizan, TS, Bender, MB. Oculomotor function in patients with Parkinson’s disease. J Neurol Sci 1972/3; 15(3): 251–265.Google Scholar
Weil, RS, Schrag, AE, Warren, JD, et al. Visual dysfunction in Parkinson’s disease. Brain 2016; 139(11): 2827–2843.Google Scholar
DeJong, JD, Jones, GM. Akinesia, hypokinesia, and bradykinesia in the oculomotor system of patients with Parkinson’s disease. Exp Neurol 1971; 32(1): 58–68.CrossRefGoogle ScholarPubMed
Walker, R, Walker, DG, Husain, M, Kennard, C. Control of voluntary and reflexive saccades. Exp Brain Res 2000; 130(4): 540–544.Google Scholar
Mosimann, UP, Müri, RM, Burn, DJ, et al. Saccadic eye movement changes in Parkinson’s disease dementia and dementia with Lewy bodies. Brain 2005; 128: 1267–1276.CrossRefGoogle ScholarPubMed
Macaskill, MR, Graham, CF, Pitcher, TL, et al. The influence of motor and cognitive impairment upon visually guided saccades in Parkinson’s disease. Neuropsychologia 2012; 50(14): 3338–3347.Google Scholar
Terao, Y, Fukuda, H, Yugeta, A, 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 2011; 49(7): 1794–1806.CrossRefGoogle ScholarPubMed
Anderson, TJ, MacAskill, MR. Eye movements in patients with neurodegenerative disorders. Nat Rev Neurol 2013; 9(2): 74–85.Google Scholar
Stuart, S, Lawson, RA, Yarnall, AJ, et al. Pro-saccades predict cognitive decline in Parkinson’s disease: ICICLE-PD. Mov Disord 2019; 34(11): 1690–1698.CrossRefGoogle ScholarPubMed
Chan, F, Armstrong, IT, Pari, G, et al. Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 2005; 43(5): 784–796.CrossRefGoogle ScholarPubMed
Pinkhardt, EH, Jurgens, R, Becker, W, et al. Differential diagnostic value of eye movement recording in PSP-parkinsonism, Richardson’s syndrome, and idiopathic Parkinson’s disease. J Neurol 2008; 255(12): 1916–1925.Google Scholar
Pinkhardt, EH, Kassubek, J. Ocular motor abnormalities in Parkinsonian syndromes. Parkinsonism Relat Disord 2011; 17(4): 223–230.Google Scholar
Nakashima, H, Terada, S, Ishizu, H, et al. An autopsied case of dementia with Lewy bodies with supranuclear gaze palsy. Neurol Res 2003; 25(5): 533–537.CrossRefGoogle ScholarPubMed
Grotzsch, H, Sztajzel, R, Burkhard, PR. Levodopa-induced ocular dyskinesia in Parkinson’s disease. Eur J Neurol 2007; 14(10): 1124–1128.Google Scholar
Racette, BA, Gokden, MS, Tychsen, LS, Perlmutter, JS. Convergence insufficiency in idiopathic Parkinson’s disease responsive to levodopa. Strabismus 1999; 7(3): 169–174.Google Scholar
Sharpe, JA, Fletcher, WA, Lang, AE, Zackon, DH. Smooth pursuit during dose-related on-off fluctuations in Parkinson’s disease. Neurology 1987; 37(8): 1389–1392.Google Scholar
Gilman, S, Wenning, GK, Low, PA, et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 2008; 71(9): 670–676.CrossRefGoogle ScholarPubMed
Anderson, T, Luxon, L, Quinn, N, et al. Oculomotor function in multiple system atrophy: clinical and laboratory features in 30 patients. Mov Disord 2008; 23(7): 977–984.Google Scholar
Lee, JY, Lee, WW, Kim, JS, et al. Perverted head-shaking and positional downbeat nystagmus in patients with multiple system atrophy. Mov Disord 2009; 24(9): 1290–1295.Google Scholar
Chen, AL, Riley, DE, King, SA, et al. The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis. Front Neurol 2010; 1: 147.CrossRefGoogle ScholarPubMed
Litvan, I, Agid, Y, Calne, D, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996; 47(1): 1–9.Google Scholar
Troost, BT, Daroff, RB. The ocular motor defects in progressive supranuclear palsy. Ann Neurol 1977; 2(5): 397–403.Google Scholar
Altiparmak, UE, 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 2006; 26(4): 257–259.Google Scholar
Williams, DR, de Silva, R, Paviour, DC, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 2005; 128(Pt 6): 1247–1258.Google Scholar
Williams, DR, Holton, JL, Strand, K, Revesz, T, Lees, AJ. Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 2007; 22(15): 2235–2241.CrossRefGoogle ScholarPubMed
Stell, R, Bronstein, AM. Eye movement abnormalities in extra pyramidal disease. In: Marsden, CD, Fahn, S (eds.). Movement Disorders 3. Butterworth-Heinemann Ltd; 1994, 88–113.Google Scholar
Vidailhet, M, Rivaud-Pechoux, S. Eye movement disorders in corticobasal degeneration. Adv Neurol 2000; 82: 161–167.Google Scholar
Boxer, AL, Garbutt, S, Seeley, WW, et al. Saccade abnormalities in autopsy-confirmed frontotemporal lobar degeneration and Alzheimer disease. Arch Neurol 2012; 69(4): 509–517.Google Scholar
Bejjani, BP, Arnulf, I, Houeto, JL, et al. Concurrent excitatory and inhibitory effects of high frequency stimulation: an oculomotor study. J Neurol Neurosurg Psychiatry 2002; 72(4): 517–522.Google Scholar
Shaikh, AG, Antoniades, C, Fitzgerald, J, Ghasia, FF. Effects of deep brain stimulation on eye movements and vestibular function. Front Neurol 2018; 9: 444.Google Scholar
Khan, AN, Bronstein, A, Bain, P, Pavese, N, Nandi, D. Pedunculopontine and subthalamic nucleus stimulation effect on saccades in Parkinson disease. World Neurosurg 2019; 126: e219–e31.Google Scholar
Fasano, A, Aquino, CC, Krauss, JK, Honey, CR, Bloem, BR. Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol 2015; 11(2): 98–110.Google Scholar
Krack, P, Batir, A, Van Blercom, N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 2003; 349(20): 1925–1934.Google Scholar
Bostan, AC, Strick, PL. The cerebellum and basal ganglia are interconnected. Neuropsychol Rev 2010; 20(3): 261–270.CrossRefGoogle ScholarPubMed
Shaikh, AG, Straumann, D, Palla, A. Motion illusion-evidence towards human vestibulo-thalamic projections. Cerebellum 2017; 16(3): 656–663.Google Scholar
Stuart, S, Alcock, L, Galna, B, Lord, S, Rochester, L. The measurement of visual sampling during real-world activity in Parkinson’s disease and healthy controls: a structured literature review. J Neurosci Methods 2014; 222: 175–188.CrossRefGoogle ScholarPubMed
Anastasopoulos, D, Ziavra, N, Savvidou, E, Bain, P, Bronstein, AM. Altered eye-to-foot coordination in standing parkinsonian patients during large gaze and whole-body reorientations. Mov Disord 2011; 26(12): 2201–2211.Google Scholar
Glickstein, M, Stein, J. Paradoxical movement in Parkinson’s disease. Trends Neurosci 1991; 14(11): 480–482.Google Scholar
Vitorio, R, Lirani-Silva, E, Pieruccini-Faria, F, et al. Visual cues and gait improvement in Parkinson’s disease: which piece of information is really important? Neuroscience 2014; 277: 273–280.CrossRefGoogle ScholarPubMed
Lohnes, CA, Earhart, GM. Saccadic eye movements are related to turning performance in Parkinson disease. J Parkinsons Dis 2011; 1(1): 109–118.CrossRefGoogle ScholarPubMed
Matsumoto, H, Terao, Y, Furubayashi, T, et al. Small saccades restrict visual scanning area in Parkinson’s disease. Mov Disord 2011; 26(9): 1619–1626.Google Scholar
Archibald, NK, Hutton, SB, Clarke, MP, Mosimann, UP, Burn, DJ. Visual exploration in Parkinson’s disease and Parkinson’s disease dementia. Brain 2013; 136(Pt 3): 739–750.Google Scholar
Jehangir, N, Yu, CY, Song, J, et al. Slower saccadic reading in Parkinson’s disease. PLoS One 2018; 13(1): e0191005.Google Scholar
Moes, E, Lombardi, KM. The relationship between contrast sensitivity, gait, and reading speed in Parkinson’s disease. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 2009; 16(2): 121–132.Google Scholar
Pascoe, M, Alamri, Y, Dalrymple-Alford, J, Anderson, T, MacAskill, M. The symbol-digit modalities test in mild cognitive impairment: evidence from Parkinson’s disease patients. Eur Neurol 2018; 79(3–4): 206–210.Google Scholar
Cano Porras, D, Siemonsma, P, Inzelberg, R, Zeilig, G, Plotnik, M. Advantages of virtual reality in the rehabilitation of balance and gait: systematic review. Neurology 2018; 90(22): 1017–1025.Google Scholar
Marazzi, S, Kiper, P, Palmer, K, Agostini, M, Turolla, A. Effects of vibratory stimulation on balance and gait in Parkinson’s disease: a systematic review and meta-analysis. Eur J Phys Rehabil Med 2020; DOI: 10.23736/S1973-9087.20.06099-2Google Scholar
Olson, M, Lockhart, TE, Lieberman, A. Motor learning deficits in Parkinson’s disease (PD) and their effect on training response in gait and balance: a narrative review. Front Neurol 2019; 10: 62.Google Scholar
Reichert, WH, Doolittle, J, McDowell, FH. Vestibular dysfunction in Parkinson disease. Neurology 1982; 32(10): 1133–1138.Google Scholar
Cipparrone, L, Ginanneschi, A, Degl’Innocenti, F, et al. Electro-oculographic routine examination in Parkinson’s disease. Acta Neurol Scand 1988; 77(1): 6–11.Google Scholar
Venhovens, J, Meulstee, J, Bloem, BR, Verhagen, WI. Neurovestibular analysis and falls in Parkinson’s disease and atypical parkinsonism. Eur J Neurosci 2016; 43(12): 1636–1646.Google Scholar
Scocco, DH, Wagner, JN, Racosta, J, Chade, A, Gershanik, OS. Subjective visual vertical in Pisa syndrome. Parkinsonism Relat Disord 2014; 20(8): 878–883.Google Scholar
Vitale, C, Marcelli, V, Furia, T, et al. Vestibular impairment and adaptive postural imbalance in parkinsonian patients with lateral trunk flexion. Mov Disord 2011; 26(8): 1458–1463.Google Scholar
Bronstein, AM, Yardley, L, Moore, AP, Cleeves, L. Visually and posturally mediated tilt illusion in Parkinson’s disease and in labyrinthine defective subjects. Neurology 1996; 47(3): 651–656.CrossRefGoogle ScholarPubMed
White, OB, Saintcyr, JA, Tomlinson, RD, Sharpe, JA. Ocular motor deficits in Parkinson’s disease. 3. Coordination of eye and head movements. Brain 1988; 111: 115–129.Google Scholar
Lv, W, Guan, Q, Hu, X, et al. Vestibulo-ocular reflex abnormality in Parkinson’s disease detected by video head impulse test. Neurosci Lett 2017; 657: 211–214.Google Scholar
Bronstein, AM, Kennard, C. Predictive ocular motor control in Parkinson’s disease. Brain 1985; 108: 925–940.Google Scholar
Waterston, JA, Barnes, GR, Grealy, MA, Collins, S. Abnormalities of smooth eye and head movement control in Parkinson’s disease. Ann Neurol 1996; 39(6): 749–760.Google Scholar
Cronin, T, Arshad, Q, Seemungal, BM. Vestibular deficits in neurodegenerative disorders: balance, dizziness, and spatial disorientation. Front Neurol 2017; 8: 538.Google Scholar
Bisdorff, AR, Bronstein, AM, Wolsley, C, et al. EMG responses to free fall in elderly subjects and akinetic rigid patients. J Neurol Neurosurg Psychiatry 1999; 66(4): 447–455.Google Scholar
Shalash, AS, Hassan, DM, Elrassas, HH, et al. Auditory- and vestibular-evoked potentials correlate with motor and non-motor features of Parkinson’s disease. Front Neurol 2017; 8: 55.Google Scholar
Cicekli, E, Titiz, AP, Titiz, A, Oztekin, N, Mujdeci, B. Vestibular evoked myogenic potential responses in Parkinson’s disease. Ideggyogyaszati szemle 2019; 72(11–12): 419–425.Google Scholar
de Natale, ER, Ginatempo, F, Paulus, KS, et al. Paired neurophysiological and clinical study of the brainstem at different stages of Parkinson’s disease. Clin Neurophysiol 2015; 126(10): 1871–1878.Google Scholar
de Natale, ER, Ginatempo, F, Paulus, KS, et al. Abnormalities of vestibular-evoked myogenic potentials in idiopathic Parkinson’s disease are associated with clinical evidence of brainstem involvement. Neurol Sci 2015; 36(6): 995–1001.CrossRefGoogle ScholarPubMed
Pollak, L, Prohorov, T, Kushnir, M, Rabey, M. Vestibulocervical reflexes in idiopathic Parkinson disease. Clin Neurophysiol 2009; 39(4–5): 235–240.Google Scholar
Potter-Nerger, M, Govender, S, Deuschl, G, Volkmann, J, Colebatch, JG. Selective changes of ocular vestibular myogenic potentials in Parkinson’s disease. Mov Disord 2015; 30(4): 584–589.CrossRefGoogle ScholarPubMed
Potter-Nerger, M, Reich, MM, Colebatch, JG, Deuschl, G, Volkmann, J. Differential effect of dopa and subthalamic stimulation on vestibular activity in Parkinson’s disease. Mov Disord 2012; 27(10): 1268–1275.Google Scholar
Bronstein, AM, Hood, JD, Gresty, MA, Panagi, C. Visual control of balance in cerebellar and parkinsonian syndromes. Brain 1990; 113(Pt 3): 767–779.Google Scholar
Cooke, JD, Brown, JD, Brooks, VB. Increased dependence on visual information for movement control in patients with Parkinson’s disease. Can J Neurol Sci 1978; 5(4): 413–415.Google Scholar
Martin, JP. The Basal Ganglia and Posture. Lippincott; 1967.Google Scholar
Nakamura, T, Bronstein, AM. The perception of head rotation in Parkinson’s disease. Acta Otolaryngol Suppl 1995; 520(Pt 2): 387–391.Google Scholar
Nakamura, T, Bronstein, AM, Lueck, C, Marsden, CD, Rudge, P. Vestibular, cervical and visual remembered saccades in Parkinson’s disease. Brain 1994; 117(Pt 6): 1423–1432.CrossRefGoogle ScholarPubMed
Pastor, MA, Day, BL, Marsden, CD. Vestibular induced postural responses in Parkinson’s disease. Brain 1993; 116(Pt 5): 1177–1190.Google Scholar
Rothwell, JC, Obeso, JA, Traub, MM, Marsden, CD. The behaviour of the long-latency stretch reflex in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 1983; 46(1): 35–44.Google Scholar
Berardelli, A, Rothwell, JC, Thompson, PD, Hallett, M. Pathophysiology of bradykinesia in Parkinson’s disease. Brain 2001; 124(Pt 11): 2131–2146.CrossRefGoogle ScholarPubMed
Delval, A, Tard, C, Defebvre, L. Why we should study gait initiation in Parkinson’s disease. Clin Neurophysiol 2014; 44(1): 69–76.Google Scholar
Beylergil, SB, Ozinga, S, Walker, MF, McIntyre, CC, Shaikh, AG. Vestibular heading perception in Parkinson’s disease. Prog Brain Res 2019; 249: 307–319.CrossRefGoogle ScholarPubMed
Yakubovich, S, Israeli-Korn, S, Halperin, O, et al. Visual self-motion cues are impaired yet over-weighted during visual-vestibular integration in Parkinson’s disease. Brain Commun 2020; 2(1): 1–15.Google Scholar
Bertolini, G, Wicki, A, Baumann, CR, Straumann, D, Palla, A. Impaired tilt perception in Parkinson’s disease: a central vestibular integration failure. PLoS One 2015; 10(4): e0124253.Google Scholar
Putcha, D, Ross, RS, Rosen, ML, et al. Functional correlates of optic flow motion processing in Parkinson’s disease. Front Integr Neurosci 2014; 8: 57.Google Scholar
Amick, MM, Schendan, HE, Ganis, G, Cronin-Golomb, A. Frontostriatal circuits are necessary for visuomotor transformation: mental rotation in Parkinson’s disease. Neuropsychologia 2006; 44(3): 339–349.CrossRefGoogle ScholarPubMed
Gitchel, GT, Wetzel, PA, Baron, MS. Pervasive ocular tremor in patients with Parkinson disease. Arch Neurol 2012; 69(8): 1011–1017.Google Scholar
Kaski, D, Saifee, TA, Buckwell, D, Bronstein, AM. Ocular tremor in Parkinson’s disease is due to head oscillation. Mov Disord 2013; 28(4): 534–537.Google Scholar
Leigh, RJ, Martinez-Conde, S. Tremor of the eyes, or of the head, in Parkinson’s disease? Mov Disord 2013; 28(6): 691–693.Google Scholar
Kaski, D, Bronstein, AM. Ocular tremor in Parkinson’s disease: discussion, debate, and controversy. Front Neurol 2017; 8: 134.CrossRefGoogle ScholarPubMed
MacAskill, M, Myall, D. “Pervasive ocular tremor of Parkinson’s” is not pervasive, ocular, or uniquely parkinsonian. 2020. Doi: 10.31219/osf.io/s8rwtGoogle Scholar
Roze, E, Coelho-Braga, MC, Gayraud, D, et al. Head tremor in Parkinson’s disease. Mov Disord 2006; 21(8): 1245–1248.Google Scholar
Coe, BC, Trappenberg, T, Munoz, DP. Modeling saccadic action selection: cortical and basal ganglia signals coalesce in the superior colliculus. Front Syst Neurosci 2019; 13: 3.CrossRefGoogle ScholarPubMed
Bronstein, AM, Gresty, MA, Rudge, P. Neuro-otological assessment in the patient with balance and gait disorder. In: Bronstein, AM, Brandt, T, Woollacott, M, (eds.). Clinical Disorders of Balance, Posture and Gait. Hodder Arnold; 1996.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×