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Early ophthalmologic features of Parkinson’s disease: a review of preceding clinical and diagnostic markers

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Abstract

Non-motor symptoms in Parkinson’s disease are an important cause of morbidity and may even precede the onset of the motor features of the disease. Visual abnormalities are among the most frequent non-motor symptoms observed during the early stages of the disease. Some of the visual symptoms of Parkinson’s disease can likely be explained by the presence of dopaminergic neurons within the retina, where the progressive loss of dopamine and the accumulation of α-synuclein within the retinal layers leads to visual dysfunction, while some are caused by abnormalities in cortical visual processing. Many of these visual symptoms can be overlooked or go unrecognized. We review the visual symptoms in Parkinson’s disease, including visual-processing and ocular motility abnormalities, stereopsis deficits, and visual hallucinations, focusing on the early stages of the disease. We focus on the reciprocal influence between the visual symptoms and the progression of the disease, analyzing the influence of dopaminergic therapy on the visual abnormalities. Finally, we discuss the possible role of some of these visual symptoms as possible markers or early diagnostic signs of the disease.

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References

  1. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39

    Article  CAS  PubMed  Google Scholar 

  2. Coon EA, Daube JR, Dejesus-Hernandez M, Adeli A, Savica R, Parisi JE, Dickson DW, Josephs KA, Baker MC, Johnson KA, Ivnik RJ, Petersen RC, Knopman DS, Boylan KB, Rademakers R, Boeve BF (2013) Clinical and electrophysiologic variability in amyotrophic lateral sclerosis within a kindred harboring the C9ORF72 repeat expansion. Amyotrophic Lateral Scler Frontotemporal Degener 14:132–137. https://doi.org/10.3109/17482968.2012.724075

    Article  CAS  Google Scholar 

  3. Iranzo A, Molinuevo JL, Santamaria J, Serradell M, Marti MJ, Valldeoriola F, Tolosa E (2006) Rapid-eye-movement sleep behaviour disorder as an early marker for a neurodegenerative disorder: a descriptive study. Lancet Neurol 5:572–577

    Article  PubMed  Google Scholar 

  4. Iranzo A, Tolosa E, Gelpi E, Molinuevo JL, Valldeoriola F, Serradell M, Sanchez-Valle R, Vilaseca I, Lomena F, Vilas D, Llado A, Gaig C, Santamaria J (2013) Neurodegenerative disease status and post-mortem pathology in idiopathic rapid-eye-movement sleep behaviour disorder: an observational cohort study. Lancet Neurol 12:443–453. https://doi.org/10.1016/S1474-4422(13)70056-5

    Article  PubMed  Google Scholar 

  5. Savica R, Carlin JM, Grossardt BR, Bower JH, Ahlskog JE, Maraganore DM, Bharucha AE, Rocca WA (2009) Medical records documentation of constipation preceding Parkinson disease: a case-control study. Neurology 73:1752–1758. https://doi.org/10.1212/WNL.0b013e3181c34af5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Postuma RB, Gagnon JF, Vendette M, Desjardins C, Montplaisir JY (2011) Olfaction and color vision identify impending neurodegeneration in rapid eye movement sleep behavior disorder. Ann Neurol 69:811–818. https://doi.org/10.1002/ana.22282

    Article  PubMed  Google Scholar 

  7. Shiba M, Bower JH, Maraganore DM, McDonnell SK, Peterson BJ, Ahlskog JE, Schaid DJ, Rocca WA (2000) Anxiety disorders and depressive disorders preceding Parkinson’s disease: a case-control study. Mov Disord 15:669–677

    Article  CAS  PubMed  Google Scholar 

  8. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211

    Article  PubMed  Google Scholar 

  9. Ravn AH, Thyssen JP, Egeberg A (2017) Skin disorders in Parkinson’s disease: potential biomarkers and risk factors. Clin Cosmet Investig Dermatol 10:87–92. https://doi.org/10.2147/CCID.S130319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Picillo M, Palladino R, Barone P, Erro R, Colosimo C, Marconi R, Morgante L, Antonini A, Group PS (2017) The PRIAMO study: urinary dysfunction as a marker of disease progression in early Parkinson’s disease. Eur J Neurol 24:788–795. https://doi.org/10.1111/ene.13290

    Article  CAS  PubMed  Google Scholar 

  11. Brabenec L, Mekyska J, Galaz Z, Rektorova I (2017) Speech disorders in Parkinson’s disease: early diagnostics and effects of medication and brain stimulation. J Neural Transm 124:303–334. https://doi.org/10.1007/s00702-017-1676-0

    Article  CAS  PubMed  Google Scholar 

  12. Diederich NJ, Pieri V, Hipp G, Rufra O, Blyth S, Vaillant M (2010) Discriminative power of different nonmotor signs in early Parkinson’s disease. A case-control study. Mov Disord 25:882–887. https://doi.org/10.1002/mds.22963

    Article  PubMed  Google Scholar 

  13. Davidsdottir S, Cronin-Golomb A, Lee A (2005) Visual and spatial symptoms in Parkinson’s disease. Vision Res 45:1285–1296. https://doi.org/10.1016/j.visres.2004.11.006

    Article  PubMed  Google Scholar 

  14. Urwyler P, Nef T, Killen A, Collerton D, Thomas A, Burn D, McKeith I, Mosimann UP (2014) Visual complaints and visual hallucinations in Parkinson’s disease. Parkinsonism Relat Disord 20:318–322. https://doi.org/10.1016/j.parkreldis.2013.12.009

    Article  PubMed  Google Scholar 

  15. Biousse V, Skibell BC, Watts RL, Loupe DN, Drews-Botsch C, Newman NJ (2004) Ophthalmologic features of Parkinson’s disease. Neurology 62:177–180

    Article  CAS  PubMed  Google Scholar 

  16. Frederick JM, Rayborn ME, Laties AM, Lam DM, Hollyfield JG (1982) Dopaminergic neurons in the human retina. J Comp Neurol 210:65–79. https://doi.org/10.1002/cne.902100108

    Article  CAS  PubMed  Google Scholar 

  17. Nguyen-Legros J (1988) Functional neuroarchitecture of the retina: hypothesis on the dysfunction of retinal dopaminergic circuitry in Parkinson’s disease. Surg Radiol Anat 10:137–144

    Article  CAS  PubMed  Google Scholar 

  18. Harnois C, Di Paolo T (1990) Decreased dopamine in the retinas of patients with Parkinson’s disease. Invest Ophthalmol Vis Sci 31:2473–2475

    CAS  PubMed  Google Scholar 

  19. Bodis-Wollner I, Kozlowski PB, Glazman S, Miri S (2014) α-Synuclein in the inner retina in parkinson disease. Ann Neurol 75:964–966. https://doi.org/10.1002/ana.24182

    Article  CAS  PubMed  Google Scholar 

  20. Beach TG, Carew J, Serrano G, Adler CH, Shill HA, Sue LI, Sabbagh MN, Akiyama H, Cuenca N, Arizona Parkinson’s Disease C (2014) Phosphorylated alpha-synuclein-immunoreactive retinal neuronal elements in Parkinson’s disease subjects. Neurosci Lett 571:34–38. https://doi.org/10.1016/j.neulet.2014.04.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Koh SB, Suh SI, Kim SH, Kim JH (2013) Stereopsis and extrastriate cortical atrophy in Parkinson’s disease: a voxel-based morphometric study. Neuroreport 24:229–232. https://doi.org/10.1097/WNR.0b013e32835edbc5

    Article  PubMed  Google Scholar 

  22. Stebbins GT, Goetz CG, Carrillo MC, Bangen KJ, Turner DA, Glover GH, Gabrieli JD (2004) Altered cortical visual processing in PD with hallucinations: an fMRI study. Neurology 63:1409–1416

    Article  CAS  PubMed  Google Scholar 

  23. Arrigo A, Calamuneri A, Milardi D, Mormina E, Rania L, Postorino E, Marino S, Di Lorenzo G, Anastasi GP, Ghilardi MF, Aragona P, Quartarone A, Gaeta M (2017) Visual system involvement in patients with newly diagnosed Parkinson disease. Radiology 285:885–895. https://doi.org/10.1148/radiol.2017161732

    Article  PubMed  Google Scholar 

  24. Sharpe JA (2008) Neurophysiology and neuroanatomy of smooth pursuit: lesion studies. Brain Cogn 68:241–254. https://doi.org/10.1016/j.bandc.2008.08.015

    Article  PubMed  Google Scholar 

  25. Pierrot-Deseilligny C, Milea D, Muri RM (2004) Eye movement control by the cerebral cortex. Curr Opin Neurol 17:17–25

    Article  PubMed  Google Scholar 

  26. Rieger JW, Kim A, Argyelan M, Farber M, Glazman S, Liebeskind M, Meyer T, Bodis-Wollner I (2008) Cortical functional anatomy of voluntary saccades in Parkinson disease. Clin EEG Neurosci 39:169–174. https://doi.org/10.1177/155005940803900404

    Article  PubMed  Google Scholar 

  27. Postuma RB, Aarsland D, Barone P, Burn DJ, Hawkes CH, Oertel W, Ziemssen T (2012) Identifying prodromal Parkinson’s disease: pre-motor disorders in Parkinson’s disease. Mov Disord 27:617–626. https://doi.org/10.1002/mds.24996

    Article  PubMed  Google Scholar 

  28. Inzelberg R, Ramirez JA, Nisipeanu P, Ophir A (2004) Retinal nerve fiber layer thinning in Parkinson disease. Vision Res 44:2793–2797. https://doi.org/10.1016/j.visres.2004.06.009

    Article  PubMed  Google Scholar 

  29. Altintas O, Iseri P, Ozkan B, Caglar Y (2008) Correlation between retinal morphological and functional findings and clinical severity in Parkinson’s disease. Doc Ophthalmol 116:137–146. https://doi.org/10.1007/s10633-007-9091-8

    Article  PubMed  Google Scholar 

  30. La Morgia C, Barboni P, Rizzo G, Carbonelli M, Savini G, Scaglione C, Capellari S, Bonazza S, Giannoccaro MP, Calandra-Buonaura G, Liguori R, Cortelli P, Martinelli P, Baruzzi A, Carelli V (2013) Loss of temporal retinal nerve fibers in Parkinson disease: a mitochondrial pattern? Eur J Neurol 20:198–201. https://doi.org/10.1111/j.1468-1331.2012.03701.x

    Article  PubMed  Google Scholar 

  31. Roth NM, Saidha S, Zimmermann H, Brandt AU, Isensee J, Benkhellouf-Rutkowska A, Dornauer M, Kuhn AA, Muller T, Calabresi PA, Paul F (2014) Photoreceptor layer thinning in idiopathic Parkinson’s disease. Mov Disord 29:1163–1170. https://doi.org/10.1002/mds.25896

    Article  PubMed  Google Scholar 

  32. Archibald NK, Clarke MP, Mosimann UP, Burn DJ (2011) Visual symptoms in Parkinson’s disease and Parkinson’s disease dementia. Mov Disord 26:2387–2395. https://doi.org/10.1002/mds.23891

    Article  PubMed  Google Scholar 

  33. Satue M, Obis J, Rodrigo MJ, Otin S, Fuertes MI, Vilades E, Gracia H, Ara JR, Alarcia R, Polo V, Larrosa JM, Pablo LE, Garcia-Martin E (2016) Optical coherence tomography as a biomarker for diagnosis, progression, and prognosis of neurodegenerative diseases. J Ophthalmol 2016:8503859. https://doi.org/10.1155/2016/8503859

    Article  PubMed  PubMed Central  Google Scholar 

  34. Garcia-Martin E, Larrosa JM, Polo V, Satue M, Marques ML, Alarcia R, Seral M, Fuertes I, Otin S, Pablo LE (2014) Distribution of retinal layer atrophy in patients with Parkinson disease and association with disease severity and duration. Am J Ophthalmol 157:470–478 e472. https://doi.org/10.1016/j.ajo.2013.09.028

    Article  PubMed  Google Scholar 

  35. Garcia-Martin E, Satue M, Otin S, Fuertes I, Alarcia R, Larrosa JM, Polo V, Pablo LE (2014) Retina measurements for diagnosis of Parkinson disease. Retina 34:971–980. https://doi.org/10.1097/IAE.0000000000000028

    Article  PubMed  Google Scholar 

  36. Satue M, Seral M, Otin S, Alarcia R, Herrero R, Bambo MP, Fuertes MI, Pablo LE, Garcia-Martin E (2014) Retinal thinning and correlation with functional disability in patients with Parkinson’s disease. Br J Ophthalmol 98:350–355. https://doi.org/10.1136/bjophthalmol-2013-304152

    Article  CAS  PubMed  Google Scholar 

  37. Garcia-Martin E, Pablo LE, Bambo MP, Alarcia R, Polo V, Larrosa JM, Vilades E, Cameo B, Orduna E, Ramirez T, Satue M (2017) Comparison of peripapillary choroidal thickness between healthy subjects and patients with Parkinson’s disease. PLoS One 12:e0177163. https://doi.org/10.1371/journal.pone.0177163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Buttner T, Kuhn W, Muller T, Patzold T, Heidbrink K, Przuntek H (1995) Distorted color discrimination in ‘de novo’ parkinsonian patients. Neurology 45:386–387

    Article  CAS  PubMed  Google Scholar 

  39. Bertrand JA, Bedetti C, Postuma RB, Monchi O, Genier Marchand D, Jubault T, Gagnon JF (2012) Color discrimination deficits in Parkinson’s disease are related to cognitive impairment and white-matter alterations. Mov Disord 27:1781–1788. https://doi.org/10.1002/mds.25272

    Article  PubMed  Google Scholar 

  40. Regan BC, Freudenthaler N, Kolle R, Mollon JD, Paulus W (1998) Colour discrimination thresholds in Parkinson’s disease: results obtained with a rapid computer-controlled colour vision test. Vision Res 38:3427–3431

    Article  CAS  PubMed  Google Scholar 

  41. Muller T, Meisel M, Russ H, Przuntek H (2003) Motor impairment influences Farnsworth–Munsell 100 Hue test error scores in Parkinson’s disease patients. J Neurol Sci 213:61–65

    Article  PubMed  Google Scholar 

  42. Silva MF, Faria P, Regateiro FS, Forjaz V, Januario C, Freire A, Castelo-Branco M (2005) Independent patterns of damage within magno-, parvo- and koniocellular pathways in Parkinson’s disease. Brain 128:2260–2271. https://doi.org/10.1093/brain/awh581

    Article  CAS  PubMed  Google Scholar 

  43. Piro A, Tagarelli A, Nicoletti G, Fletcher R, Quattrone A (2014) Color vision impairment in Parkinson’s disease. J Parkinsons Dis 4:317–319. https://doi.org/10.3233/JPD-140359

    Article  CAS  PubMed  Google Scholar 

  44. Haug BA, Kolle RU, Trenkwalder C, Oertel WH, Paulus W (1995) Predominant affection of the blue cone pathway in Parkinson’s disease. Brain 118(Pt 3):771–778

    Article  PubMed  Google Scholar 

  45. Postuma RB, Lang AE, Massicotte-Marquez J, Montplaisir J (2006) Potential early markers of Parkinson disease in idiopathic REM sleep behavior disorder. Neurology 66:845–851

    Article  CAS  PubMed  Google Scholar 

  46. Postuma RB, Gagnon JF, Bertrand JA, Genier Marchand D, Montplaisir JY (2015) Parkinson risk in idiopathic REM sleep behavior disorder: preparing for neuroprotective trials. Neurology 84:1104–1113. https://doi.org/10.1212/WNL.0000000000001364

    Article  PubMed  PubMed Central  Google Scholar 

  47. Fereshtehnejad SM, Romenets SR, Anang JB, Latreille V, Gagnon JF, Postuma RB (2015) New clinical subtypes of parkinson disease and their longitudinal progression: a prospective cohort comparison with other phenotypes. JAMA Neurol 72:863–873. https://doi.org/10.1001/jamaneurol.2015.0703

    Article  PubMed  Google Scholar 

  48. Martin I, Dawson VL, Dawson TM (2011) Recent advances in the genetics of Parkinson’s disease. Annu Rev Genom Hum Genet 12:301–325. https://doi.org/10.1146/annurev-genom-082410-101440

    Article  CAS  Google Scholar 

  49. Marras C, Schule B, Munhoz RP, Rogaeva E, Langston JW, Kasten M, Meaney C, Klein C, Wadia PM, Lim SY, Chuang RS, Zadikof C, Steeves T, Prakash KM, de Bie RM, Adeli G, Thomsen T, Johansen KK, Teive HA, Asante A, Reginold W, Lang AE (2011) Phenotype in parkinsonian and nonparkinsonian LRRK2 G2019S mutation carriers. Neurology 77:325–333. https://doi.org/10.1212/WNL.0b013e318227042d

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Price MJ, Feldman RG, Adelberg D, Kayne H (1992) Abnormalities in color vision and contrast sensitivity in Parkinson’s disease. Neurology 42:887–890

    Article  CAS  PubMed  Google Scholar 

  51. Buttner T, Kuhn W, Patzold T, Przuntek H (1994) L-Dopa improves colour vision in Parkinson’s disease. J Neural Transm Park Dis Dement Sect 7:13–19

    Article  CAS  PubMed  Google Scholar 

  52. Ming W, Palidis DJ, Spering M, McKeown MJ (2016) Visual Contrast Sensitivity in Early-Stage Parkinson’s Disease. Invest Ophthalmol Vis Sci 57:5696–5704. https://doi.org/10.1167/iovs.16-20025

    Article  PubMed  Google Scholar 

  53. Regan D, Neima D (1984) Low-contrast letter charts in early diabetic retinopathy, ocular hypertension, glaucoma, and Parkinson’s disease. Br J Ophthalmol 68:885–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bodis-Wollner I, Marx MS, Mitra S, Bobak P, Mylin L, Yahr M (1987) Visual dysfunction in Parkinson’s disease. Loss in spatiotemporal contrast sensitivity. Brain 110(Pt 6):1675–1698

    Article  PubMed  Google Scholar 

  55. Mestre D, Blin O, Serratrice G, Pailhous J (1990) Spatiotemporal contrast sensitivity differs in normal aging and Parkinson’s disease. Neurology 40:1710–1714

    Article  CAS  PubMed  Google Scholar 

  56. Hutton JT, Morris JL, Elias JW, Varma R, Poston JN (1991) Spatial contrast sensitivity is reduced in bilateral Parkinson’s disease. Neurology 41:1200–1202

    Article  CAS  PubMed  Google Scholar 

  57. Bodis-Wollner I, Onofrj M (1987) The visual system in Parkinson’s disease. Adv Neurol 45:323–327

    CAS  PubMed  Google Scholar 

  58. Bulens C, Meerwaldt JD, Van der Wildt GJ, Van Deursen JB (1987) Effect of levodopa treatment on contrast sensitivity in Parkinson’s disease. Ann Neurol 22:365–369. https://doi.org/10.1002/ana.410220313

    Article  CAS  PubMed  Google Scholar 

  59. Hutton JT, Morris JL, Elias JW (1993) Levodopa improves spatial contrast sensitivity in Parkinson’s disease. Arch Neurol 50:721–724

    Article  CAS  PubMed  Google Scholar 

  60. Blekher T, Weaver M, Rupp J, Nichols WC, Hui SL, Gray J, Yee RD, Wojcieszek J, Foroud T (2009) Multiple step pattern as a biomarker in Parkinson disease. Parkinsonism Relat Disord 15:506–510. https://doi.org/10.1016/j.parkreldis.2009.01.002

    Article  PubMed  PubMed Central  Google Scholar 

  61. Shibasaki H, Tsuji S, Kuroiwa Y (1979) Oculomotor abnormalities in Parkinson’s disease. Arch Neurol 36:360–364

    Article  CAS  PubMed  Google Scholar 

  62. Terao Y, Fukuda H, Ugawa Y, Hikosaka O (2013) New perspectives on the pathophysiology of Parkinson’s disease as assessed by saccade performance: a clinical review. Clin Neurophysiol 124:1491–1506. https://doi.org/10.1016/j.clinph.2013.01.021

    Article  PubMed  Google Scholar 

  63. DeJong JD, Jones GM (1971) Akinesia, hypokinesia, and bradykinesia in the oculomotor system of patients with Parkinson’s disease. Exp Neurol 32:58–68

    Article  CAS  PubMed  Google Scholar 

  64. Jones GM, DeJong JD (1971) Dynamic characteristics of saccadic eye movements in Parkinson’s disease. Exp Neurol 31:17–31

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. White OB, Saint-Cyr JA, Tomlinson RD, Sharpe JA (1983) Ocular motor deficits in Parkinson’s disease. II. Control of the saccadic and smooth pursuit systems. Brain 106(Pt 3):571–587

    Article  PubMed  Google Scholar 

  67. Srivastava A, Sharma R, Sood SK, Shukla G, Goyal V, Behari M (2014) Saccadic eye movements in Parkinson’s disease. Indian J Ophthalmol 62:538–544. https://doi.org/10.4103/0301-4738.133482

    Article  PubMed  PubMed Central  Google Scholar 

  68. Terao Y, Fukuda H, Yugeta A, Hikosaka O, Nomura Y, Segawa M, Hanajima R, Tsuji S, Ugawa Y (2011) 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. https://doi.org/10.1016/j.neuropsychologia.2011.03.002

    Article  PubMed  Google Scholar 

  69. Gaymard B, Lynch J, Ploner CJ, Condy C, Rivaud-Pechoux S (2003) The parieto-collicular pathway: anatomical location and contribution to saccade generation. Eur J Neurosci 17:1518–1526

    Article  CAS  PubMed  Google Scholar 

  70. Lueck CJ, Tanyeri S, Crawford TJ, Henderson L, Kennard C (1990) Antisaccades and remembered saccades in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:284–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Briand KA, Strallow D, Hening W, Poizner H, Sereno AB (1999) Control of voluntary and reflexive saccades in Parkinson’s disease. Exp Brain Res 129:38–48

    Article  CAS  PubMed  Google Scholar 

  72. Chan F, Armstrong IT, Pari G, Riopelle RJ, Munoz DP (2005) Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 43:784–796. https://doi.org/10.1016/j.neuropsychologia.2004.06.026

    Article  PubMed  Google Scholar 

  73. Zackon DH, Sharpe JA (1987) Smooth pursuit in senescence. Effects of target acceleration and velocity. Acta Otolaryngol 104:290–297

    Article  CAS  PubMed  Google Scholar 

  74. Gibson JM, Pimlott R, Kennard C (1987) Ocular motor and manual tracking in Parkinson’s disease and the effect of treatment. J Neurol Neurosurg Psychiatry 50:853–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Basso MA, Pokorny JJ, Liu P (2005) Activity of substantia nigra pars reticulata neurons during smooth pursuit eye movements in monkeys. Eur J Neurosci 22:448–464. https://doi.org/10.1111/j.1460-9568.2005.04215.x

    Article  PubMed  Google Scholar 

  76. Bares M, Brazdil M, Kanovsky P, Jurak P, Daniel P, Kukleta M, Rektor I (2003) The effect of apomorphine administration on smooth pursuit ocular movements in early Parkinsonian patients. Parkinsonism Relat Disord 9:139–144

    Article  PubMed  Google Scholar 

  77. Waterston JA, Barnes GR, Grealy MA, Collins S (1996) Abnormalities of smooth eye and head movement control in Parkinson’s disease. Ann Neurol 39:749–760. https://doi.org/10.1002/ana.410390611

    Article  CAS  PubMed  Google Scholar 

  78. Rascol O, Sabatini U, Simonetta-Moreau M, Montastruc JL, Rascol A, Clanet M (1991) Square wave jerks in parkinsonian syndromes. J Neurol Neurosurg Psychiatry 54:599–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Abadi RV, Gowen E (2004) Characteristics of saccadic intrusions. Vision Res 44:2675–2690. https://doi.org/10.1016/j.visres.2004.05.009

    Article  CAS  PubMed  Google Scholar 

  80. Shaikh AG, Xu-Wilson M, Grill S, Zee DS (2011) ‘Staircase’ square-wave jerks in early Parkinson’s disease. Br J Ophthalmol 95:705–709. https://doi.org/10.1136/bjo.2010.179630

    Article  PubMed  Google Scholar 

  81. Averbuch-Heller L, Stahl JS, Hlavin ML, Leigh RJ (1999) Square-wave jerks induced by pallidotomy in parkinsonian patients. Neurology 52:185–188

    Article  CAS  PubMed  Google Scholar 

  82. Ghadban R, Martinez JM, Diehl NN, Mohney BG (2015) The incidence and clinical characteristics of adult-onset convergence insufficiency. Ophthalmology 122:1056–1059. https://doi.org/10.1016/j.ophtha.2014.12.010

    Article  PubMed  Google Scholar 

  83. Racette BA, Gokden MS, Tychsen LS, Perlmutter JS (1999) Convergence insufficiency in idiopathic Parkinson’s disease responsive to levodopa. Strabismus 7:169–174

    Article  CAS  PubMed  Google Scholar 

  84. Nowacka B, Lubinski W, Honczarenko K, Potemkowski A, Safranow K (2014) Ophthalmological features of Parkinson disease. Med Sci Monit 20:2243–2249. https://doi.org/10.12659/MSM.890861

    Article  PubMed  PubMed Central  Google Scholar 

  85. Almer Z, Klein KS, Marsh L, Gerstenhaber M, Repka MX (2012) Ocular motor and sensory function in Parkinson’s disease. Ophthalmology 119:178–182. https://doi.org/10.1016/j.ophtha.2011.06.040

    Article  PubMed  Google Scholar 

  86. Gitchel GT, Wetzel PA, Baron MS (2012) Pervasive ocular tremor in patients with Parkinson disease. Arch Neurol 69:1011–1017. https://doi.org/10.1001/archneurol.2012.70

    Article  PubMed  Google Scholar 

  87. Duval C (2013) Ocular tremor in Parkinson’s disease: the debate is not over. Mov Disord 28:713–714. https://doi.org/10.1002/mds.25514

    Article  PubMed  Google Scholar 

  88. Gitchel GT, Wetzel PA, Baron MS (2013) Slowed saccades and increased square wave jerks in essential tremor. Tremor Other Hyperkinet Mov (N Y) 3. https://doi.org/10.7916/D8251GXN

  89. Kaski D, Saifee TA, Buckwell D, Bronstein AM (2013) Ocular tremor in Parkinson’s disease is due to head oscillation. Mov Disord 28:534–537. https://doi.org/10.1002/mds.25342

    Article  PubMed  Google Scholar 

  90. Kim SH, Park JH, Kim YH, Koh SB (2011) Stereopsis in drug naive Parkinson’s disease patients. Can J Neurol Sci 38:299–302

    Article  PubMed  Google Scholar 

  91. Sun L, Zhang H, Gu Z, Cao M, Li D, Chan P (2014) Stereopsis impairment is associated with decreased color perception and worse motor performance in Parkinson’s disease. Eur J Med Res 19:29. https://doi.org/10.1186/2047-783X-19-29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Kwon KY, Kang SH, Kim M, Lee HM, Jang JW, Kim JY, Lee SM, Koh SB (2014) Nonmotor symptoms and cognitive decline in de novo Parkinson’s disease. Can J Neurol Sci 41:597–602. https://doi.org/10.1017/cjn.2014.3

    Article  PubMed  Google Scholar 

  93. Diederich NJ, Fenelon G, Stebbins G, Goetz CG (2009) Hallucinations in Parkinson disease. Nat Rev Neurol 5:331–342. https://doi.org/10.1038/nrneurol.2009.62

    Article  CAS  PubMed  Google Scholar 

  94. Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG (2008) The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord 23:837–844. https://doi.org/10.1002/mds.21956

    Article  PubMed  Google Scholar 

  95. Factor SA, Molho ES, Podskalny GD, Brown D (1995) Parkinson’s disease: drug-induced psychiatric states. Adv Neurol 65:115–138

    CAS  PubMed  Google Scholar 

  96. Diederich NJ, Goetz CG, Raman R, Pappert EJ, Leurgans S, Piery V (1998) Poor visual discrimination and visual hallucinations in Parkinson’s disease. Clin Neuropharmacol 21:289–295

    CAS  PubMed  Google Scholar 

  97. Pagonabarraga J, Martinez-Horta S, Fernandez de Bobadilla R, Perez J, Ribosa-Nogue R, Marin J, Pascual-Sedano B, Garcia C, Gironell A, Kulisevsky J (2016) Minor hallucinations occur in drug-naive Parkinson’s disease patients, even from the premotor phase. Mov Disord 31:45–52. https://doi.org/10.1002/mds.26432

    Article  PubMed  Google Scholar 

  98. Forsaa EB, Larsen JP, Wentzel-Larsen T, Goetz CG, Stebbins GT, Aarsland D, Alves G (2010) A 12-year population-based study of psychosis in Parkinson disease. Arch Neurol 67:996–1001. https://doi.org/10.1001/archneurol.2010.166

    Article  PubMed  Google Scholar 

  99. Sweet RD, McDowell FH, Feigenson JS, Loranger AW, Goodell H (1976) Mental symptoms in Parkinson’s disease during chronic treatment with levodopa. Neurology 26:305–310

    Article  CAS  PubMed  Google Scholar 

  100. Merims D, Shabtai H, Korczyn AD, Peretz C, Weizman N, Giladi N (2004) Antiparkinsonian medication is not a risk factor for the development of hallucinations in Parkinson’s disease. J Neural Transm 111:1447–1453. https://doi.org/10.1007/s00702-004-0209-9

    Article  CAS  PubMed  Google Scholar 

  101. Ffytche DH, Creese B, Politis M, Chaudhuri KR, Weintraub D, Ballard C, Aarsland D (2017) The psychosis spectrum in Parkinson disease. Nat Rev Neurol 13:81–95. https://doi.org/10.1038/nrneurol.2016.200

    Article  PubMed  PubMed Central  Google Scholar 

  102. Anang JB, Gagnon JF, Bertrand JA, Romenets SR, Latreille V, Panisset M, Montplaisir J, Postuma RB (2014) Predictors of dementia in Parkinson disease: a prospective cohort study. Neurology 83:1253–1260. https://doi.org/10.1212/WNL.0000000000000842

    Article  PubMed  PubMed Central  Google Scholar 

  103. Diederich NJ, Raman R, Leurgans S, Goetz CG (2002) Progressive worsening of spatial and chromatic processing deficits in Parkinson disease. Arch Neurol 59:1249–1252

    Article  PubMed  Google Scholar 

  104. Boeve BF, Silber MH, Ferman TJ, Kokmen E, Smith GE, Ivnik RJ, Parisi JE, Olson EJ, Petersen RC (1998) REM sleep behavior disorder and degenerative dementia: an association likely reflecting Lewy body disease. Neurology 51:363–370

    Article  CAS  PubMed  Google Scholar 

  105. Birch J, Kolle RU, Kunkel M, Paulus W, Upadhyay P (1998) Acquired colour deficiency in patients with Parkinson’s disease. Vision Res 38:3421–3426

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Lea Dacy for assistance with proof-reading and formatting.

Funding

PT and BLB have nothing to disclose. JJC receives research support from the National Institute on Aging and has received research support from Quark Pharmaceuticals within the last 12 months. RS receives research support from the National Institute on Aging and through a Small Grants Program funded by CTSA Grant Number UL1 TR000135 from the National Center for Advancing Translational Sciences (NCATS), a component of the National Institutes of Health (NIH).

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Authors and Affiliations

  1. Department of Neurology, Mayo Clinic, 200 First Street, SW, Rochester, MN, 55902, USA

    Pierpaolo Turcano, John J. Chen, Britta L. Bureau & Rodolfo Savica

  2. Department of Ophthalmology, Mayo Clinic, 200 First Street, SW, Rochester, MN, 55902, USA

    John J. Chen

  3. Division of Epidemiology, Department of Health Sciences Research, Mayo Clinic, 200 First Street, SW, Rochester, MN, 55902, USA

    Rodolfo Savica

Authors
  1. Pierpaolo Turcano
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  2. John J. Chen
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  3. Britta L. Bureau
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  4. Rodolfo Savica
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Contributions

PT participated in execution of the research project, and wrote the first draft. JJC participated in organization of the research project and review and critique of the manuscript. BLB participated in execution of the research project and review and critique of the manuscript. RS was responsible for conception of the research project; and review and critique of the manuscript.

Corresponding author

Correspondence to Rodolfo Savica.

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Ethical approval for research involving human participants

This manuscript is a review of past clinical studies, all of which were performed in accordance with ethical standards in effect on their respective publication dates.

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All authors declare that they have no conflict of interest.

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Turcano, P., Chen, J.J., Bureau, B.L. et al. Early ophthalmologic features of Parkinson’s disease: a review of preceding clinical and diagnostic markers. J Neurol 266, 2103–2111 (2019). https://doi.org/10.1007/s00415-018-9051-0

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  • DOI: https://doi.org/10.1007/s00415-018-9051-0

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