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01-11-2009 | Basic Neurosciences, Genetics and Immunology - Original Article

Retinopathy in Parkinson disease

Author: Ivan Bodis-Wollner

Published in: Journal of Neural Transmission | Issue 11/2009

Abstract

One of the non-motor manifestations of PD is visual system involvement. Foveal vision is a main contributor to both visual recognition and discrimination and to both overt and covert visual attention. Experimental evidence from humans and monkeys shows that D1 and D2 receptors are essential for retinal ganglion cell receptive field organization. The evidence linking retinopathy and foveal visual impairment in PD is discussed. A model of retinal preganglionic dopaminergic circuitry is presented. Experimental evidence in humans, using Optical Coherence Tomography shows morphological changes of retinal neurons, including ganglion cells in PD. The diagnosis of pre-cardinal stage of PD (PCPD) may take advantage of the wide availability of optical coherence tomography as a potential biomarker. Fourier-domain OCT and visual testing may contribute a quantitative approach to the early diagnosis, the effects of treatment and follow-up of progression of PD.

Altintas O, Iseri P, Ozkan B, Caglar Y (2008) Correlation between retinal morphological and functional findings and clinical severity in Parkinsons disease. Doc Ophthalmol 1116:137–146CrossRef

Antal A, Pfeiffer R, Bodis-Wollner I (1996) Simultaneously evoked primary and cognitive visual evoked potentials distinguish younger and older patients with Parkinson’s disease. J Neural Trans 103:1053–1067CrossRef

Berisha F, Feke GT, Trempe CL et al (2007) Retinal abnormalities in early Alzheimer’s disease. Invest Ophthalmol Vis Sci 48:2285–2289CrossRefPubMed

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

Blumenthal EZ, Williams JM, Weinreb RN et al (2000) Reproducibility of nerve fiber layer thickness measurements by use of optical coherence tomography. Ophthalmology 107:2278–2282CrossRefPubMed

Bobak P, Bodis-Wollner I, Harnois C et al (1983) Pattern electroretinograms and visual-evoked potentials in glaucoma and multiple sclerosis. Am J Ophthalmol 96:72–83PubMed

Bodis-Wollner I (1972) Visual acuity and contrast sensitivity in patients with cerebral lesions. Science 178:769–771CrossRefPubMed

Bodis-Wollner I (1990) Visual deficit related to dopamine deficiency in experimental animals and Parkinson’s disease. Trends Neurosci 13:296–301CrossRefPubMed

Bodis-Wollner I (2008) Diagnosing and treating early: is there a pre-cardinal stage of Parkinson disease? Parkinson Rep 19:9–10

Bodis-Wollner I, Diamond S (1976) The measurement of spatial contrast sensitivity in cases of blurred vision associated with cerebral lesions. Brain 99:695–710CrossRefPubMed

Bodis-Wollner I, Tzelepi A (1998) The push-pull action of dopamine on spatial tuning of the monkey retina: the effects of dopaminergic deficiency and selective D1 and D2 receptor ligands on the pattern electroretinogram. Vision Res 38:1479–1487CrossRefPubMed

Bodis-Wollner I, Tzelepi A (2002) Push-pull model of Dopamine’s action in the retina in: models of the visual system. Hung GK, Ciuffreda KJ (eds) Kluwer Academic/Plenum Publishers, New York, Boston, Dordrecht, London, Moscow. Chapter 5, pp 191–214

Bodis-Wollner I, Tzelepi A (2005) The effect of diverse dopamine receptors on spatial processing in the central retina: a model. Chapter 17. In: Jenkin M, Harris L (eds) Seeing spatial form. Oxford University Press, New York, NY

Bodis-Wollner I, Yahr MD (1978) Measurement of visual evoked potentials in Parkinson’s disease. Brain 101:661–671CrossRefPubMed

Bodis-Wollner I, Marx MS, Mitra S et al (1987) Visual dysfunction in Parkinsons disease. Brain 110:1675–1698CrossRefPubMed

Bodis-Wollner I, Brannan JR, Storch RL, Hajee M, Minko M (2009) The effect of background spatial contrast on electroretinographic responses in the human retina. Vision Res 49(9):922–930CrossRefPubMed

Bodis-Wollner I, Yahr MD, Mylin LH, Thornton J (1982) Dopaminergic deficiency and delayed visual evoked potentials in humans. Ann Neurol 11:478–483CrossRefPubMed

Braak H, Del Tredici K, Bratzke H et al (2002) Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson’s disease (preclinical and clinical stages). J Neurol 249:1–5CrossRef

Bulens C, Meerwaldt JD, van der Wildt GJ, Keemink CJ (1986) Contrast sensitivity in Parkinson’s disease. Neurology 36:1121–1125PubMed

Buttner T, Kuhn W, Muller T, Heinze T, Puhl C, Przuntek H (1996) Chromatic and achromatic visual evoked potentials in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 100:443–447PubMed

Dacey DM (1988) Dopamine-accumulating retinal neurons revealed by in vitro fluorescence display a unique morphology. Science 240(4856):1196–1198CrossRefPubMed

Davenport CM, Detwiler PB, Dacey DM (2007) Functional polarity of dendrites and axons of primate A1 amacrine cells. Vis Neurosci 24:449–457CrossRefPubMed

Djamgoz MB, Hankins MW, Hirano J et al (1997) Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vision Res 37:3509–3529CrossRefPubMed

Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187(3):517–552PubMed

Frederick JM, Rayborn ME, Laties AM, Lam DM, Hollyfield JG (1982) Dopaminergic neurons in the human retina. J Comp Neurol 210(1):65–79CrossRefPubMed

Ghilardi MF, Bodis-Wollner I, Onofrj MC et al (1988) Spatial frequency dependent abnormalities of the pattern electroretinogram and visual evoked potentials in a parkinsonian monkey model. Brain 3:131–184CrossRef

Ghilardi MF, Marx MS, Bodis-Wollner I et al (1989) The effect of intraocular 6-hydroxydopamine on retinal processing of primates. Ann Neurol 25:357–364CrossRefPubMed

Hajee M, March W, Lazzaro D, Wolintz A, Shrier E, Glazman S, Bodis-Wollner I (2009) Inner retinal layer thinning in Parkinson disease. Arch Ophthalmol 127(6):737–741CrossRefPubMed

Hampson EC, Vaney DI, Weiler R (1992) Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J Neurosci 12:4911–4922PubMed

Harnois C, DiPaolo T (1990) Decreased dopamine in the retinas of patients with Parkinsons disease. Invest Ophthalmol Vis Sci 31:2473–2475PubMed

Hollander H, Bisti S, Maffei L, Hebel R (1984) Electroretinographic responses and anterograde changes of morphology after intercranial optic nerve section. A quantitative analysis in the cat. Exp Brain Res 5:483–493

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

Ikeda H, Head GM, Ellis CJ (1994) Electrophysiological signs of retinal dopamine deficiency in recently diagnosed Parkinson’s disease and a follow up study. Vision Res 34:2629–2638CrossRefPubMed

Inzelberg R, Ramirez JA, Nisipeanu P et al (2004) Retinal nerve fiber layer thinning in Parkinson disease. Vision Res 44:2793–2797CrossRefPubMed

Krizaj D, Gábriel R, Owen WG, Witkovsky P (1988) Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. J Comp Neurol 398(4):529–538CrossRef

Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 1:37–68

Maffei L, Fiorentini A, Bisti S, Hollander H (1985) Pattern ERG in the monkey after section of the optic nerve. Exp Brain Res 59:423–425CrossRefPubMed

Marx M, Bodis-Wollner I, Bobak P, Harnois C (1986) Temporal frequency-dependent VEP changes in Parkinson’s disease. Vision Res 26:185–193CrossRefPubMed

Masson G, Mestre D, Blin O (1993) Dopaminergic modulation of visual sensitivity in man. Fundam Clin Pharmacol 7(8):449–463CrossRefPubMed

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(2):137–144CrossRefPubMed

Nguyen-Legros J, Simon A, Caillé I, Bloch B (1997) Immunocytochemical localization of dopamine D1 receptors in the retina of mammals. Vis Neurosci 14(3):545–551CrossRefPubMed

Nguyen-Legros J, Versaux-Botteri C, Vernier P (1999) Dopamine receptor localization in the mammalian retina. Mol Neurobiol 19(3):181–204CrossRefPubMed

Onofrj M, Bodis-Wollner I (1982) Dopaminergic deficiency causes delayed VEPs in rats. Ann Neurol 11:484–490CrossRefPubMed

Onofrj M, Ghilardi MF, Basciani M, Gambi D (1986) Visual evoked potentials in parkinsonism and dopamine blockade reveal a stimulus-dep endent dopamine function in humans. J Neurol Neurosurg Psychiatry 49(10):1150–1159CrossRefPubMed

Peppe A, Antal A, Tagliati M, Stanzione P, Bodis-Wollner I (1998a) Dl agonist CY208–243 attenuates the PERG to low spatial frequency stimuli in the monkey. Neurosci Lett 242:1–4CrossRef

Peppe A, Stanzione P, Pierantozzi M, Semprini R, Bassi A, Santilli AM, Formisano R, Piccolino M, Bernardi G (1998b) Does pattern electroretinogram spatial tuning alteration in Parkinson’s disease depend on motor disturbances or retinal dopaminergic loss? Electroencephalogr Clin Neurophysiol 106(4):374–382CrossRefPubMed

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

Regan D, Maxner C (1987) Orientation-selective visual loss in patients with Parkinson’s disease. Brain 110(Pt 2):415–432CrossRefPubMed

Regan D, Neima D (1984) Low-contrast letter charts in early diabetic retinopathy, ocular hypertension, glaucoma, and Parkinson’s disease. Br J Ophthalmol 68(12):885–889CrossRefPubMed

Sartucci F, Orlandi G, Lucetti C et al (2003) Changes in pattern electroretinograms to equiluminant red-green and blue-yellow gratings in patients with early Parkinson’s disease. J Clin Neurophysiol 20:375–381CrossRefPubMed

Schulman JS, Pedut-Kloizman T, Hertzmark E et al (1996) Reproducibility of nerve fiber layer thickness measurements using optical coherence tomography. Ophthalmology 103:1889–1898

Silva MF, Faria P, Regateiro FS, Forjaz V, Januário C, Freire A, Castelo-Branco M (2005) Independent patterns of damage within magno-, parvo- and koniocellular pathways in Parkinson’s disease. Brain 128:2260–2271CrossRefPubMed

Skirboll LR, Grace AA, Bunney BS (1977) Dopamine auto- and postsynaptic receptors: electrophysiological evidence for differential sensitivity to dopamine agonists. Science 206:80–82CrossRef

Stanzione P, Pierantozzi M, Semprini R, Tagliati M, Traversa R, Peppe A et al (1995) Increasing doses of l-sulpiride reveal dose- and spatial frequency-dependent effects of D2 selective blockade in the human electroretinogram. Vision Res 35:2659–2664CrossRefPubMed

Tagliati M, Bodis-Wollner I, Yahr MD (1996) The pattern electroretinogram in Parkinson’s disease reveals lack of retinal spatial tuning. Electroencephalogr Clin Neurophysiol 100:1–11CrossRefPubMed

Tagliati M, Bodis-Wollner I, Kovanecz I, Stanzione P (1994) Spatial frequency tuning of the monkey pattern ERG depends on D2 receptor-linked action of dopamine. Vision Res 34:2051–2057CrossRefPubMed

Tartaglione A, Pizio N, Bino G, Spadavecchia L, Favale E (1984) VEP changes in Parkinson’s disease are stimulus dependent. J Neurol Neurosurg Psychiatry 47(3):305–307CrossRefPubMed

Tartaglione A, Oneto A, Bandini F, Favale E (1987) Visual evoked potentials and pattern electroretinograms in Parkinson’s disease and control subjects. J Neurol Neurosurg Psychiatry 50(9):1243–1244CrossRefPubMed

Valenti DA (2007) Neuroimaging of retinal nerve fiber layer in AD using optical coherence tomography. Neurology 69:1060CrossRefPubMed

Witkovsky P (2004) Dopamine and retinal function. Doc Ophthalmol 108:17–39CrossRefPubMed

Witkovsky P, Gabriel R, Krizaj D, Akopian A (1995) Feedback from luminosity horizontal cells mediates depolarizing responses of chromaticity horizontal cells in the Xenopus retina. Proc Natl Acad Sci USA 92(8):3556–3560CrossRefPubMed

Wojtkowski M, Srinivasan V, Fujimoto J et al (2005) Three-dimensional retinal imaging with high speed ultrahigh resolution optical coherence tomography. Ophthalmology 112:1734–1746CrossRefPubMed

Yavas GF, Yilmaz O, Küsbeci T, Oztürk F (2007) The effect of levodopa and dopamine agonists on optic nerve head in Parkinson disease. Eur J Ophthalmol 17:812–816PubMed

Title: Retinopathy in Parkinson disease
Author: Ivan Bodis-Wollner
Publication date: 01-11-2009
Publisher: Springer Vienna
Published in: Journal of Neural Transmission / Issue 11/2009
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-009-0292-z

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Retinopathy in Parkinson disease

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