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The intrinsically restructured fovea is correlated with contrast sensitivity loss in Parkinson’s disease

  • Neurology and Preclinical Neurological Studies - Original Article
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Abstract

Foveal structure that is specified by the thickness, depth and the overall shape of the fovea is a promising tool to qualify and quantify retinal pathology in Parkinson’s disease. To determine the model variable that is best suited for discriminating Parkinson’s disease eyes from those of healthy controls and to assess correlations between impaired contrast sensitivity and foveal shape we characterized the fovea in 48 Parkinson’s disease patients and 45 control subjects by optical coherence tomography (OCT). The model quantifies structural changes in the fovea of Parkinson’s disease patients that are correlated with a decline in contrast sensitivity. Retinal foveal remodeling may serve as a parameter for vision deficits in Parkinson’s disease. Whether foveal remodeling reflects dopaminergic driven pathology or rather both dopaminergic and non-dopaminergic pathology has to be investigated in longitudinal studies.

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References

  • Adam CR, Shrier E, Ding Y et al (2013) Correlation of inner retinal thickness evaluated by spectral-domain optical coherence tomography and contrast sensitivity in Parkinson disease. J Neuroophthalmol 33:137–142

    Article  Google Scholar 

  • Bhaskar PA, Vanchilingam S, Bhaskar EA et al (1986) Effect of L-dopa on visual evoked potential in patients with Parkinson’s disease. Neurology 36:1119–1121

    Article  CAS  Google Scholar 

  • Bodis-Wollner I (1972) Visual acuity and contrast sensitivity in patients with cerebral lesions. Science 178:769–771. https://doi.org/10.1126/science.178.4062.769

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bodis-Wollner I, Marx MS, Mitra S et al (1987) Visual dysfunction in Parkinson’s disease. Loss in spatiotemporal contrast sensitivity. Brain 110(Pt 6):1675–1698

    Article  Google Scholar 

  • Bodis-Wollner I, Miri S, Glazman S (2013) Venturing into the no-man’s land of the retina in Parkinson’s disease. Mov Disord 29:15–22

    Article  Google Scholar 

  • Bodis-Wollner I, Kozlowski PB, Glazman S, Miri S (2014) Alpha-synuclein in the inner retina in Parkinson disease. Ann Neurol 75(6):964–966

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Buttner T, Kuhn W, Muller T et al (1996) Chromatic and achromatic visual evoked potentials in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 100:443–447

    Article  CAS  Google Scholar 

  • Chorostecki J, Seraji-Bozorgzad N, Shah A et al (2015) Characterization of retinal architecture in Parkinson’s disease. J Neurol Sci 355:44–48. https://doi.org/10.1016/j.jns.2015.05.007

    Article  PubMed  Google Scholar 

  • Delalande I, Hache JC, Forzy G et al (1998) Do visual-evoked potentials and spatiotemporal contrast sensitivity help to distinguish idiopathic Parkinson’s disease and multiple system atrophy? Mov Disord 13:446–452

    Article  CAS  Google Scholar 

  • Ding Y, Spund B, Glazman S et al (2014) Application of an OCT data-based mathematical model of the foveal pit in Parkinson disease. J Neural Transm 121:1367–1376

    Article  Google Scholar 

  • Firsov ML, Astakhova LA (2016) The role of dopamine in controlling retinal photoreceptor function in vertebrates. Neurosci Behav Physiol 46:138–145. https://doi.org/10.1007/s11055-015-0210-9

    Article  CAS  Google Scholar 

  • Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752

    Article  CAS  Google Scholar 

  • Guo L, Normando EM, Shah PA et al (2018) Oculo-visual abnormalities in Parkinson’s disease: possible value as biomarkers. Mov Disord 33:1390–1406. https://doi.org/10.1002/mds.27454

    Article  PubMed  Google Scholar 

  • Hajee ME, March WF, Lazzaro DR et al (2009) Inner retinal layer thinning in Parkinson disease. Arch Ophthalmol 127:737–741

    Article  Google Scholar 

  • 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 

  • Hasbi A, O’Dowd BF, George SR (2011) Dopamine D1–D2 receptor heteromer signaling pathway in the brain: emerging physiological relevance. Mol Brain 4:26. https://doi.org/10.1186/1756-6606-4-26

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Inzelberg R, Ramirez JA, Nisipeanu P, Ophir A (2004) Retinal nerve fiber layer thinning in Parkinson disease. Vis Res 44:2793–2797

    Article  Google Scholar 

  • Müller A-K, Blasberg C, Südmeyer M et al (2014) Photoreceptor layer thinning in parkinsonian syndromes. Mov Disord 29:1222–1223

    Article  Google Scholar 

  • Nieves-Moreno M, Martínez-de-la-Casa JM, Morales-Fernández L et al (2018) Impacts of age and sex on retinal layer thicknesses measured by spectral domain optical coherence tomography with Spectralis. PLoS ONE 13:1–9. https://doi.org/10.1371/journal.pone.0194169

    Article  CAS  Google Scholar 

  • Nightingale S, Mitchell KW, Howe JW (1986) Visual evoked cortical potentials and pattern electroretinograms in Parkinson’s disease and control subjects. J Neurol Neurosurg Psychiatry 49:1280–1287

    Article  CAS  Google Scholar 

  • Ridder A, Müller MLTM, Kotagal V et al (2017) Impaired contrast sensitivity is associated with more severe cognitive impairment in Parkinson disease. Parkinsonism Relat Disord 34:15–19

    Article  CAS  Google Scholar 

  • Schneider M, Müller H-P, Lauda F et al (2014) Retinal single-layer analysis in Parkinsonian syndromes: an optical coherence tomography study. J Neural Transm 121:41–47

    Article  Google Scholar 

  • Slotnick S, Ding Y, Glazman S et al (2015) A novel retinal biomarker for Parkinson’s disease: quantifying the foveal pit with optical coherence tomography. Mov Disord 30(12):1692–1695

    Article  Google Scholar 

  • Spund B, Ding Y, Liu T et al (2013) Remodeling of the fovea in Parkinson disease. J Neural Transm 120(5):745–753

    Article  CAS  Google Scholar 

  • Stanzione P, Bodis-Wollner I, Pierantozzi M et al (1999) A mixed D1 and D2 antagonist does not replay pattern electroretinogram alterations observed with a selective D2 antagonist in normal humans: relationship with Parkinson’s disease pattern electroretinogram alterations. Clin Neurophysiol 110:82–85

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tan JMM, Wong ESP, Lim K-L (2009) Protein misfolding and aggregation in Parkinson’s disease. Antioxid Redox Signal 11:2119–2134. https://doi.org/10.1089/ars.2009.2490

    Article  CAS  PubMed  Google Scholar 

  • Terry L, Cassels N, Lu K et al (2016) Using spectral domain optical coherence tomography : evaluation of inter-session repeatability and agreement between devices. PLoS ONE. https://doi.org/10.1371/journal.pone.0162001

    Article  PubMed  PubMed Central  Google Scholar 

  • Turcano P, Chen JJ, Bureau BL, Savica R (2018) Early ophthalmologic features of Parkinson’s disease: a review of preceding clinical and diagnostic markers. J Neurol. https://doi.org/10.1007/s00415-018-9051-0

    Article  PubMed  Google Scholar 

  • Watson AB, Barlow HB, Robson JG (1983) What does the eye see best? Nature 302:419–422. https://doi.org/10.1038/302419a0

    Article  CAS  PubMed  Google Scholar 

  • Young JB, Godara P, Williams V et al (2019) Assessing retinal structure in patients with Parkinson disease. J Neurol Neurophysiol. https://doi.org/10.4172/2155-9562.1000485

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

A. Markopoulou from NorthShore University Health System, Evanston IL, USA participated in the study. Due to methodological reasons only the measurements from Ulm University were used for the final evaluation of the data.

Funding

The research was supported by the Michael J. Fox Foundations for Parkinson’s Research.

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Correspondence to Ivan Bodis-Wollner.

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All authors have no conflicts of interest and no competing interests.

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All procedures performed were in accordance with the ethical standards of the institutional research committees of the University of Ulm (36/13), the Institutional Review Board (IRB) of NorthShore University HealthSystem (EH13-077) and the SUNY Downstate Medical Center Institutional Review Board (418805) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Written informed consent was obtained from each subject.

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Pinkhardt, E.H., Ding, Y., Slotnick, S. et al. The intrinsically restructured fovea is correlated with contrast sensitivity loss in Parkinson’s disease. J Neural Transm 127, 1275–1283 (2020). https://doi.org/10.1007/s00702-020-02224-9

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  • DOI: https://doi.org/10.1007/s00702-020-02224-9

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