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Open Access 01-10-2010 | Original research article

Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease

Authors: Kamila Krasodomska, Wojciech Lubiński, Andrzej Potemkowski, Krystyna Honczarenko

Published in: Documenta Ophthalmologica | Issue 2/2010

Abstract

Alzheimer’s disease (AD) is one of the most common causes of dementia in the world. Patients with AD frequently complain of vision disturbances that do not manifest as changes in routine ophthalmological examination findings. The main causes of these disturbances are neuropathological changes in the visual cortex, although abnormalities in the retina and optic nerve cannot be excluded. Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) tests are commonly used in ophthalmology to estimate bioelectrical function of the retina and optic nerve. The aim of this study was to determine whether retinal and optic nerve function, measured by PERG and PVEP tests, is changed in individuals in the early stages of AD with normal routine ophthalmological examination results. Standard PERG and PVEP tests were performed in 30 eyes of 30 patients with the early stages of AD. The results were compared to 30 eyes of 30 normal healthy controls. PERG and PVEP tests were recorded in accordance with the International Society for Clinical Electrophysiology of Vision (ISCEV) standards. Additionally, neural conduction was measured using retinocortical time (RCT)—the difference between P100-wave latency in PVEP and P50-wave implicit time in PERG. In PERG test, PVEP test, and RCT, statistically significant changes were detected. In PERG examination, increased implicit time of P50-wave (P < 0.03) and amplitudes reductions in P50- and N95-waves (P < 0.0001) were observed. In PVEP examination, increased latency of P100-wave (P < 0.0001) was found. A significant increase in RCT (P < 0.0001) was observed. The most prevalent features were amplitude reduction in N95-wave and increased latency of P100-wave which were seen in 56.7% (17/30) of the AD eyes. In patients with the early stages of AD and normal routine ophthalmological examination results, dysfunction of the retinal ganglion cells as well as of the optic nerve is present, as detected by PERG and PVEP tests. These dysfunctions, at least partially, explain the cause of visual disturbances observed in patients with the early stages of AD.

Lobo A, Launer LJ, Fratiglioni L, Andersen K, Di Carlo A, Breteler MM, Copeland JR, Dartigues JF, Jagger C, Martinez-Lage J, Soininen H, Hofman A (2000) Prevalence of dementia and major subtypes in Europe: a collaborative study of population-based cohorts. Neurologic diseases in the elderly research group. Neurology 54:4–9

Mendez MF, Mendez MA, Martin R, Smyth KA, Whitehouse PJ (1990) Complex visual disturbances in Alzheimer’s disease. Neurology 40:439–443PubMed

Holoryd S, Sphepherd ML (2001) Alzheimer’s disease: a review for the ophthalmologist. Surv Ophthalmol 45:516–524CrossRef

Sadun AA, Bassi CJ (1990) The visual system in Alzheimer’s disease. Res Publ Assoc Res Nerv Ment Dis 67:331–347PubMed

Katz B, Rimmer S (1989) Ophthalmologic manifestations of Alzheimer’s disease. Surv Ophthalmol 34:31–43CrossRefPubMed

Pelak VS, Hall DA (2004) Neuro-ophthalmic manifestations of neurodegenerative disease. Ophthalmol Clin North Am 17:311–320CrossRefPubMed

Fletcher WA (1994) Ophthalmological aspects of Alzheimer’s disease. Curr Opin Ophthalmol 5:38–44CrossRefPubMed

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

Hinton DR, Sadun AA, Blanks JC, Miller CA (1986) Optic-nerve degeneration in Alzheimer’s disease. N Engl J Med 315:485–487CrossRefPubMed

10.

Danesh-Meyer HV, Birch H, Ku JY, Carroll S, Gamble G (2006) Reduction of optic nerve fibers in patients with Alzheimer disease identified by laser imaging. Neurology 67:1852–1854CrossRefPubMed

11.

Syed AB, Armstrong RA, Smith CU (2005) A quantitative analysis of optic nerve axons in elderly control subjects and patients with Alzheimer’s disease. Folia Neuropathol 43:1–6PubMed

12.

Frederikse PH, Garland D, Zigler JS Jr, Piatigorsky J (1996) Oxidative stress increases production of beta-amyloid precursor protein and beta-amyloid (Abeta) in mammalian lenses, and Abeta has toxic effects on lens epithelial cells. J Biol Chem 271:10169–10174CrossRefPubMed

13.

Bruban J, Glotin AL, Dinet V, Chalour N, Sennlaub F, Jonet L, An N, Faussat AM, Mascarelli F (2009) Amyloid-beta(1–42) alters structure and function of retinal pigmented epithelial cells. Aging Cell 8:162–177CrossRefPubMed

14.

Townes-Anderson E, Vogt BA (1989) Distribution of muscarinic acetylcholine receptors on processes of isolated retinal cells. J Comp Neurol 290:369–383CrossRefPubMed

15.

Katz B, Rimmer S, Iragui V, Katzman R (1989) Abnormal pattern electroretinogram in Alzheimer’s disease: evidence for retinal ganglion cell degeneration? Ann Neurol 26:221–225CrossRefPubMed

16.

Trick GL, Barris MC, Bickler-Bluth M (1989) Abnormal pattern electroretinogram in patients with senile dementia of the Alzheimer type. Ann Neurol 26:226–231CrossRefPubMed

17.

Parisi V, Restuccia R, Fattapposta F, Mina C, Bucci MG, Pierelli F (2001) Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin Neurophysiol 112:1860–1867CrossRefPubMed

18.

Partanen J, Hartikainen P, Könönen M, Jousmäki V, Soinien H, Riekkinen P (1994) Prolonged latencies of pattern reversal visual evoked early potentials in Alzheimer disease. Alzheimer Dis Assoc Disord 8:250–258CrossRefPubMed

19.

Pollock VE, Schneider LS, Chui HC, Henderson V, Zemansky M, Sloane RB (1989) Visual evoked potentials in dementia: a meta-analysis and empirical study of Alzheimer’s disease patients. Biol Psychiatry 25:1003–1013CrossRefPubMed

20.

Grayson AS, Weiler EM, Sandman DE (1995) Visual evoked potentials in early Alzheimer’s dementia: an exploratory study. J Gen Psychol 122:113–129CrossRefPubMed

21.

Kergoat H, Kergoat MJ, Justino L, Chertkow H, Robillard A, Bergman H (2002) Visual retinocortical function in dementia of the Alzheimer’s type. Gerontology 48:197–203CrossRefPubMed

22.

Rizzo JF 3rd, Cronin-Golomb A, Growdon JH, Corkin S, Rosen TJ, Sandberg MA, Chiappa KH, Lessell S (1992) Retinocalcarine function in Alzheimer’s disease. A clinical and electrophysiological study. Arch Neurol 49:93–101PubMed

23.

Strenn K, Dal-Bianco P, Weghaupt H, Koch G, Vass C, Gottlob I (1991) Pattern electroretinogram and luminance electroretinogram in Alzheimer’s disease. J Neural Transm Suppl 33:73–80PubMed

24.

Iseri P, Altinaş Ö, Tokay T, Yűskel N (2006) Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease. J Neuro-Ophthalmol 26:18–24CrossRef

25.

Philpot MP, Amin D, Levy R (1990) Visual evoked potentials in Alzheimer’s disease: correlation with age and severity. Electroencephalogr Clin Neurophysiol 77:323–329CrossRefPubMed

26.

McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical Diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of the department of health and human services task force on Alzheimer’s disease. Neurology 34:939–944PubMed

27.

Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMed

28.

Celesia GG, Kaufman D (1985) Pattern ERGs and visual evoked potentials in maculopathies and optic nerve diseases. Invest Ophthalmol Vis Sci 26:726–735PubMed

29.

Celesia GG, Kaufman D, Cone SB (1986) Simultaneous recording of pattern electroretinography and visual evoked potentials in multiple sclerosis. A method to separate demyelination from axonal damage to the optic nerve. Arch Neurol 43:1247–1252PubMed

30.

Bach M, Hawlina M, Holder GE, Marmor MF, Meigen T, Vaegan, Miyake Y (2000) Standard for pattern electroretinography. Doc Ophthalmol 101:11–18

31.

Holder GE, Brigell MG, Hawlina M, Meigen T, Vaegan, Bach M (2007) ISCEV standard for clinical pattern electroretinography—2007 update. Doc Ophthalmol 114:111–116

32.

Odom JV, Bach M, Barber C, Brigell M, Marmor MF, Tormene AP, Holder GE, Vaegan (2004) Visual evoked potentials standard (2004). Doc Ophthalmol 108:115–123

33.

Odom JV, Bach M, Brigell M, Holder GH, McCulloch DL, Tormene AP, Vaegan (2010) ISCEV standard for clinical Visual Evoked Potentials Standard (2009 update). Doc Ophthalmol 120:111–119

34.

American Clinical Neurophysiology Society (2006) Guideline 5: guidelines for standard electrode position nomenclature. J Clin Neurophysiol 23:107–110CrossRef

35.

Holder GH (2006) The pattern electroretinogram. In: Heckenlively JR, Arden GB (eds) Principles and practice of clinical electrophysiology of vision, 2nd edn. MIT Press, Cambridge, pp 341–351

36.

Viswanathan S, Frishman LJ, Robson JG (2000) The uniform field and pattern ERG in macaques with experimental glaucoma: removal of spiking activity. Invest Ophthalmol Vis Sci 41:2797–2810PubMed

37.

Holder GH (2006) Localizing lesions in the visual system. In: Heckenlively JR, Arden GB (eds) Principles and practice of clinical electrophysiology of vision, 2nd edn. MIT Press, Cambridge, pp 505–517

38.

Eckstein MB, Spalton DJ, Holder G (1993) Visual loss from central serous retinopathy in systemic lupus erythematosus. Br J Ophthalmol 77:607–609CrossRefPubMed

39.

Lam BL (2005) Visual evoked potential. In: Lam BL (ed) Electrophysiology of vision. Clinical testing and applications, 1st edn. Taylor&Francis Group, Boca Raton, pp 123–135

40.

Bodis-Wollner I, Antal A (2006) Optic nerve and central nervous dysfunctions: Parkinson’s disease and multiple sclerosis. In: Heckenlively JR, Arden GB (eds) Principles and practice of clinical electrophysiology of vision, 2nd edn. MIT Press, Cambridge, pp 341–351

41.

Parisi V, Pernini C, Guinetti C, Neuschuler R, Bucci MG (1997) Electrophysiological assessment of visual pathways in glaucoma. Eur J Ophthalmol 7:229–235PubMed

42.

Löffler KU, Edward DP, Tso MO (1995) Immunoreactivity against tau, amyloid precursor protein, and beta-amyloid in the human retina. Invest Ophthalmol Vis Sci 36:24–31PubMed

43.

Liu B, Rasool S, Yang Z, Glabe CG, Schreiber SS, Ge J, Tan Z (2009) Amyloid-peptide vaccinations reduce {beta}-amyloid plaques but exacerbate vascular deposition and inflammation in the retina of Alzheimer’s transgenic mice. Am J Pathol 175:2099–2110CrossRefPubMed

44.

Melo JB, Agostinho P, Oliveira CR (2002) Amyloid beta-peptide 25–35 reduces [3H]acetylcholine release in retinal neurons. Involvement of metabolic dysfunction. Amyloid 9:221–228PubMed

45.

Aruoma OI, Jen SS, Watts HR, George J, Gentleman SM, Anderson PJ, Jen LS (2009) Acute and chronic effects of intravitreally injected beta-amyloid on the neurotransmitter system in the retina. Toxicology 256:92–100CrossRefPubMed

46.

Dimitrieva NA, Christianne ES, Kent TK (2007) Expression of alpha 7 nicotinic acetylcholine receptors by bipolar, amacrine, and ganglion cells of the rabbit retina. J Histochem Cytochem 55:461–476CrossRef

47.

Antal A, Kéri S, Bodis-Wollner I (1999) L-alpha-glycerylphosphorylcholine enhances the amplitude of the pattern electroretinogram in rhesus monkeys. A pilot study. Neurobiology 7:407–412PubMed

48.

Holl G, Straschill M, Thomsen T, Fischer JP, Kewitz H (1992) Effect of the cholinesterase inhibiting substance galanthamine on human EEG and visual evoked potentials. Electroencephalogr Clin Neurophysiol 82:445–452CrossRefPubMed

49.

Sannita WG, Balestra V, DiBon G, Marotta V, Rosadini G (1993) Human flash-VEP and quantitative EEG are independently affected by acute scopolamine. Electroencephalogr Clin Neurophysiol 86:275–282CrossRefPubMed

50.

Kergoat H, Kergoat KJ, Justino L, Chertkow H, Robillard A, Bergman H (2001) An evaluation of the retinal nerve fibre layer thickness by scanning laser polarimetry in individuals with dementia of the Alzheimer type. Acta Ophthalmol Scand 79:187–191CrossRefPubMed

Title: Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease
Authors: Kamila Krasodomska
Wojciech Lubiński
Andrzej Potemkowski
Krystyna Honczarenko
Publication date: 01-10-2010
Publisher: Springer-Verlag
Published in: Documenta Ophthalmologica / Issue 2/2010
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI: https://doi.org/10.1007/s10633-010-9238-x

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Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease

Abstract

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