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Decoding PERG: a Neuro-Ophthalmic Retinal Ganglion Cell Function Review

  • Pedro MonsalveEmail author
Retina (R Goldhardt, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Retina

Abstract

Purpose of Review

Currently, the clinical evaluation of neuro-ophthalmologic diseases is mainly focused on identifying stages where structural or functional damage occurs. Recognition of retinal ganglion cell (RGC) functional patterns as well as monitoring RGC dysfunction can be performed using steady-state pattern electroretinogram (PERG). The analysis of the amplitude and latency shift aids on providing information on early damage or monitoring of the RGC, allowing for prompt clinical intervention and management modification, potentially changing the natural history of the disease. The purpose of this article is to review the latest findings in PERG, in early manifest glaucoma, non-arteritic ischemic optic neuropathy, multiple sclerosis with unilateral recovered optic neuritis, and its fellow eyes.

Recent Findings

The steady-state PERG responses provide new and early specific information in neuro-ophthalmic diseases affecting the inner retina.

Summary

Steady-state PERG presents specific amplitude and latency outcomes based on the neuro-ophthalmic disease affecting the inner retina, allowing early recognition of changes at the level of RGC and the degree of RGC dysfunction. In addition, PERG alterations may be induced in healthy subjects as well as susceptible eyes using different stress tests such as head-down tilting or water-drinking tests.

Keywords

Retinal ganglion cell function Non-arteritic ischemic optic neuropathy (NAION) Multiple sclerosis Optic neuritis Glaucoma Steady-state PERG 

Notes

Funding Information

Supported by NIH Center Core Grant R43EY023460 and Research to Prevent Blindness Unrestricted Grant.

Compliance With Ethical Standards

Conflict of Interest

Pedro Monsalve declares that he has no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Porciatti V. Electrophysiological assessment of retinal ganglion cell function. Exp Eye Res. 2015;141:164–70.  https://doi.org/10.1016/j.exer.2015.05.008.Google Scholar
  2. 2.
    Porciatti V, Ventura LM. The PERG as a tool for early detection and monitoring of glaucoma. Current Ophthalmology Reports. 2017;5(1):7–13.  https://doi.org/10.1007/s40135-017-0128-1.Google Scholar
  3. 3.
    Holder GE. Pattern electroretinography (PERG) and an integrated approach to visual pathway diagnosis. Prog Retin Eye Res. 2001;20(4):531–61.Google Scholar
  4. 4.
    Bach M, Brigell MG, Hawlina M, Holder GE, Johnson MA, McCulloch DL, et al. ISCEV standard for clinical pattern electroretinography (PERG): 2012 update. Doc Ophthalmol. 2013;126(1):1–7.  https://doi.org/10.1007/s10633-012-9353-y.Google Scholar
  5. 5.
    Hood DC, Xu L, Thienprasiddhi P, Greenstein VC, Odel JG, Grippo TM, et al. The pattern electroretinogram in glaucoma patients with confirmed visual field deficits. Invest Ophthalmol Vis Sci. 2005;46(7):2411–8.  https://doi.org/10.1167/iovs.05-0238.Google Scholar
  6. 6.
    •• Monsalve P, Triolo G, Toft-Nielsen J, Bohorquez J, Henderson AD, Delgado R, et al. Next generation PERG method: expanding the response dynamic range and capturing response adaptation. Transl Vis Sci Technol, This study compares the new steady state PERG method to a previously validated PERG method. 2017;6(3):5.  https://doi.org/10.1167/tvst.6.3.5.
  7. 7.
    •• Monsalve P, Ren S, Triolo G, Vazquez L, Henderson AD, Kostic M, et al. Steady-state PERG adaptation: a conspicuous component of response variability with clinical significance. Doc Ophthalmol. 2018;136(3):157–64.  https://doi.org/10.1007/s10633-018-9633-2 This study describes the within test variability of the steady state PERG reponse and describes its significant physiological and clinical implications.Google Scholar
  8. 8.
    Porciatti V, Sartucci F. Retinal and cortical evoked responses to chromatic contrast stimuli. Specific losses in both eyes of patients with multiple sclerosis and unilateral optic neuritis. Brain. 1996;119(Pt 3):723–40.Google Scholar
  9. 9.
    Jansonius NM, Kooijman AC. The effect of defocus on edge contrast sensitivity. Ophthalmic Physiol Opt. 1997;17(2):128–32.Google Scholar
  10. 10.
    Digre KB, Evangelou N, Konz D, Esiri MM, et al. Size-selective neuronal changes in the anterior optic pathways suggest a differential susceptibility to injury in multiple sclerosis. J Neuroophthalmol. 2002;22(2):143.  https://doi.org/10.1097/00041327-200206000-00040.Google Scholar
  11. 11.
    Centofanti M, Fogagnolo P, Oddone F, Orzalesi N, Vetrugno M, Manni G, et al. Learning effect of Humphrey matrix frequency doubling technology perimetry in patients with ocular hypertension. J Glaucoma. 2008;17(6):436–41.  https://doi.org/10.1097/IJG.0b013e31815f531d.Google Scholar
  12. 12.
    Porciatti V, Sorokac N, Buchser W. Habituation of retinal ganglion cell activity in response to steady state pattern visual stimuli in normal subjects. Invest Ophthalmol Vis Sci. 2005;46(4):1296–302.  https://doi.org/10.1167/iovs.04-1242.Google Scholar
  13. 13.
    Porciatti V, Ventura LM. Adaptive changes of inner retina function in response to sustained pattern stimulation. Vis Res. 2009;49(5):505–13.  https://doi.org/10.1016/j.visres.2008.12.001.Google Scholar
  14. 14.
    Porciatti V, Bosse B, Parekh PK, Shif OA, Feuer WJ, Ventura LM. Adaptation of the steady-state PERG in early glaucoma. J Glaucoma. 2014;23(8):494–500.  https://doi.org/10.1097/IJG.0b013e318285fd95.Google Scholar
  15. 15.
    Bach M. Electrophysiological approaches for early detection of glaucoma. Eur J Ophthalmol. 2001;11(Suppl 2):S41–9.Google Scholar
  16. 16.
    Trick GL. Retinal potentials in patients with primary open-angle glaucoma: physiological evidence for temporal frequency tuning deficits. Invest Ophthalmol Vis Sci. 1985;26(12):1750–8.Google Scholar
  17. 17.
    Hattenhauer MG, Leavitt JA, Hodge DO, Grill R, Gray DT. Incidence of nonarteritic anteripr ischemic optic neuropathy. Am J Ophthalmol. 1997;123(1):103–7.  https://doi.org/10.1016/s0002-9394(14)70999-7.Google Scholar
  18. 18.
    Parisi V, Gallinaro G, Ziccardi L, Coppola G. Electrophysiological assessment of visual function in patients with non-arteritic ischaemic optic neuropathy. Eur J Neurol. 2008;15(8):839–45.  https://doi.org/10.1111/j.1468-1331.2008.02200.x.Google Scholar
  19. 19.
    Kidd DP, Plant GT. Chapter 6 Optic Neuritis. Blue Books of Neurology. 2008. p. 134–52.Google Scholar
  20. 20.
    Plant GT. Optic neuritis and multiple sclerosis. Curr Opin Neurol. 2008;21(1):16–21.  https://doi.org/10.1097/WCO.0b013e3282f419ca.Google Scholar
  21. 21.
    Petzold A, Wattjes MP, Costello F, Flores-Rivera J, Fraser CL, Fujihara K, et al. The investigation of acute optic neuritis: a review and proposed protocol. Nat Rev Neurol. 2014;10(8):447–58.  https://doi.org/10.1038/nrneurol.2014.108.Google Scholar
  22. 22.
    Szilasiová J, Klímová E, Veselá D. Optic neuritis as the first sign of multiple sclerosis. Cesk Slov Oftalmol. 2002;58(4):259–64.Google Scholar
  23. 23.
    Lizrova Preiningerova J, Grishko A, Sobisek L, Andelova M, Benova B, Kucerova K, et al. Do eyes with and without optic neuritis in multiple sclerosis age equally? Neuropsychiatr Dis Treat. 2018;14:2281–5.  https://doi.org/10.2147/NDT.S169638.Google Scholar
  24. 24.
    Hokazono K, Raza AS, Oyamada MK, Hood DC, Monteiro MLR. Pattern electroretinogram in neuromyelitis optica and multiple sclerosis with or without optic neuritis and its correlation with FD-OCT and perimetry. Doc Ophthalmol. 2013;127(3):201–15.  https://doi.org/10.1007/s10633-013-9401-2.Google Scholar
  25. 25.
    Klistorner A, Sriram P, Vootakuru N, Wang C, Barnett MH, Garrick R, et al. Axonal loss of retinal neurons in multiple sclerosis associated with optic radiation lesions. Neurology. 2014;82(24):2165–72.  https://doi.org/10.1212/WNL.0000000000000522.Google Scholar
  26. 26.
    Akçam HT, Capraz IY, Aktas Z, Batur Caglayan HZ, Ozhan Oktar S, Hasanreisoglu M, et al. Multiple sclerosis and optic nerve: an analysis of retinal nerve fiber layer thickness and color Doppler imaging parameters. Eye. 2014;28(10):1206–11.  https://doi.org/10.1038/eye.2014.178.Google Scholar
  27. 27.
    Janaky M, Janossy A, Horvath G, Benedek G, Braunitzer G. VEP and PERG in patients with multiple sclerosis, with and without a history of optic neuritis. Documenta ophthalmologica Advances in ophthalmology. 2017;134(3):185–93.  https://doi.org/10.1007/s10633-017-9589-7.Google Scholar
  28. 28.
    Rodriguez-Mena D, Almarcegui C, Dolz I, Herrero R, Bambo MP, Fernandez J, et al. Electropysiologic evaluation of the visual pathway in patients with multiple sclerosis. J Clin Neurophysiol. 2013;30(4):376–81.  https://doi.org/10.1097/WNP.0b013e31829d75f7.Google Scholar
  29. 29.
    Fraser CL, Holder GE. Electroretinogram findings in unilateral optic neuritis. Documenta ophthalmologica Advances in ophthalmology. 2011;123(3):173–8.  https://doi.org/10.1007/s10633-011-9294-x.Google Scholar
  30. 30.
    Parisi V, Manni G, Spadaro M, Colacino G, Restuccia R, Marchi S, et al. Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest Ophthalmol Vis Sci. 1999;40(11):2520–7.Google Scholar
  31. 31.
    Falsini B, Porrello G, Porciatti V, Fadda A, Salgarello T, Piccardi M. The spatial tuning of steady state pattern electroretinogram in multiple sclerosis. Eur J Neurol. 1999;6(2):151–62.Google Scholar
  32. 32.
    Falsini B, Porciatti V. The temporal frequency response function of pattern ERG and VEP: changes in optic neuritis. Electroencephalogr Clin Neurophysiol. 1996;100(5):428–35.Google Scholar
  33. 33.
    •• Monsalve P, Ren S, Jiang H, Wang J, Kostic M, Gordon P, et al. Retinal ganglion cell function in recovered optic neuritis: faster is not better. Clin Neurophysiol, This study describes the steady state PERG response in patients with multiple sclerosis and recovered optice neuritis. 2018;129(9):1813–8.  https://doi.org/10.1016/j.clinph.2018.06.012.
  34. 34.
    Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90(3):262–7.  https://doi.org/10.1136/bjo.2005.081224.Google Scholar
  35. 35.
    Porciatti V, Ventura LM. Retinal ganglion cell functional plasticity and optic neuropathy: a comprehensive model. J Neuroophthalmol. 2012;32(4):354–8.  https://doi.org/10.1097/WNO.0b013e3182745600.Google Scholar
  36. 36.
    Banitt MR, Ventura LM, Feuer WJ, Savatovsky E, Luna G, Shif O, et al. Progressive loss of retinal ganglion cell function precedes structural loss by several years in glaucoma suspects. Invest Ophthalmol Vis Sci. 2013;54(3):2346–52.  https://doi.org/10.1167/iovs.12-11026.Google Scholar
  37. 37.
    Karaśkiewicz J, Drobek-Słowik M, Lubiński W. Pattern electroretinogram (PERG) in the early diagnosis of normal-tension preperimetric glaucoma: a case report. Doc Ophthalmol. 2013;128(1):53–8.  https://doi.org/10.1007/s10633-013-9414-x.Google Scholar
  38. 38.
    Bach M, Hoffmann MB. Update on the pattern electroretinogram in glaucoma. Optom Vis Sci. 2008;85(6):386–95.  https://doi.org/10.1097/OPX.0b013e318177ebf3.Google Scholar
  39. 39.
    Ventura LM, Porciatti V, Ishida K, Feuer WJ, Parrish RK 2nd. Pattern electroretinogram abnormality and glaucoma. Ophthalmology. 2005;112(1):10–9.  https://doi.org/10.1016/j.ophtha.2004.07.018.Google Scholar
  40. 40.
    Bode SF, Jehle T, Bach M. Pattern electroretinogram in glaucoma suspects: new findings from a longitudinal study. Invest Ophthalmol Vis Sci. 2011;52(7):4300–6.  https://doi.org/10.1167/iovs.10-6381.Google Scholar
  41. 41.
    Porciatti V, Feuer WJ, Monsalve P, Triolo G, Vazquez L, McSoley J, et al. Head-down posture in glaucoma suspects induces changes in IOP, systemic pressure, and PERG that predict future loss of optic nerve tissue. J Glaucoma. 2017;26(5):459–65.  https://doi.org/10.1097/ijg.0000000000000648.Google Scholar
  42. 42.
    Fadda A, Di Renzo A, Martelli F, Marangoni D, Batocchi AP, Giannini D, et al. Reduced habituation of the retinal ganglion cell response to sustained pattern stimulation in multiple sclerosis patients. Clin Neurophysiol. 2013;124(8):1652–8.  https://doi.org/10.1016/j.clinph.2013.03.001.Google Scholar
  43. 43.
    Yücel YH. Loss of neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus in glaucoma. Arch Ophthalmol. 2000;118(3):378–84.  https://doi.org/10.1001/archopht.118.3.378.Google Scholar
  44. 44.
    La Morgia C, Di Vito L, Carelli V, Carbonelli M. Patterns of retinal ganglion cell damage in neurodegenerative disorders: parvocellular vs magnocellular degeneration in optical coherence tomography studies. Front Neurol. 2017;8.  https://doi.org/10.3389/fneur.2017.00710.
  45. 45.
    Gameiro G, Monsalve P, Golubev I, Ventura L, Porciatti V. Neurovascular changes associated with the water drinking test. J Glaucoma. 2018;27(5):429–32.  https://doi.org/10.1097/IJG.0000000000000898.Google Scholar
  46. 46.
    Trick GL, Nesher R, Cooper DG, Shields SM. The human pattern ERG: alteration of response properties with aging. Optom Vis Sci. 1992;69(2):122–8.Google Scholar
  47. 47.
    Porciatti V, Burr DC, Morrone MC, Fiorentini A. The effects of aging on the pattern electroretinogram and visual evoked potential in humans. Vis Res. 1992;32(7):1199–209.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Bascom Palmer Eye Institute, Department of OphthalmologyUniversity of Miami Miller School of MedicineMiamiUSA

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