Abstract
Purpose
The purpose of this study was to assess eye movements during a multifocal ERG (mfERG) recording. This study evaluated the relationship between bivariate contour ellipse areas (BCEAs), mfERG amplitudes (Amps) and mfERG implicit times (ITs) with repeat testing and experienced subjects.
Methods
Thirty subjects were selected (15 experienced to ocular procedures and 15 novices). All were confirmed to have healthy retinas and at least 20/25 vision. MfERGs with a stimulus near 100% contrast and 4-min m-sequence were recorded on two different days using our common clinical technique, which did not constrain the head. VERIS with fundus monitoring system was used for recording with a Burian-Allen electrode. An external camera captured the fundus during each mfERG recording. The optic nerve head position was tracked in each video using a custom algorithm in order to determine BCEAs. Each subject performed one mfERG on two different days. MfERGs were analyzed for Amps and ITs for the fovea and whole eye.
Results
There was no correlation between the mfERG metrics and BCEAs with repeat testing. There were also no differences between the experienced and novice subjects for mfERG Amps, ITs or BCEAs. Eye movements between visits were highly correlated (multiple r = 0.67). BCEAs were larger during mfERGs (1.04 ± 0.8 deg2) than those observed in previous literature using brief viewing tasks (< 0.3 deg2). The proportion of time spent fixating within 1.0 and 2.0 degrees of the central hexagon was 68 and 93%, respectively.
Conclusions
This study is the first to evaluate the stability of the retina while recording a mfERG in healthy subjects and indicates that the center of fixation during a mfERG stays within the central hexagon. Eye stability during an initial recording is the best indicator of stability on the second recording. The amount of movement during these recordings did not seem to affect the mfERG Amps or ITs. These data suggest clinical confidence with mfERGs when recording novice patients.
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Data availability
These data used in this study are available by the corresponding author upon reasonable request.
Code availability
Available upon request.
Complaince with ethical standards.
References
Hood DC, Odel JG, Chen CS, Winn BJ (2003) The multifocal electroretinogram. J Neuroophthalmol 23(3):225–235. https://doi.org/10.1097/00041327-200309000-00008
Sutter EE, Tran D (1992) The field topography of ERG components in man–I. Photopic Luminance Response Vision Res 32(3):433–446. https://doi.org/10.1016/0042-6989(92)90235-b
Chu PH, Chan HH, Leat SJ (2006) Effects of unsteady fixation on multifocal electroretinogram (mfERG). Graefes Arch Clin Exp Ophthalmol 244(10):1273–1282. https://doi.org/10.1007/s00417-006-0304-8
Simão S, Costa M, Sun JK, Cunha-Vaz J, Simó R (2017) Development of a normative database for multifocal electroretinography in the context of a multicenter clinical trial. Ophthalmic Res 57(2):107–117. https://doi.org/10.1159/000450958
Oyamada MK, Dotto PdF, Abdalla M (2007) Fatores técnicos intervenientes na realização do exame de eletrorretinograma multifocal (ERGmf). Arq Bras Oftalmol 70:713–717
Keating D, Parks S, Evans A (2000) Technical aspects of multifocal ERG recording. Doc Ophthalmol 100(2–3):77–98. https://doi.org/10.1023/a:1002723501303
Zhang B, Stevenson SS, Cheng H, Laron M, Kumar G, Tong J, Chino YM (2008) Effects of fixation instability on multifocal VEP (mfVEP) responses in amblyopes. J Vis 8(3):1611–1614
Chisholm JA, Keating D, Parks S, Evans AL (2001) The impact of fixation on the multifocal electroretinogram. Doc Ophthalmol 102(2):131–139. https://doi.org/10.1023/a:1017536625847
Henriques JF, Caseiro R, Martins P, Batista J (2015) High-speed tracking with kernelized correlation filters. IEEE Trans Pattern Anal Mach Intell 37(3):583–596. https://doi.org/10.1109/tpami.2014.2345390
Bradski G (2000) The OpenCV library. Dr Dobb’s J Softw Tools 25:120–125
Bellmann C, Feely M, Crossland MD, Kabanarou SA, Rubin GS (2004) Fixation stability using central and pericentral fixation targets in patients with age-related macular degeneration. Ophthalmology 111(12):2265–2270. https://doi.org/10.1016/j.ophtha.2004.06.019
Castet E, Crossland M (2012) Quantifying eye stability during a fixation task: a review of definitions and methods. See Perceiv 25(5):449–469. https://doi.org/10.1163/187847611X620955
Di Russo F, Pitzalis S, Spinelli D (2003) Fixation stability and saccadic latency in elite shooters. Vision Res 43(17):1837–1845. https://doi.org/10.1016/s0042-6989(03)00299-2
Rohrschneider K, Becker M, Schumacher N, Fendrich T, Volcker HE (1998) Normal values for fundus perimetry with the scanning laser ophthalmoscope. Am J Ophthalmol 126(1):52–58. https://doi.org/10.1016/s0002-9394(98)00065-8
Timberlake GT, Mainster MA, Peli E, Augliere RA, Essock EA, Arend LE (1986) Reading with a macular scotoma I retinal location of scotoma and fixation area. Invest Ophthalmol Vis Sci 27(7):1137–1147
Steinman RM (1965) Effect of target size, luminance, and color on monocular fixation*. J Opt Soc Am 55(9):1158–1164. https://doi.org/10.1364/JOSA.55.001158
Timberlake GT, Sharma MK, Grose SA, Gobert DV, Gauch JM, Maino JH (2005) Retinal location of the preferred retinal locus relative to the fovea in scanning laser ophthalmoscope images. Optom Vis Sci 82(3):177–185. https://doi.org/10.1097/01.opx.0000156311.49058.c8
Menz M, Sutter E, Menz M (2004) The effect of fixation instability on the multifocal VEP. Doc Ophthalmol 109(2):147–156. https://doi.org/10.1007/s10633-004-3790-1
Dunbar HM, Crossland MD, Rubin GS (2010) Fixation stability: a comparison between the Nidek MP-1 and the rodenstock scanning laser ophthalmoscope in persons with and without diabetic maculopathy. Invest Ophthalmol Vis Sci 51(8):4346–4350. https://doi.org/10.1167/iovs.09-4556
Rohrschneider K, Becker M, Kruse FE, Fendrich T, Völcker HE (1995) Stability of fixation: results of fundus-controlled examination using the scanning laser ophthalmoscope. Ger J Ophthalmol 4(4):197–202
Rohrschneider K, Becker M, Schumacher N, Fendrich T, Völcker HE (1998) Normal values for fundus perimetry with the scanning laser ophthalmoscope. Am J Ophthalmol 126(1):52–58. https://doi.org/10.1016/s0002-9394(98)00065-8
Fujii GY, de Juan E Jr, Sunness J, Humayun MS, Pieramici DJ, Chang TS (2002) Patient selection for macular translocation surgery using the scanning laser ophthalmoscope. Ophthalmology 109(9):1737–1744. https://doi.org/10.1016/s0161-6420(02)01120-x
Hawlina M, Konec B (1992) New noncorneal HK-loop electrode for clinical electroretinography. Doc Ophthalmol 81(2):253–259. https://doi.org/10.1007/bf00156014
Hammer DX, Ferguson RD, Magill JC, Paunescu LA, Beaton S, Ishikawa H, Wollstein G, Schuman JS (2005) Active retinal tracker for clinical optical coherence tomography systems. J Biomed Opt 10(2):024038–024038. https://doi.org/10.1117/1.1896967
Ferguson RD, Hammer DX, Paunescu LA, Beaton S, Schuman JS (2004) Tracking optical coherence tomography. Opt Lett 29(18):2139–2141. https://doi.org/10.1364/ol.29.002139
Ishikawa H, Gabriele ML, Wollstein G, Ferguson RD, Hammer DX, Paunescu LA, Beaton SA, Schuman JS (2006) Retinal nerve fiber layer assessment using optical coherence tomography with active optic nerve head tracking. Invest Ophthalmol Vis Sci 47(3):964–967. https://doi.org/10.1167/iovs.05-0748
Guestrin ED, Eizenman M (2006) General theory of remote gaze estimation using the pupil center and corneal reflections. IEEE Trans Biomed Eng 53(6):1124–1133. https://doi.org/10.1109/tbme.2005.863952
Mestre C, Gautier J, Pujol J (2018) Robust eye tracking based on multiple corneal reflections for clinical applications. J Biomed Opt 23(3):1–9. https://doi.org/10.1117/1.Jbo.23.3.035001
Palmowski-Wolfe AM, Woerdehoff U (2005) A comparison of the fast stimulation multifocal-ERG in patients with an IOL and control groups of different age. Doc Ophthalmol 111(2):87–93. https://doi.org/10.1007/s10633-005-4506-x
Mohidin N, Yap MK, Jacobs RJ (1999) Influence of age on the multifocal electroretinography. Ophthalmic Physiol Opt 19(6):481–488. https://doi.org/10.1046/j.1475-1313.1999.00468.x
Feigl B, Stewart IB, Brown B, Zele AJ (2008) Local neuroretinal function during acute hypoxia in healthy older people. Invest Ophthalmol Vis Sci 49(2):807–813. https://doi.org/10.1167/iovs.07-0994
Fragiotta S, Carnevale C, Cutini A, Rigoni E, Grenga PL, Vingolo EM (2018) Factors influencing fixation stability area: a comparison of two methods of recording. Optom Vis Sci 95(4):384–390. https://doi.org/10.1097/opx.0000000000001201
Schonbach EM, Ibrahim MA, Kong X, Strauss RW, Munoz B, Birch DG, Sunness JS, West SK, Scholl HPN (2017) Metrics and acquisition modes for fixation stability as a visual function biomarker. Invest Ophthalmol Vis Sci 58(6):268–276. https://doi.org/10.1167/iovs.17-21710
Longhin E, Convento E, Pilotto E, Bonin G, Vujosevic S, Kotsafti O, Midena E (2013) Static and dynamic retinal fixation stability in microperimetry. Can J Ophthalmol 48(5):375–380. https://doi.org/10.1016/j.jcjo.2013.05.021
Zhu X, He W, Zhang K, Zhang Y, Fan Q, Lu Y (2019) Fixation characteristics in highly myopic eyes: the Shanghai high myopia study. Sci Rep 9(1):6502. https://doi.org/10.1038/s41598-019-42895-3
Acknowledgements
The authors would like to thank Dr. Laura Frishman for assistance with the manuscript, Dr. Scott Stevenson for consideration with the results, Dr. Marcus Bearse for assistance formulating initial ideas, and Nicole Karson for data collection.
Funding
This work was supported by UHCO startup funds to the labs of Dr. Wendy W. Harrison and Dr. Daniel R. Coates. NIH EY007088 also provided funding for AJ and RW.
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Jennyffer Smith, Yes; Allison Jussel, Yes; Rachel Wang, Yes; Daniel R. Coates, Yes; Wendy W. Harrison, Yes.
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University of Houston IRB approval for study 1637.
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Smith, J.D., Jussel, A., Wang, R. et al. Fundus motion during mfERG testing. Doc Ophthalmol 143, 129–139 (2021). https://doi.org/10.1007/s10633-021-09829-9
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DOI: https://doi.org/10.1007/s10633-021-09829-9