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Quantitative and objective diagnosis of color vision deficiencies based on steady-state visual evoked potentials

Abstract

Purpose

Traditional color vision tests depend on subjective judgments and are not suitable for infant children and subjects with cognitive dysfunction. We aimed to explore an objective and quantitative color vision testing method based on sweep steady-state visual evoked potentials (sweep SSVEPs) and compare the results with subjective Farnsworth–Munsell (FM) 100-hue test results.

Methods

A red-green SSVEP pattern reversal checkboard paradigm at different luminance ratios was used to induce visual evoked potentials (VEPs) from 15 color vision deficiencies (CVDs) and 11 normal color vision subjects. After electroencephalography signals were processed by canonical correlation analysis, an equiluminance turning curve corresponding to the activation of the L-cones and M-cones at different levels of color vision was established. Then, we obtained different equiluminance T and proposed the SSVEP color vision severity index (ICVD) to quantify color vision function and the severity of CVDs. In addition, the FM 100-hue test was used to obtain subjective data for the diagnosis of color vision.

Results

The value of ICVD can be an indicator of the level of color vision. Both the total error scores (TES) and confusion index (C-index) of the FM 100-hue test were significantly correlated with ICVD values (P < 0.001, respectively). ICVD also had a good classification effect in detecting normals, anomalous trichromats and dichromats. Moreover, equiluminance T had a good effect on classifying protans and deutans in subjects with CVDs.

Conclusion

Color vision evaluation with sweep SSVEPs showed a good correlation with subjective psychophysical methods. SSVEPs can be an objective and quantitative method to test color vision and diagnose CVDs.

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References

  1. Rushton WAH (1965) Chemical basis of colour vision and colour blindness. Nature 206:1087. https://doi.org/10.1038/2061087a0

    CAS  Article  PubMed  Google Scholar 

  2. Simunovic MP (2009) Colour vision deficiency. Eye 24:747. https://doi.org/10.1038/eye.2009.251

    Article  PubMed  Google Scholar 

  3. Oliveira MM (2013) Towards more accessible visualizations for color-vision-deficient individuals. Comput Sci Eng 15(5):80–87. https://doi.org/10.1109/MCSE.2013.113

    Article  Google Scholar 

  4. Fairchild MD (2013) Color appearance models, 3rd edn. Rochester institute of technology, USA

    Book  Google Scholar 

  5. Graham CH, Yun H (1958) Color defect and color theory. Science 127(3300):675–682. https://doi.org/10.1126/science.127.3300.675

    CAS  Article  PubMed  Google Scholar 

  6. Greenstein VC, Hood DC, Ritch R, Steinberger D, Carr RE (1989) S (blue) cone pathway vulnerability in retinitis pigmentosa, diabetes and glaucoma. Invest Ophthalmol Vis Sci 30(8):1732–1737. https://doi.org/10.1016/0014-4835(89)90103-6

    CAS  Article  PubMed  Google Scholar 

  7. Yuichi N, Sanae M, Fumiyuki N, Takayuki M, Masahito O (2014) Evaluation of acquired color vision deficiency in glaucoma using the Rabin cone contrast test. Invest Ophthalmol Vis Sci 55(10):6686. https://doi.org/10.1167/iovs.14-14079

    CAS  Article  Google Scholar 

  8. O'Neill-Biba M, Sivaprasad S, Rodriguez-Carmona M, Wolf JE, Barbur JL (2010) Loss of chromatic sensitivity in AMD and diabetes: a comparative study. Ophthalmic Physiol Opt 30(5):705–716. https://doi.org/10.1111/j.1475-1313.2010.00775.x

    CAS  Article  PubMed  Google Scholar 

  9. Vingrys AJ, King-Smith PE (1988) A quantitative scoring technique for panel tests of color vision. Invest Ophthalmol Vis Sci 29(1):50–63

    CAS  PubMed  Google Scholar 

  10. Birch J (1989) Use of the Farnsworth–Munsell 100-Hue test in the examination of congenital colour vision defects. Ophthal Physiol Opt 9(2):156–162

    CAS  Article  Google Scholar 

  11. Ghose S, Parmar T, Dada T, Vanathi M, Sharma S (2014) A new computer-based Farnsworth Munsell 100-hue test for evaluation of color vision. Int Ophthalmol 34(4):747–751. https://doi.org/10.1007/s10792-013-9865-9

    Article  PubMed  Google Scholar 

  12. Rabin JC, Kryder AC, Lam D (2016) Diagnosis of normal and abnormal color vision with cone-specific VEPs. Transl Vis Sci Technol 5(3):8. https://doi.org/10.1167/tvst.5.3.8

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kai X, Hou M, Ye G (2005). Novel method for the quantitative measurement of color vision deficiencies. Optics in health care and biomedical optics: diagnostics and treatment, 5630. https://doi.org/10.1117/12.572902

  14. Salomao RC, Martins ICVD, Risuenho BBO, Guimaraes DL, Silveira LCL, Ventura DF, Souza GS (2019) Visual evoked cortical potential elicited by pseudoisochromatic stimulus. Doc Ophthalmol 138(1):43–54. https://doi.org/10.1007/s10633-018-09669-0

    Article  PubMed  Google Scholar 

  15. Crognale MA, Switkes E, Rabin J, Schneck ME, Haegerstrom-Portnoy G, Adams AJ (1993) Application of the spatiochromatic visual evoked potential to detection of congenital and acquired color-vision deficiencies. J Opt Soc Am A Opt Image Sci Vis 10(8):1818–1825. https://doi.org/10.1364/JOSAA.10.001818

    CAS  Article  PubMed  Google Scholar 

  16. Adachi-Usami E, Tsukamoto M, Shimada Y (1995) Color vision and color pattern visual evoked cortical potentials in a patient with acquired cerebral dyschromatopsia. Doc Ophthalmol 90(3):259–269

    CAS  Article  Google Scholar 

  17. Xie J, Xu G, Wang J, Li M, Han C, Jia Y (2016) Effects of mental load and fatigue on steady-state evoked potential based brain computer interface tasks: a comparison of periodic flickering and motion-reversal based visual attention. PLoS ONE 11(9):e0163426. https://doi.org/10.1371/journal.pone.0163426

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Zheng X, Xu G, Zhi Y, Wang Y, Han C, Wang B, Zhang S, Zhang K, Liang R (2019) Objective and quantitative assessment of interocular suppression in strabismic amblyopia based on steady-state motion visual evoked potentials. Vis Res 164:44–52. https://doi.org/10.1016/j.visres.2019.07.003

    Article  PubMed  Google Scholar 

  19. Kremers J, Bhatt D (2016) Towards an electroretinographic assay for studying colour vision in human observers. Doc Ophthalmol 133(2):109–120. https://doi.org/10.1007/s10633-016-9561-y

    Article  PubMed  Google Scholar 

  20. Aher AJ, Martins CMG, Barboni MTS, Nagy BV, Hauzman E, Bonci DMO, Ventura DF, Kremers J (2018) Electroretinographical determination of human color vision type. J Opt Soc Am A Opt Image Sci Vis 35(4):B92–B99. https://doi.org/10.1364/JOSAA.35.000B92

    CAS  Article  PubMed  Google Scholar 

  21. Barboni MTS, Hauzman E, Nagy BV, Martins CMG, Aher AJ, Tsai TI, Bonci DMO, Ventura DF, Kremers J (2019) Electrodiagnosis of dichromacy. Vision Res 158:135–145. https://doi.org/10.1016/j.visres.2019.02.011

    Article  PubMed  Google Scholar 

  22. Regan BC, Reffin JP, Mollon JD (1994) Luminance noise and the rapid determination of discrimination ellipses in colour deficiency. Vision Res 34(10):1279–1299. https://doi.org/10.1016/0042-6989(94)90203-8

    CAS  Article  PubMed  Google Scholar 

  23. Odom JV, Bach M, Brigell M, Holder GE, McCulloch DL, Mizota A, Tormene AP, International Society for Clinical Electrophysiology of V (2016) ISCEV standard for clinical visual evoked potentials: (2016 update). Doc Ophthalmol 133 (1):1–9. http://doi.org/10.1007/s10633-016-9553-y

  24. American Clinical Neurophysiology S (2006) Guideline 5: guidelines for standard electrode position nomenclature. J Clin Neurophysiol 23(2):107–110. https://doi.org/10.1097/00004691-200604000-00006

    Article  Google Scholar 

  25. Zheng X, Xu G, Wu Y, Wang Y, Du C, Wu Y, Zhang S, Han C (2020) Comparison of the performance of six stimulus paradigms in visual acuity assessment based on steady-state visual evoked potentials. Doc Ophthalmol. https://doi.org/10.1007/s10633-020-09768-x

    Article  PubMed  Google Scholar 

  26. Stockman A, Sharpe LT (1998) Human cone spectral sensitivities: a progress report. Vis Res 38(21):3193–3206. https://doi.org/10.1016/S0042-6989(98)00060-1

    CAS  Article  PubMed  Google Scholar 

  27. Stockman A, Sharpe LT, Fach C (1999) The spectral sensitivity of the human short-wavelength sensitive cones derived from thresholds and color matches. Vis Res 39(17):2901–2927. https://doi.org/10.1016/S0042-6989(98)00225-9

    CAS  Article  PubMed  Google Scholar 

  28. Stockman A, Sharpe LT (2000) The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype. Vis Res 40(13):1711–1737. https://doi.org/10.1016/S0042-6989(00)00021-3

    CAS  Article  PubMed  Google Scholar 

  29. Stockman A, MacLeod DI, Johnson NE (1993) Spectral sensitivities of the human cones. J Opt Soc Am Opt Image Sci Vis 10(12):2491–2521

    CAS  Article  Google Scholar 

  30. Neitz J, Jacobs GH (1986) Polymorphism of the long-wavelength cone in normal human colour vision. Nature 323(6089):623–625. https://doi.org/10.1038/323623a0

    CAS  Article  PubMed  Google Scholar 

  31. Waaler GH (1968) Heredity of two normal types of colour vision. Nature 218(5142):688–689

    CAS  Article  Google Scholar 

  32. Gerling J, Meigen T, Bach M (1997) Shift of equiluminance in congenital color vision deficiencies: pattern-ERG, VEP and psychophysical findings. Vis Res 37(6):821–826

    CAS  Article  Google Scholar 

  33. Wyszecki G, Stiles WS (1982) Color science: concepts and methods quantitative data and formulae, 2nd edn. Wiley, New York

    Google Scholar 

  34. Gundogan FC, Tas A, Altun S, Oz O, Erdem U, Sobaci G (2013) Color vision versus pattern visual evoked potentials in the assessment of subclinical optic pathway involvement in multiple sclerosis. Indian J Ophthalmol 61(3):100–103. https://doi.org/10.4103/0301-4738.99842

    Article  PubMed  PubMed Central  Google Scholar 

  35. Vingrys AJ, Atchison DA, Bowman KJ (2010) The use of colour difference vectors in diagnosing congenital colour vision deficiencies with the Farnsworth–Munsell 100-hue test. Ophthalmic Physiol Opt 12(1):38–45

    Google Scholar 

  36. Winston JV, Martin DA, Heckenlively JR (1986) Computer analysis of Farnsworth–Munsell 100-hue test. Doc Ophthalmol 62(1):61–72

    CAS  Article  Google Scholar 

  37. Smith VC, Pokorny J, Pass AS (1985) Color-axis determination on the Farnsworth–Munsell 100-hue test. Am J Ophthalmol 100(1):176–182

    CAS  Article  Google Scholar 

  38. Thyagarajan S, Moradi P, Membrey L, Alistair D, Laidlaw H (2007) Technical note: the effect of refractive blur on colour vision evaluated using the Cambridge Colour Test, the Ishihara Pseudoisochromatic Plates and the Farnsworth Munsell 100 Hue Test. Ophthalmic Physiol Opt 27(3):315–319. https://doi.org/10.1111/j.1475-1313.2007.00469.x

    Article  PubMed  Google Scholar 

  39. Kowser Z, Shaj B, Ramya D, Vaitheeswaran K, Deepa V, Rajiv R, Tarun S (2010) Effect of illumination on colour vision testing with Farnsworth–Munsell 100 hue test: customized colour vision booth versus room illumination. Korean J Ophthalmol 24(3):159–162

    Article  Google Scholar 

  40. Dobkins KR, Gunther KL, Peterzell DH (2000) What covariance mechanisms underlie green/red equiluminance, luminance contrast sensitivity and chromatic (green/red) contrast sensitivity? Vis Res 40(6):613–628. https://doi.org/10.1016/S0042-6989(99)00211-4

    CAS  Article  PubMed  Google Scholar 

  41. Han C, Xu G, Xie J, Chen C, Zhang S (2018) Highly Interactive Brain Computer Interface Based on Flicker Free Steady State Motion Visual Evoked Potential. Sci Rep 8(1):5835

    Article  Google Scholar 

  42. Hotelling H (1936) Relations between two sets of variates. Biometrika 28(3/4):321–377. https://doi.org/10.2307/2333955

    Article  Google Scholar 

  43. Bantis LE, Nakas CT, Reiser B (2014) Construction of confidence regions in the ROC space after the estimation of the optimal Youden index-based cut-off point. Biometrics 70(1):212–223. https://doi.org/10.1111/biom.12107

    Article  PubMed  Google Scholar 

  44. Dajun X, Ahmed O, Stephanie C, Hinde S, James G, Robert S (2015) Brightness-color interactions in human early visual cortex. J Neurosci 35(5):2226. https://doi.org/10.1523/jneurosci.3740-14.2015

    Article  Google Scholar 

  45. Li X, Chen Y, Lashgari R, Bereshpolova Y, Swadlow HA, Lee BB, Alonso JM (2015) Mixing of chromatic and luminance retinal signals in primate area V1. Cereb Cortex 25(7):1920–1937. https://doi.org/10.1093/cercor/bhu002

    Article  PubMed  Google Scholar 

  46. Gomes BD, Souza GS, Rodrigues AR, Saito CA, Silveira LC, da Silva FM (2006) Normal and dichromatic color discrimination measured with transient visual evoked potential. Vis Neurosci 23(3–4):617–627. https://doi.org/10.1017/S0952523806233194

    Article  PubMed  Google Scholar 

  47. Iris Z, Susan C, Teller DY (2007) Infant color vision: prediction of infants' spontaneous color preferences. Vis Res 47(10):1368–1381. https://doi.org/10.1016/j.visres.2006.09.024

    Article  Google Scholar 

  48. Mercer ME, Drodge SC, Courage ML, Adams RJ (2014) A pseudoisochromatic test of color vision for human infants. Vis Res 100:72–77. https://doi.org/10.1016/j.visres.2014.04.006

    Article  PubMed  Google Scholar 

  49. Kremers J, Scholl HP, Knau H, Berendschot TT, Usui T, Sharpe LT (2000) L/M cone ratios in human trichromats assessed by psychophysics, electroretinography and retinal densitometry. J Opt Soc Am A Opt Image Sci Vis 17(3):517–526. https://doi.org/10.1364/josaa.17.000517

    CAS  Article  PubMed  Google Scholar 

  50. Carroll J, McMahon C, Neitz M, Neitz J (2000) Flicker-photometric electroretinogram estimates of L: M cone photoreceptor ratio in men with photopigment spectra derived from genetics. J Opt Soc Am A Opt Image Sci Vis 17(3):499–509. https://doi.org/10.1364/josaa.17.000499

    CAS  Article  PubMed  Google Scholar 

  51. Dees EW, Gilson SJ, Neitz M, Baraas RC (2015) The influence of L-opsin gene polymorphisms and neural ageing on spatio-chromatic contrast sensitivity in 20–71 year olds. Vision Res 116(Pt A):13–24. https://doi.org/10.1016/j.visres.2015.08.015

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank all the subjects for their participation in this study, supported by the Special Guidance Funds for the Construction of World-class Universities (Disciplines) and Characteristic Development in Central Universities (PY3A071) and the grants from the National Natural Science Foundation of China (NSFC-51775415).

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Correspondence to Guanghua Xu.

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Zheng, X., Xu, G., Wang, Y. et al. Quantitative and objective diagnosis of color vision deficiencies based on steady-state visual evoked potentials. Int Ophthalmol 41, 587–598 (2021). https://doi.org/10.1007/s10792-020-01613-z

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  • DOI: https://doi.org/10.1007/s10792-020-01613-z

Keywords

  • Color vision deficiency (CVD)
  • Equiluminance
  • Steady-state visual evoked potential (SSVEP)
  • Color vision test