Abstract
Purpose
Exposure to blue light is thought to be harmful to the retina. The purpose of this study was to determine the effects of long-term exposure to narrowband blue light on retinal function in rhesus monkeys.
Methods
Young rhesus monkeys were reared under short-wavelength “blue” light (n = 7; 465 nm, 183 ± 28 lx) on a 12-h light/dark cycle starting at 26 ± 2 days of age. Age-matched control monkeys were reared under broadband “white” light (n = 8; 504 ± 168 lx). Light- and dark-adapted full-field flash electroretinograms (ERGs) were recorded at 330 ± 9 days of age. Photopic stimuli were brief red flashes (0.044–5.68 cd.s/m2) on a rod-saturating blue background and the International Society for Clinical Electrophysiology of Vision (ISCEV) standard 3.0 white flash on a 30 cd/m2 white background. Monkeys were dark adapted for 20 min and scotopic stimuli were ISCEV standard white flashes of 0.01, 3.0, and 10 cd.s/m2. A-wave, b-wave, and photopic negative response (PhNR) amplitudes were measured. Light-adapted ERGs in young monkeys were compared to ERGs in adult monkeys reared in white light (n = 10; 4.91 ± 0.88 years of age).
Results
For red flashes on a blue background, there were no significant differences in a-wave (P = 0.46), b-wave (P = 0.75), and PhNR amplitudes (P = 0.94) between white light and blue light reared monkeys for all stimulus energies. ISCEV standard light- and dark-adapted a- and b-wave amplitudes were not significantly different between groups (P > 0.05 for all). There were no significant differences in a- and b-wave implicit times between groups for all ISCEV standard stimuli (P > 0.05 for all). PhNR amplitudes of young monkeys were significantly smaller compared to adult monkeys for all stimulus energies (P < 0.05 for all). There were no significant differences in a-wave (P = 0.19) and b-wave (P = 0.17) amplitudes between young and adult white light reared monkeys.
Conclusions
Long-term exposure to narrowband blue light did not affect photopic or scotopic ERG responses in young monkeys. Findings suggest that exposure to 12 h of daily blue light for approximately 10 months does not result in altered retinal function.
Similar content being viewed by others
References
Brainard GC, Hanifin JP, Greeson JM, Byrne B, Glickman G, Gerner E et al (2001) Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J Neurosci 21(16):6405–6412. https://doi.org/10.1523/jneurosci.21-16-06405.2001
Thapan K, Arendt J, Skene DJ (2001) An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J Physiol 535(Pt 1):261–267. https://doi.org/10.1111/j.1469-7793.2001.t01-1-00261.x
Lockley SW, Brainard GC, Czeisler CA (2003) High sensitivity of the human circadian melatonin rhythm to resetting by short wavelength light. J Clin Endocrinol Metab 88(9):4502–4505. https://doi.org/10.1210/jc.2003-030570
Cajochen C, Münch M, Kobialka S, Kräuchi K, Steiner R, Oelhafen P et al (2005) High sensitivity of human melatonin, alertness, thermoregulation, and heart rate to short wavelength light. J Clin Endocrinol Metab 90(3):1311–1316. https://doi.org/10.1210/jc.2004-0957
Revell VL, Arendt J, Fogg LF, Skene DJ (2006) Alerting effects of light are sensitive to very short wavelengths. Neurosci Lett 399(1–2):96–100. https://doi.org/10.1016/j.neulet.2006.01.032
Cajochen C (2007) Alerting effects of light. Sleep Med Rev 11(6):453–464. https://doi.org/10.1016/j.smrv.2007.07.009
Wahl S, Engelhardt M, Schaupp P, Lappe C, Ivanov IV (2019) The inner clock-Blue light sets the human rhythm. J Biophotonics 12(12):102. https://doi.org/10.1002/jbio.201900102
Touitou Y, Point S (2020) Effects and mechanisms of action of light-emitting diodes on the human retina and internal clock. Environ Res 190:109942. https://doi.org/10.1016/j.envres.2020.109942
Bullough JD, Bierman A, Rea MS (2019) Evaluating the blue-light hazard from solid state lighting. Int J Occup Saf Erg 25(2):311–320. https://doi.org/10.1080/10803548.2017.1375172
Ham WT Jr, Mueller HA, Sliney DH (1976) Retinal sensitivity to damage from short wavelength light. Nature 260(5547):153–155. https://doi.org/10.1038/260153a0
Ham WT Jr, Ruffolo JJ Jr, Mueller HA, Clarke AM, Moon ME (1978) Histologic analysis of photochemical lesions produced in rhesus retina by short-wave-length light. Invest Ophthalmol Vis Sci 17(10):1029–1035
Shang YM, Wang GS, Sliney D, Yang CH, Lee LL (2014) White light-emitting diodes (LEDs) at domestic lighting levels and retinal injury in a rat model. Environ Health Perspect 122(3):269–276. https://doi.org/10.1289/ehp.1307294
Shang YM, Wang GS, Sliney DH, Yang CH, Lee LL (2017) Light-emitting-diode induced retinal damage and its wavelength dependency in vivo. Int J Ophthalmol 10(2):191–202. https://doi.org/10.18240/ijo.2017.02.03
Krigel A, Berdugo M, Picard E, Levy-Boukris R, Jaadane I, Jonet L et al (2016) Light-induced retinal damage using different light sources, protocols and rat strains reveals LED phototoxicity. Neuroscience 339:296–307. https://doi.org/10.1016/j.neuroscience.2016.10.015
Point S, Beroud M (2019) Blue light hazard: does rat retina make relevant model for discussing exposure limit values applicable to humans? Radioprotection 54(2):141–147. https://doi.org/10.1051/radiopro/2019013
Lei B, Yao G (2006) Spectral attenuation of the mouse, rat, pig and human lenses from wavelengths 360 nm to 1020 nm. Exp Eye Res 83(3):610–614. https://doi.org/10.1016/j.exer.2006.02.013
O’Hagan JB, Khazova M, Price LL (2016) Low-energy light bulbs, computers, tablets and the blue light hazard. Eye 30(2):230–233. https://doi.org/10.1038/eye.2015.261
Lin KH, Tran T, Kim S, Park S, Stout JT, Chen R et al (2021) Advanced retinal imaging and ocular parameters of the rhesus macaque eye. Transl Vis Sci Technol 10(6):7. https://doi.org/10.1167/tvst.10.6.7
Qiao-Grider Y, Hung L-F, Kee CS, Ramamirtham R, Smith EL 3rd (2007) Normal ocular development in young rhesus monkeys (Macaca mulatta). Vision Res 47(11):1424–1444. https://doi.org/10.1016/j.visres.2007.01.025
Lou L, Arumugam B, Hung L-F, She Z, Beach KM, Smith EL 3rd et al (2021) Long-term narrowband lighting influences activity but not intrinsically photosensitive retinal ganglion cell-driven pupil responses. Front Physiol 12:711525. https://doi.org/10.3389/fphys.2021.711525
Hung L-F, Beach K, She Z, Arumugam B, Ostrin L, Smith EL (2020) Effect of narrowband, short-wavelength ambient lighting on refractive development in infant rhesus monkeys. Invest Ophthalmol Vis Sci 61(7):560
Hung L-F, Beach KM, She Z, Ostrin LA, Smith EL (2021) Effects of narrowband, short-wavelength ambient lighting on form deprivation myopia in infant rhesus monkeys. Invest Ophthalmol Vis Sci 62(8):1378
She Z, Hung L-F, Arumugam B, Beach KM, Smith EL 3rd (2020) Effects of low intensity ambient lighting on refractive development in infant rhesus monkeys (Macaca mulatta). Vision Res 176:48–59. https://doi.org/10.1016/j.visres.2020.07.004
Baylor DA, Nunn BJ, Schnapf JL (1987) Spectral sensitivity of cones of the monkey Macaca fascicularis. J Physiol 390:145–160. https://doi.org/10.1113/jphysiol.1987.sp016691
Smith EL 3rd, Hung L-F (1999) The role of optical defocus in regulating refractive development in infant monkeys. Vision Res 39(8):1415–1435. https://doi.org/10.1016/S0042-6989(98)00229-6
Delori F (2014) The ANSI 2014 standard for safe use of lasers. Frontiers in Optics 2014. Tucson, Optica Publishing Group, Arizona https://doi.org/10.1364/FIO.2014.FW1F.2
Dawson WW, Trick GL, Litzkow CA (1979) Improved electrode for electroretinography. Invest Ophthalmol Vis Sci 18(9):988–991
Frishman L, Sustar M, Kremers J, McAnany JJ, Sarossy M, Tzekov R et al (2018) ISCEV extended protocol for the photopic negative response (PhNR) of the full-field electroretinogram. Doc Ophthalmol 136(3):207–211. https://doi.org/10.1007/s10633-018-9638-x
Robson AG, Frishman LJ, Grigg J, Hamilton R, Jeffrey BG, Kondo M et al (2022) ISCEV standard for full-field clinical electroretinography (2022 update). Doc Ophthalmol 144(3):165–177. https://doi.org/10.1007/s10633-022-09872-0
Fulton AB, Rushton WAH (1978) The human rod ERG: correlation with psychophysical responses in light and dark adaptation. Vision Res 18(7):793–800. https://doi.org/10.1016/0042-6989(78)90119-0
Binns AM, Mortlock KE, North RV (2011) The relationship between stimulus intensity and response amplitude for the photopic negative response of the flash electroretinogram. Doc Ophthalmol 122(1):39–52. https://doi.org/10.1007/s10633-010-9257-7
Johnson MA, Jeffrey BG, Messias AMV, Robson AG (2019) ISCEV extended protocol for the stimulus-response series for the dark-adapted full-field ERG b-wave. Doc Ophthalmol 138(3):217–227. https://doi.org/10.1007/s10633-019-09687-6
Brown KT, Wiesel TN (1961) Localization of origins of electroretinogram components by intraretinal recording in the intact cat eye. J Physiol 158(2):257–280. https://doi.org/10.1113/jphysiol.1961.sp006768
Bush RA, Sieving PA (1994) A proximal retinal component in the primate photopic ERG a-wave. Invest Ophthalmol Vis Sci 35(2):635–645
Robson JG, Saszik SM, Ahmed J, Frishman LJ (2003) Rod and cone contributions to the a-wave of the electroretinogram of the macaque. J Physiol 547(2):509–530. https://doi.org/10.1113/jphysiol.2002.030304
Knapp AG, Schiller PH (1984) The contribution of on-bipolar cells to the electroretinogram of rabbits and monkeys. A study using 2-amino-4-phosphonobutyrate (APB). Vision Res 24(12):1841–6. https://doi.org/10.1016/0042-6989(84)90016-6
Sieving PA, Murayama K, Naarendorp F (1994) Push-pull model of the primate photopic electroretinogram: a role for hyperpolarizing neurons in shaping the b-wave. Vis Neurosci 11(3):519–532. https://doi.org/10.1017/s0952523800002431
Viswanathan S, Frishman LJ, Robson JG, Harwerth RS, Smith EL 3rd (1999) The photopic negative response of the macaque electroretinogram: reduction by experimental glaucoma. Invest Ophthalmol Vis Sci 40(6):1124–1136
Harwerth RS, Sperlng HG (1971) Prolonged color blindness induced by intense spectral lights in rhesus monkeys. Science 174(4008):520–523. https://doi.org/10.1126/science.174.4008.520
Behar-Cohen F, Martinsons C, Viénot F, Zissis G, Barlier-Salsi A, Cesarini JP et al (2011) Light-emitting diodes (LED) for domestic lighting: any risks for the eye? Prog Retin Eye Res 30(4):239–257. https://doi.org/10.1016/j.preteyeres.2011.04.002
Jaadane I, Boulenguez P, Chahory S, Carré S, Savoldelli M, Jonet L et al (2015) Retinal damage induced by commercial light emitting diodes (LEDs). Free Radic Biol Med 84:373–384. https://doi.org/10.1016/j.freeradbiomed.2015.03.034
Gorgels TG, van Norren D (1992) Spectral transmittance of the rat lens. Vision Res 32(8):1509–1512. https://doi.org/10.1016/0042-6989(92)90206-x
van Norren D (1972) Macaque lens absorption in vivo. Invest Ophthalmol 11(3):177–181
Boettner EA, Wolter JR (1962) Transmission of the ocular media. Invest Ophthalmol Vis Sci 1(6):776–783
Harwerth RS, Smith EL 3rd (1985) Rhesus monkey as a model for normal vision of humans. Am J Optom Physiol Opt 62(9):633–641. https://doi.org/10.1097/00006324-198509000-00009
Lindbloom-Brown Z, Tait LJ, Horwitz GD (2014) Spectral sensitivity differences between rhesus monkeys and humans: implications for neurophysiology. J Neurophysiol 112(12):3164–3172. https://doi.org/10.1152/jn.00356.2014
Prayag AS, Münch M, Aeschbach D, Chellappa SL, Gronfier C (2019) Light modulation of human clocks, wake, and sleep. Clocks Sleep 1(1):193–208. https://doi.org/10.3390/clockssleep1010017
Foulds WS, Barathi VA, Luu CD (2013) Progressive myopia or hyperopia can be induced in chicks and reversed by manipulation of the chromaticity of ambient light. Invest Ophthalmol Vis Sci 54(13):8004–8012. https://doi.org/10.1167/iovs.13-12476
Jiang L, Zhang S, Schaeffel F, Xiong S, Zheng Y, Zhou X et al (2014) Interactions of chromatic and lens-induced defocus during visual control of eye growth in guinea pigs (Cavia porcellus). Vision Res 94:24–32. https://doi.org/10.1016/j.visres.2013.10.020
Liu R, Qian Y-F, He JC, Hu M, Zhou X-T, Dai J-H et al (2011) Effects of different monochromatic lights on refractive development and eye growth in guinea pigs. Exp Eye Res 92(6):447–453. https://doi.org/10.1016/j.exer.2011.03.003
Gawne TJ, Ward AH, Norton TT (2018) Juvenile tree shrews do not maintain emmetropia in narrow-band blue light. Optom Vis Sci 95(10):911–920. https://doi.org/10.1097/OPX.0000000000001283
Breton ME, Quinn GE, Schueller AW (1995) Development of electroretinogram and rod phototransduction response in human infants. Invest Ophthalmol Vis Sci 36(8):1588–1602
Westall CA, Panton CM, Levin AV (1998) Time courses for maturation of electroretinogram responses from infancy to adulthood. Doc Ophthalmol 96(4):355–379. https://doi.org/10.1023/a:1001856911730
Rangaswamy NV, Frishman LJ, Dorotheo EU, Schiffman JS, Bahrani HM, Tang RA (2004) Photopic ERGs in patients with optic neuropathies: comparison with primate ERGs after pharmacologic blockade of inner retina. Invest Ophthalmol Vis Sci 45(10):3827–3837. https://doi.org/10.1167/iovs.04-0458
Wang J, Cheng H, Hu YS, Tang RA, Frishman LJ (2012) The photopic negative response of the flash electroretinogram in multiple sclerosis. Invest Ophthalmol Vis Sci 53(3):1315–1323. https://doi.org/10.1167/iovs.11-8461
Acknowledgements
The authors thank Hope Queener for the MATLAB program and Dr. Alexander Schill for help with the blue light exposure limit calculations.
Funding
Supported by National Institute of Health Grants R01 EY003611 and P30 EY007551, and funds from the Brien Holden Vision Institute and the UH Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
ELS holds patents for optical and pharmaceutical treatment strategies for myopia and is a paid consultant for SightGlass Vision Inc., Treehouse Eyes Inc., and Vision CRC USA. The other authors declare that they have no conflict of interest.
Ethical approval
Study procedures were reviewed and approved by the Institutional Animal Care and Use Committee at the University of Houston.
Informed consent
There are no human subjects in this study. We have included the ethics statements associated with animal studies.
Statement on the welfare of animals
All procedures conformed to the ARVO statement for the Use of Animals in Ophthalmic and Vision Research.
Statement of human rights
This article does not contain any studies with human participants performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lou, L., Frishman, L.J., Beach, K.M. et al. Long-term blue light rearing does not affect in vivo retinal function in young rhesus monkeys. Doc Ophthalmol 147, 45–57 (2023). https://doi.org/10.1007/s10633-023-09931-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10633-023-09931-0