Chinese Journal of Lasers, Volume. 50, Issue 9, 0907105(2023)

High‑Accuracy Quantitative Functional Imaging Technique for Retinal Opto‑Physiology with Optical Coherence Tomography

Yanhong Ma and Pengfei Zhang*
Author Affiliations
  • School of Optoelectronic Engineering and Instrumentation Science, Dalian University of Technology, Dalian 116024, Liaoning, China
  • show less
    References(80)

    [1] Wong W L, Su X Y, Li X et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis[J]. The Lancet Global Health, 2, e106-e116(2014).

    [2] Song P G, Du Y H, Chan K Y et al. The national and subnational prevalence and burden of age-related macular degeneration in China[J]. Journal of Global Health, 7, 020703(2017).

    [4] Verbakel S K, van Huet R A C, Boon C J F et al. Non-syndromic retinitis pigmentosa[J]. Progress in Retinal and Eye Research, 66, 157-186(2018).

    [5] Luo X T, Liu Y, Wang F H et al. Opportunities and challenges of gene therapy for retinitis pigmentosa[J]. Scientia Sinica: Vitae, 52, 1015-1022(2022).

    [6] Mitchell P, Liew G, Gopinath B et al. Age-related macular degeneration[J]. The Lancet, 392, 1147-1159(2018).

    [7] Fricke T R, Jong M, Naidoo K S et al. Global prevalence of visual impairment associated with myopic macular degeneration and temporal trends from 2000 through 2050: systematic review, meta-analysis and modelling[J]. The British Journal of Ophthalmology, 102, 855-862(2018).

    [8] Casson R J, Chidlow G, Wood J P M et al. Definition of glaucoma: clinical and experimental concepts[J]. Clinical & Experimental Ophthalmology, 40, 341-349(2012).

    [9] Datta S, Cano M, Ebrahimi K et al. The impact of oxidative stress and inflammation on RPE degeneration in non-neovascular AMD[J]. Progress in Retinal and Eye Research, 60, 201-218(2017).

    [10] Apte R S. Gene therapy for retinal degeneration[J]. Cell, 173, 5(2018).

    [11] Biesemeier A, Taubitz T, Julien S et al. Choriocapillaris breakdown precedes retinal degeneration in age-related macular degeneration[J]. Neurobiology of Aging, 35, 2562-2573(2014).

    [12] Zhang S, Zhang G Y, Zhou X et al. Changes in choroidal thickness and choroidal blood perfusion in Guinea pig myopia[J]. Investigative Ophthalmology & Visual Science, 60, 3074-3083(2019).

    [13] Wong C W, Phua V, Lee S Y et al. Is choroidal or scleral thickness related to myopic macular degeneration?[J]. Investigative Ophthalmology & Visual Science, 58, 907-913(2017).

    [14] Tode J, Richert E, Koinzer S et al. Thermal stimulation of the retina reduces bruch's membrane thickness in age related macular degeneration mouse models[J]. Translational Vision Science & Technology, 7, 2(2018).

    [15] Collin G B, Gogna N, Chang B et al. Mouse models of inherited retinal degeneration with photoreceptor cell loss[J]. Cells, 9, 931(2020).

    [16] Frishman L J. Origins of the electroretinogram[M]. Heckenlively J R, Arden G B. Principles and practice of clinical electrophysiology of vision, 139-183(2006).

    [17] Brown K T. The electroretinogram: its components and their origins[J]. Vision Research, 8, 633-677(1968).

    [18] Hood D C, Odel J G, Chen C S et al. The multifocal electroretinogram[J]. Journal of Neuro Ophthalmology, 23, 225-235(2003).

    [19] Berninger T A, Arden G B. The pattern electroretinogram[J]. Eye, 2, S257-S283(1988).

    [20] Bernardes R, Serranho P, Lobo C. Digital ocular fundus imaging: a review[J]. Ophthalmologica, 226, 161-181(2011).

    [21] Li L, Zhang Y, Li M X et al. Current application and progress of laser technology in ophthalmology[J]. Chinese Journal of Lasers, 49, 0507103(2022).

    [22] Laíns I, Wang J C, Cui Y et al. Retinal applications of swept source optical coherence tomography (OCT) and optical coherence tomography angiography (OCTA)[J]. Progress in Retinal and Eye Research, 84, 100951(2021).

    [23] Xue P. Development of high-performance optical coherence tomography[J]. Chinese Journal of Lasers, 48, 1517001(2021).

    [24] Lazebnik M, Marks D L, Potgieter K et al. Functional optical coherence tomography for detecting neural activity through scattering changes[J]. Optics Letters, 28, 1218-1220(2003).

    [25] Yao X C, Yamauchi A, Perry B et al. Rapid optical coherence tomography and recording functional scattering changes from activated frog retina[J]. Applied Optics, 44, 2019-2023(2005).

    [26] Bizheva K, Pflug R, Hermann B et al. Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography[J]. Proceedings of the National Academy of Sciences of the United States of America, 103, 5066-5071(2006).

    [27] Srinivasan V J, Wojtkowski M, Fujimoto J G et al. In vivo measurement of retinal physiology with high-speed ultrahigh-resolution optical coherence tomography[J]. Optics Letters, 31, 2308-2310(2006).

    [28] Srinivasan V J, Chen Y, Duker J S et al. In vivo functional imaging of intrinsic scattering changes in the human retina with high-speed ultrahigh resolution OCT[J]. Optics Express, 17, 3861-3877(2009).

    [29] Yao X C, Wang B Q. Intrinsic optical signal imaging of retinal physiology: a review[J]. Journal of Biomedical Optics, 20, 090901(2015).

    [30] Wang B Q, Lu R W, Zhang Q X et al. En face optical coherence tomography of transient light response at photoreceptor outer segments in living frog eyecup[J]. Optics Letters, 38, 4526-4529(2013).

    [31] Zhang Q X, Lu R W, Wang B Q et al. Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors[J]. Scientific Reports, 5, 9595(2015).

    [32] Thapa D, Wang B Q, Lu Y M et al. Enhancement of intrinsic optical signal recording with split spectrum optical coherence tomography[J]. Journal of Modern Optics, 64, 1800-1807(2017).

    [33] Wang B Q, Lu Y M, Yao X C. In vivo optical coherence tomography of stimulus-evoked intrinsic optical signals in mouse retinas[J]. Journal of Biomedical Optics, 21, 096010(2016).

    [34] Son T, Kim T H, Ma G Y et al. Functional intrinsic optical signal imaging for objective optoretinography of human photoreceptors[J]. Experimental Biology and Medicine, 246, 639-643(2021).

    [35] Son T, Wang B Q, Thapa D et al. Optical coherence tomography angiography of stimulus evoked hemodynamic responses in individual retinal layers[J]. Biomedical Optics Express, 7, 3151-3162(2016).

    [36] Son T, Alam M, Toslak D et al. Functional optical coherence tomography of neurovascular coupling interactions in the retina[J]. Journal of Biophotonics, 11, e201800089(2018).

    [37] Radhakrishnan H, Srinivasan V J. Multiparametric optical coherence tomography imaging of the inner retinal hemodynamic response to visual stimulation[J]. Journal of Biomedical Optics, 18, 086010(2013).

    [38] Leitgeb R A, Bachmann A H, Villiger M et al. Measurement of retinal physiology using functional Fourier domain OCT concepts[J]. Proceedings of SPIE, 6426, 642609(2007).

    [39] Schmoll T, Kolbitsch C, Leitgeb R A. In vivo functional retinal optical coherence tomography[J]. Journal of Biomedical Optics, 15, 041513(2010).

    [40] Tumlinson A R, Hermann B, Hofer B et al. Techniques for extraction of depth-resolved in vivo human retinal intrinsic optical signals with optical coherence tomography[J]. Japanese Journal of Ophthalmology, 53, 315-326(2009).

    [41] Messner A, dos Santos V A, Stegmann H et al. Quantification of intrinsic optical signals in the outer human retina using optical coherence tomography[J]. Annals of the New York Academy of Sciences, 1510, 145-157(2022).

    [42] Mathis T, Vasseur V, Zuber K et al. Light-induced modifications of the outer retinal hyperreflective layers on spectral-domain optical coherence tomography in humans: an experimental study[J]. Acta Ophthalmologica, 99, 765-772(2021).

    [43] Moayed A A, Hariri S, Choh V et al. In vivo imaging of intrinsic optical signals in chicken retina with functional optical coherence tomography[J]. Optics Letters, 36, 4575-4577(2011).

    [44] Moayed A A, Hariri S, Bizheva K et al. Correlation of visually evoked intrinsic optical signals and electroretinograms recorded from chicken retina with a combined functional optical coherence tomography and electroretinography system[J]. Journal of Biomedical Optics, 17, 016011(2012).

    [45] Tan B Y, Mason E, MacLellan B et al. Correlation of visually evoked functional and blood flow changes in the rat retina measured with a combined OCT+ERG system[J]. Investigative Ophthalmology & Visual Science, 58, 1673-1681(2017).

    [46] Suzuki W, Tsunoda K, Hanazono G et al. Stimulus-induced changes of reflectivity detected by optical coherence tomography in macaque retina[J]. Investigative Ophthalmology & Visual Science, 54, 6345-6354(2013).

    [47] Erchova I, Tumlinson A R, Fergusson J et al. Optophysiological characterisation of inner retina responses with high-resolution optical coherence tomography[J]. Scientific Reports, 8, 1813(2018).

    [48] Bissig D, Zhou C G, Le V et al. Optical coherence tomography reveals light-dependent retinal responses in Alzheimer’s disease[J]. NeuroImage, 219, 117022(2020).

    [49] Hunter J J, Merigan W H, Schallek J B. Imaging retinal activity in the living eye[J]. Annual Review of Vision Science, 5, 15-45(2019).

    [50] Hillmann D, Spahr H, Pfäffle C et al. In vivo optical imaging of physiological responses to photostimulation in human photoreceptors[J]. Proceedings of the National Academy of Sciences of the United States of America, 113, 13138-13143(2016).

    [51] Zhang P F, Zawadzki R J, Goswami M et al. In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors[J]. Proceedings of the National Academy of Sciences of the United States of America, 114, E2937-E2946(2017).

    [52] Lu C D, Lee B K, Schottenhamml J et al. Photoreceptor layer thickness changes during dark adaptation observed with ultrahigh-resolution optical coherence tomography[J]. Investigative Ophthalmology & Visual Science, 58, 4632-4643(2017).

    [53] Spahr H, Pfäffle C, Burhan S et al. Phase-sensitive interferometry of decorrelated speckle patterns[J]. Scientific Reports, 9, 11748(2019).

    [54] Pfäffle C, Spahr H, Kutzner L et al. Simultaneous functional imaging of neuronal and photoreceptor layers in living human retina[J]. Optics Letters, 44, 5671-5674(2019).

    [55] Miller E B, Zhang P F, Ching K et al. In vivo imaging reveals transient microglia recruitment and functional recovery of photoreceptor signaling after injury[J]. Proceedings of the National Academy of Sciences of the United States of America, 116, 16603-16612(2019).

    [56] Zhang P F, Shibata B, Peinado G et al. Measurement of diurnal variation in rod outer segment length in vivo in mice with the OCT optoretinogram[J]. Investigative Ophthalmology & Visual Science, 61, 9(2020).

    [57] Zhang L J, Dong R Y, Zawadzki R J et al. Volumetric data analysis enabled spatially resolved optoretinogram to measure the functional signals in the living retina[J]. Journal of Biophotonics, 15, e202100252(2022).

    [58] Pijewska E, Zhang P F, Meina M et al. Extraction of phase-based optoretinograms (ORG) from serial B-scans acquired over tens of seconds by mouse retinal raster scanning OCT system[J]. Biomedical Optics Express, 12, 7849-7871(2021).

    [59] Azimipour M, Migacz J V, Zawadzki R J et al. Functional retinal imaging using adaptive optics swept-source OCT at 1.6 MHz[J]. Optica, 6, 300-303(2019).

    [60] Azimipour M, Valente D, Vienola K V et al. Optoretinogram: optical measurement of human cone and rod photoreceptor responses to light[J]. Optics Letters, 45, 4658-4661(2020).

    [61] Zhang F R, Kurokawa K, Lassoued A et al. Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics[J]. Proceedings of the National Academy of Sciences of the United States of America, 116, 7951-7956(2019).

    [62] Lassoued A, Zhang F R, Kurokawa K et al. Cone photoreceptor dysfunction in retinitis pigmentosa revealed by optoretinography[J]. Proceedings of the National Academy of Sciences of the United States of America, 118, 2107444118(2021).

    [63] Pandiyan V P, Jiang X Y, Maloney-Bertelli A et al. High-speed adaptive optics line-scan OCT for cellular-resolution optoretinography[J]. Biomedical Optics Express, 11, 5274-5296(2020).

    [64] Pandiyan V P, Maloney-Bertelli A, Kuchenbecker J A et al. The optoretinogram reveals the primary steps of phototransduction in the living human eye[J]. Science Advances, 6, eabc1124(2020).

    [65] Boyle K C, Chen Z C, Ling T et al. Mechanisms of light-induced deformations in photoreceptors[J]. Biophysical Journal, 119, 1481-1488(2020).

    [66] Pandiyan V P, Nguyen P T, Pugh E N, et al. Human cone elongation responses can be explained by photoactivated cone opsin and membrane swelling and osmotic response to phosphate produced by RGS9-catalyzed GTPase[J]. Proceedings of the National Academy of Sciences of the United States of America, 119, e2202485119(2022).

    [67] Li Y C, Fariss R N, Qian J W et al. Light-induced thickening of photoreceptor outer segment layer detected by ultra-high resolution OCT imaging[J]. Investigative Ophthalmology & Visual Science, 57, OCT105-OCT111(2016).

    [68] Li Y C, Zhang Y K, Chen S et al. Light-dependent OCT structure changes in photoreceptor degenerative rd 10 mouse retina[J]. Investigative Ophthalmology & Visual Science, 59, 1084-1094(2018).

    [69] Berkowitz B A, Podolsky R H, Qian H H et al. Mitochondrial respiration in outer retina contributes to light-evoked increase in hydration in vivo[J]. Investigative Ophthalmology & Visual Science, 59, 5957-5964(2018).

    [70] Gao S S, Li Y C, Bissig D et al. Functional regulation of an outer retina hyporeflective band on optical coherence tomography images[J]. Scientific Reports, 11, 10260(2021).

    [71] Berkowitz B A, Podolsky R H, Childers K L et al. Functional changes within the rod inner segment ellipsoid in wildtype mice: an optical coherence tomography and electron microscopy study[J]. Investigative Opthalmology & Visual Science, 63, 8(2022).

    [72] Berkowitz B A, Podolsky R H, Lins-Childers K M et al. Outer retinal oxidative stress measured in vivo using QUEnch-assiSTed (QUEST) OCT[J]. Investigative Ophthalmology & Visual Science, 60, 1566-1570(2019).

    [73] Berkowitz B A, Podolsky R H, Childers K L et al. Rod photoreceptor neuroprotection in dark-reared Pde6brd10 mice[J]. Investigative Ophthalmology & Visual Science, 61, 14(2020).

    [74] Messner A, Werkmeister R M, Seidel G et al. Light-induced changes of the subretinal space of the temporal retina observed via optical coherence tomography[J]. Scientific Reports, 9, 13632(2019).

    [75] Tomczewski S, Węgrzyn P, Borycki D et al. Light-adapted flicker optoretinograms captured with a spatio-temporal optical coherence-tomography (STOC-T) system[J]. Biomedical Optics Express, 13, 2186-2201(2022).

    [76] Sun P C, Li Q, Li H et al. Depth-resolved physiological response of retina to transcorneal electrical stimulation measured with optical coherence tomography[J]. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 27, 905-915(2019).

    [77] Su X F, Zheng H, Li Q et al. Retinal neurovascular responses to transcorneal electrical stimulation measured with optical coherence tomography[J]. Experimental Biology and Medicine, 245, 289-300(2020).

    [78] Deng X F, Liu K Y, Zhu T P et al. Dynamic inverse SNR-decorrelation OCT angiography with GPU acceleration[J]. Biomedical Optics Express, 13, 3615-3628(2022).

    [79] Zhang Z Y, Yu C Y, Qiao Y L et al. Intraoperative optical coherence tomography angiography with micro integration[J]. Chinese Journal of Lasers, 49, 1507301(2022).

    [80] Kim T H, Ma G Y, Son T et al. Functional optical coherence tomography for intrinsic signal optoretinography: recent developments and deployment challenges[J]. Frontiers in Medicine, 9, 864824(2022).

    [81] Kim T H, Wang B Q, Lu Y M et al. Functional optical coherence tomography enables in vivo optoretinography of photoreceptor dysfunction due to retinal degeneration[J]. Biomedical Optics Express, 11, 5306-5320(2020).

    Tools

    Get Citation

    Copy Citation Text

    Yanhong Ma, Pengfei Zhang. High‑Accuracy Quantitative Functional Imaging Technique for Retinal Opto‑Physiology with Optical Coherence Tomography[J]. Chinese Journal of Lasers, 2023, 50(9): 0907105

    Download Citation

    EndNote(RIS)BibTexPlain Text
    Save article for my favorites
    Paper Information

    Category: Biomedical Optical Imaging

    Received: Oct. 8, 2022

    Accepted: Nov. 25, 2022

    Published Online: Apr. 25, 2023

    The Author Email: Zhang Pengfei (pfzhang@dlut.edu.cn)

    DOI:10.3788/CJL221304

    Topics