Spectral Analysis of Light-Adapted Electroretinograms in Neurodevelopmental Disorders: Classification with Machine Learning
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
PubMed
39851292
PubMed Central
PMC11761560
DOI
10.3390/bioengineering12010015
PII: bioengineering12010015
Knihovny.cz E-resources
- Keywords
- attention deficit hyperactivity disorder, autism, biomarker, feature selection, medication, retina, sex,
- Publication type
- Journal Article MeSH
Electroretinograms (ERGs) show differences between typically developing populations and those with a diagnosis of autism spectrum disorder (ASD) or attention deficit/hyperactivity disorder (ADHD). In a series of ERGs collected in ASD (n = 77), ADHD (n = 43), ASD + ADHD (n = 21), and control (n = 137) groups, this analysis explores the use of machine learning and feature selection techniques to improve the classification between these clinically defined groups. Standard time domain and signal analysis features were evaluated in different machine learning models. For ASD classification, a balanced accuracy (BA) of 0.87 was achieved for male participants. For ADHD, a BA of 0.84 was achieved for female participants. When a three-group model (ASD, ADHD, and control) the BA was lower, at 0.70, and fell further to 0.53 when all groups were included (ASD, ADHD, ASD + ADHD, and control). The findings support a role for the ERG in establishing a broad two-group classification of ASD or ADHD, but the model's performance depends upon sex and is limited when multiple classes are included in machine learning modeling.
Biomedical Engineering Department University of Connecticut Storrs CT 06269 USA
College of Psychology and Education Flinders University Adelaide 5000 SA Australia
National Institute of Public Health Srobarova 48 100 00 Prague Czech Republic
Pattern Recognition Lab Friedrich Alexander Universität Erlangen Nürnberg 91058 Erlangen Germany
UCL Great Ormond Street Institute of Child Health University College London London WC1N 1EH UK
See more in PubMed
Parellada M., Andreu-Bernabeu Á., Burdeus M., San José Cáceres A., Urbiola E., Carpenter L.L., Kraguljac N.V., McDonald W.M., Nemeroff C.B., Rodriguez C.I., et al. In search of biomarkers to guide interventions in autism spectrum disorder: A Systematic Review. Am. J. Psychiatry. 2023;180:23–40. doi: 10.1176/appi.ajp.21100992. PubMed DOI PMC
London A., Benhar I., Schwartz M. The retina as a window to the brain—From eye research to CNS disorders. Nat. Rev. Neurol. 2013;9:44–53. doi: 10.1038/nrneurol.2012.227. PubMed DOI
Hébert M., Mérette C., Gagné A.M., Paccalet T., Moreau I., Lavoie J., Maziade M. The electroretinogram may differentiate schizophrenia from bipolar disorder. Biol. Psychiatry. 2020;87:263–270. doi: 10.1016/j.biopsych.2019.06.014. PubMed DOI
Asanad S., Felix C.M., Fantini M., Harrington M.G., Sadun A.A., Karanjia R. Retinal ganglion cell dysfunction in preclinical Alzheimer’s disease: An electrophysiologic biomarker signature. Sci. Rep. 2021;11:6344. doi: 10.1038/s41598-021-85010-1. PubMed DOI PMC
Schwitzer T., Le Cam S., Cosker E., Vinsard H., Leguay A., Angioi-Duprez K., Laprevote V., Ranta R., Schwan R., Dorr V.L. Retinal electroretinogram features can detect depression state and treatment response in adults: A machine learning approach. J. Affect. Disord. 2022;306:208–214. doi: 10.1016/j.jad.2022.03.025. PubMed DOI
Elanwar R., Al Masry H., Ibrahim A., Hussein M., Ibrahim S., Masoud M.M. Retinal functional and structural changes in patients with Parkinson’s disease. BMC Neurol. 2023;23:330. doi: 10.1186/s12883-023-03373-6. PubMed DOI PMC
Constable P.A., Lim J.K.H., Thompson D.A. Retinal electrophysiology in central nervous system disorders. A review of human and mouse studies. Front. Neurosci. 2023;17:1215097. doi: 10.3389/fnins.2023.1215097. PubMed DOI PMC
Schwitzer T., Leboyer M., Laprévote V., Louis Dorr V., Schwan R. Using retinal electrophysiology toward precision psychiatry. Eur. Psychiatry. 2022;65:e9. doi: 10.1192/j.eurpsy.2022.3. PubMed DOI PMC
Schwitzer T., Lavoie J., Giersch A., Schwan R., Laprevote V. The emerging field of retinal electrophysiological measurements in psychiatric research: A review of the findings and the perspectives in major depressive disorder. J. Psychiatr. Res. 2015;70:113–120. doi: 10.1016/j.jpsychires.2015.09.003. PubMed DOI
Ritvo E.R., Creel D., Realmuto G., Crandall A.S., Freeman B.J., Bateman J.B., Barr R., Pingree C., Coleman M., Purple R. Electroretinograms in autism: A pilot study of b-wave amplitudes. Am. J. Psychiatry. 1988;145:229–232. doi: 10.1176/ajp.145.2.229. PubMed DOI
Realmuto G., Purple R., Knobloch W., Ritvo E. Electroretinograms (ERGs) in four autistic probands and six first-degree relatives. Can. J. Psychiatry. 1989;34:435–439. doi: 10.1177/070674378903400513. PubMed DOI
Constable P.A., Gaigg S.B., Bowler D.M., Jägle H., Thompson D.A. Full-field electroretinogram in autism spectrum disorder. Doc. Ophthalmol. 2016;132:83–99. doi: 10.1007/s10633-016-9529-y. PubMed DOI
Constable P.A., Ritvo E.R., Ritvo A.R., Lee I.O., McNair M.L., Stahl D., Sowden J., Quinn S., Skuse D.H., Thompson D.A., et al. Light-Adapted electroretinogram differences in Autism Spectrum Disorder. J. Autism Dev. Disord. 2020;50:2874–2885. doi: 10.1007/s10803-020-04396-5. PubMed DOI
Constable P.A., Lee I.O., Marmolejo-Ramos F., Skuse D.H., Thompson D.A. The photopic negative response in autism spectrum disorder. Clin. Exp. Optom. 2021;104:841–847. doi: 10.1080/08164622.2021.1903808. PubMed DOI
Lee I.O., Skuse D.H., Constable P.A., Marmolejo-Ramos F., Olsen L.R., Thompson D.A. The electroretinogram b-wave amplitude: A differential physiological measure for Attention Deficit Hyperactivity Disorder and Autism Spectrum Disorder. J. Neurodev. Disord. 2022;14:30. doi: 10.1186/s11689-022-09440-2. PubMed DOI PMC
Constable P.A., Marmolejo-Ramos F., Gauthier M., Lee I.O., Skuse D.H., Thompson D.A. Discrete Wavelet Transform analysis of the electroretinogram in Autism Spectrum Disorder and Attention Deficit Hyperactivity Disorder. Front. Neurosci. 2022;16:890461. doi: 10.3389/fnins.2022.890461. PubMed DOI PMC
Friedel E.B.N., Schäfer M., Endres D., Maier S., Runge K., Bach M., Heinrich S.P., Ebert D., Domschke K., Tebartz van Elst L., et al. Electroretinography in adults with high-functioning autism spectrum disorder. Autism Res. 2022;15:2026–2037. doi: 10.1002/aur.2823. PubMed DOI
Huang Q., Ellis C.L., Leo S.M., Velthuis H., Pereira A.C., Dimitrov M., Ponteduro F.M., Wong N.M.L., Daly E., Murphy D.G.M., et al. Retinal GABAergic alterations in adults with Autism Spectrum Disorder. J. Neurosci. 2024;44:e1218232024. doi: 10.1523/JNEUROSCI.1218-23.2024. PubMed DOI PMC
Bubl E., Dörr M., Riedel A., Ebert D., Philipsen A., Bach M., Tebartz van Elst L. Elevated background noise in adult attention deficit hyperactivity disorder is associated with inattention. PLoS ONE. 2015;10:e0118271. doi: 10.1371/journal.pone.0118271. PubMed DOI PMC
Dubois M.A., Pelletier C.A., Mérette C., Jomphe V., Turgeon R., Bélanger R.E., Grondin S., Hébert M. Evaluation of electroretinography (ERG) parameters as a biomarker for ADHD. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2023;127:110807. doi: 10.1016/j.pnpbp.2023.110807. PubMed DOI
Hamilton R., Bees M.A., Chaplin C.A., McCulloch D.L. The luminance-response function of the human photopic electroretinogram: A mathematical model. Vision. Res. 2007;47:2968–2972. doi: 10.1016/j.visres.2007.04.020. PubMed DOI
Constable P.A., Skuse D.H., Thompson D.A., Lee I.O. Brief report: Effects of methylphenidate on the light adapted electroretinogram. Doc. Ophthalmol. 2024 doi: 10.1007/s10633-024-10000-3. PubMed DOI
Robson A.G., Frishman L.J., Grigg J., Hamilton R., Jeffrey B.G., Kondo M., Li S., McCulloch D.L. ISCEV standard for full-field clinical electroretinography (2022 update) Doc. Ophthalmol. 2022;144:165–177. doi: 10.1007/s10633-022-09872-0. PubMed DOI PMC
Manjur S.M., Diaz L.R.M., Lee I.O., Skuse D.H., Thompson D.A., Marmolejos-Ramos F., Constable P.A., Posada-Quintero H.F. Detecting Autism Spectrum Disorder and Attention Deficit Hyperactivity Disorder using multimodal time-frequency analysis with machine learning using the electroretinogram from two flash strengths. J. Autism Dev. Disord. 2024 doi: 10.1007/s10803-024-06290-w. PubMed DOI
Manjur S.M., Hossain M.B., Constable P.A., Thompson D.A., Marmolejo-Ramos F., Lee I.O., Posada-Quintero H.F. Spectral analysis of Electroretinography to differentiate autism spectrum disorder and attention deficit hyperactivity disorder; Proceedings of the 2023 IEEE EMBS International Conference on Biomedical and Health Informatics (BHI); Pittsburgh, PA, USA. 15–18 October 2023; p. 10313406. DOI
Manjur S.M., Hossain M.B., Constable P.A., Thompson D.A., Marmolejo-Ramos F., Lee I.O., Skuse D.H., Posada-Quintero H.F. Detecting Autism Spectrum Disorder using spectral analysis of electroretinogram and machine learning: Preliminary results. IEEE Trans. Biomed. Eng. 2022;2022:435–3438. doi: 10.1109/EMBC48229.2022.9871173. PubMed DOI
Gauvin M., Sustar M., Little J.M., Brecelj J., Lina J.M., Lachapelle P. Quantifying the ON and OFF Contributions to the Flash ERG with the Discrete Wavelet Transform. Transl. Vis. Sci. Technol. 2017;6:3. doi: 10.1167/tvst.6.1.3. PubMed DOI PMC
Gauvin M., Dorfman A.L., Trang N., Gauthier M., Little J.M., Lina J.M., Lachapelle P. Assessing the contribution of the oscillatory potentials to the genesis of the photopic ERG with the Discrete Wavelet Transform. Biomed. Res. Int. 2016;2016:2790194. doi: 10.1155/2016/2790194. PubMed DOI PMC
Gauvin M., Little J.M., Lina J.M., Lachapelle P. Functional decomposition of the human ERG based on the discrete wavelet transform. J. Vis. 2015;15:14. doi: 10.1167/15.16.14. PubMed DOI
Gauvin M., Lina J.M., Lachapelle P. Advance in ERG analysis: From peak time and amplitude to frequency, power, and energy. Biomed. Res. Int. 2014;2014:246096. doi: 10.1155/2014/246096. PubMed DOI PMC
Wang H., Siu K., Ju K., Chon K.H. A high resolution approach to estimating time-frequency spectra and their amplitudes. Ann. Biomed. Eng. 2006;34:326–338. doi: 10.1007/s10439-005-9035-y. PubMed DOI
Habib F., Huang H., Gupta A., Wright T. MERCI: A machine learning approach to identifying hydroxychloroquine retinopathy using mfERG. Doc. Ophthalmol. 2022;145:53–63. doi: 10.1007/s10633-022-09879-7. PubMed DOI
Gajendran M.K., Rohowetz L.J., Koulen P., Mehdizadeh A. Novel Machine-Learning based framework using electroretinography data for the detection of early-stage glaucoma. Front. Neurosci. 2022;16:869137. doi: 10.3389/fnins.2022.869137. PubMed DOI PMC
Glinton S.L., Calcagni A., Lilaonitkul W., Pontikos N., Vermeirsch S., Zhang G., Arno G., Wagner S.K., Michaelides M., Keane P.A., et al. Phenotyping of ABCA4 retinopathy by Machine Learning analysis of full-field electroretinography. Transl. Vis. Sci. Technol. 2022;11:34. doi: 10.1167/tvst.11.9.34. PubMed DOI PMC
Müller P.L., Treis T., Odainic A., Pfau M., Herrmann P., Tufail A., Holz F.G. Prediction of function in ABCA4-related retinopathy using ensemble Machine Learning. J. Clin. Med. 2020;9:2428. doi: 10.3390/jcm9082428. PubMed DOI PMC
Martinez S., Stoyanov K., Carcache L. Unraveling the spectrum: Overlap, distinctions, and nuances of ADHD and ASD in children. Front. Psychiatry. 2024;15:1387179. doi: 10.3389/fpsyt.2024.1387179. PubMed DOI PMC
Berg L.M., Gurr C., Leyhausen J., Seelemeyer H., Bletsch A., Schaefer T., Ecker C. The neuroanatomical substrates of autism and ADHD and their link to putative genomic underpinnings. Mol. Autism. 2023;14:36. doi: 10.1186/s13229-023-00568-z. PubMed DOI PMC
Knott R., Johnson B.P., Tiego J., Mellahn O., Finlay A., Kallady K., Bellgrove M. The Monash Autism-ADHD genetics and neurodevelopment (MAGNET) project design and methodologies: A dimensional approach to understanding neurobiological and genetic aetiology. Mol. Autism. 2021;12:55. doi: 10.1186/s13229-021-00457-3. PubMed DOI PMC
Xu M., Calhoun V., Jiang R., Yan W., Sui J. Brain imaging-based machine learning in autism spectrum disorder: Methods and applications. J. Neurosci. Methods. 2021;361:109271. doi: 10.1016/j.jneumeth.2021.109271. PubMed DOI PMC
Liu M., Li B., Hu D. Autism Spectrum Disorder studies using fMRI data and machine learning: A review. Front. Neurosci. 2021;15:697870. doi: 10.3389/fnins.2021.697870. PubMed DOI PMC
Ingalhalikar M., Shinde S., Karmarkar A., Rajan A., Rangaprakash D., Deshpande G. Functional connectivity-based prediction of autism on site harmonized ABIDE Dataset. IEEE Trans. Biomed. Eng. 2021;68:3628–3637. doi: 10.1109/TBME.2021.3080259. PubMed DOI PMC
Sá R.O.D.S., Michelassi G.C., Butrico D.D.S., Franco F.O., Sumiya F.M., Portolese J., Brentani H., Nunes F.L.S., Machado-Lima A. Enhancing ensemble classifiers utilizing gaze tracking data for autism spectrum disorder diagnosis. Comput. Biol. Med. 2024;182:109184. doi: 10.1016/j.compbiomed.2024.109184. PubMed DOI
Wei Q., Dong W., Yu D., Wang K., Yang T., Xiao Y., Long D., Xiong H., Chen J., Xu X., et al. Early identification of autism spectrum disorder based on machine learning with eye-tracking data. J. Affect. Disord. 2024;358:326–334. doi: 10.1016/j.jad.2024.04.049. PubMed DOI
Ranaut A., Khandnor P., Chand T. Identifying autism using EEG: Unleashing the power of feature selection and machine learning. Biomed. Phys. Eng. Express. 2024;10:035013. doi: 10.1088/2057-1976/ad31fb. PubMed DOI
Posada-Quintero H.F., Manjur S.M., Hossain M.B., Marmolejo-Ramos F., Lee I.O., Skuse D.H., Thompson D.A., Constable P.A. Autism spectrum disorder detection using variable frequency complex demodulation of the electroretinogram. Res. Aut. Spectr. Disord. 2023;109:102258. doi: 10.1016/j.rasd.2023.102258. DOI
Chawla N.V., Bowyer K.W., Hall L.O., Kegelmeyer W.P. SMOTE: Synthetic minority over-sampling technique. J. Artif. Intell. Res. 2002;16:321–357. doi: 10.1613/jair.953. DOI
Saeb S., Lonini L., Jayaraman A., Mohr D.C., Kording K.P. The need to approximate the use-case in clinical machine learning. Gigascience. 2017;6:1–9. doi: 10.1093/gigascience/gix019. PubMed DOI PMC
Chen R.-C., Dewi C., Huang S.-W., Caraka R.E. Selecting critical features for data classification based on machine learning methods. J. Big Data. 2020;7:52. doi: 10.1186/s40537-020-00327-4. DOI
Chandrashekar G., Sahin F. A survey on feature selection methods. Comput. Electr. Eng. 2014;40:16–28. doi: 10.1016/j.compeleceng.2013.11.024. DOI
Prasetiyowati M.I., Maulidevi N.U., Surendro K. Determining threshold value on information gain feature selection to increase speed and prediction accuracy of random forest. J. Big Data. 2021;8:84. doi: 10.1186/s40537-021-00472-4. DOI
Fryer D., Strümke I., Nguyen G. Shapley values for feature selection: The good, the bad, and the axioms. IEEE Access. 2021;9:144352–144360. doi: 10.1109/ACCESS.2021.3119110. DOI
Gramegna A., Giudici P. Shapley feature selection. FinTech. 2022;1:72–80. doi: 10.3390/fintech1010006. DOI
Rozemberczki B., Watson L., Bayer P., Yang H.-T., Kiss O., Nilsson S., Sarkar R. The shapley value in machine learning. arXiv. 2022 doi: 10.48550/arXiv.2202.05594.2202.05594 DOI
Witkovsky P. Dopamine and retinal function. Doc. Ophthalmol. 2004;108:17–40. doi: 10.1023/B:DOOP.0000019487.88486.0a. PubMed DOI
Wang J., Zhang L., Wang Q., Chen L., Shi J., Chen X., Li Z., Shen D. Multi-Class ASD classification based on functional connectivity and functional correlation tensor via multi-source domain adaptation and multi-view sparse representation. IEEE Trans. Med. Imaging. 2020;39:3137–3147. doi: 10.1109/TMI.2020.2987817. PubMed DOI
Al-Hiyali M.I., Yahya N., Faye I., Hussein A.F. Identification of autism subtypes based on Wavelet Coherence of BOLD FMRI signals using Convolutional Neural Network. Sensors. 2021;21:5256. doi: 10.3390/s21165256. PubMed DOI PMC
Waterhouse L. Heterogeneity thwarts autism explanatory power: A proposal for endophenotypes. Front. Psychiatry. 2022;13:947653. doi: 10.3389/fpsyt.2022.947653. PubMed DOI PMC
Jacob S., Wolff J.J., Steinbach M.S., Doyle C.B., Kumar V., Elison J.T. Neurodevelopmental heterogeneity and computational approaches for understanding autism. Transl. Psychiatry. 2019;9:63. doi: 10.1038/s41398-019-0390-0. PubMed DOI PMC
Santos S., Ferreira H., Martins J., Gonçalves J., Castelo-Branco M. Male sex bias in early and late onset neurodevelopmental disorders: Shared aspects and differences in Autism Spectrum Disorder, Attention Deficit/hyperactivity Disorder, and Schizophrenia. Neurosci. Biobehav. Rev. 2022;135:104577. doi: 10.1016/j.neubiorev.2022.104577. PubMed DOI
Raman S.R., Man K.K.C., Bahmanyar S., Berard A., Bilder S., Boukhris T., Bushnell G., Crystal S., Furu K., KaoYang Y.-H., et al. Trends in attention-deficit hyperactivity disorder medication use: A retrospective observational study using population-based databases. Lancet Psychiatry. 2018;5:824–835. doi: 10.1016/S2215-0366(18)30293-1. PubMed DOI
Werner A.L., Tebartz van Elst L., Ebert D., Friedel E., Bubl A., Clement H.W., Lukačin R., Bach M., Bubl E. Normalization of increased retinal background noise after ADHD treatment: A neuronal correlate. Schizophr. Res. 2020;219:77–83. doi: 10.1016/j.schres.2019.04.013. PubMed DOI
Gustafsson U., Hansen M. QbTest for monitoring medication treatment response in ADHD: A Systematic Review. Clin. Pract. Epidemiol. Ment. Health. 2023;19:e17450179276630. doi: 10.2174/0117450179276630231030093814. PubMed DOI PMC
Lord C., Rutter M., Goode S., Heemsbergen J., Jordan H., Mawhood L., Schopler E. Autism diagnostic observation schedule: A standardized observation of communicative and social behavior. J. Autism Dev. Disord. 1989;19:185–212. doi: 10.1007/BF02211841. PubMed DOI
Skuse D., Warrington R., Bishop D., Chowdhury U., Lau J., Mandy W., Place M. The developmental, dimensional and diagnostic interview (3di): A novel computerized assessment for autism spectrum disorders. J. Am. Acad. Child. Adolesc. Psychiatry. 2004;43:548–558. doi: 10.1097/00004583-200405000-00008. PubMed DOI
Ruigrok A.N.V., Lai M.C. Sex/gender differences in neurology and psychiatry: Autism. Handb. Clin. Neurol. 2020;175:283–297. doi: 10.1016/B978-0-444-64123-6.00020-5. PubMed DOI
Lai M.C., Lerch J.P., Floris D.L., Ruigrok A.N., Pohl A., Lombardo M.V., Baron-Cohen S. Imaging sex/gender and autism in the brain: Etiological implications. J. Neurosci. Res. 2017;95:380–397. doi: 10.1002/jnr.23948. PubMed DOI
Muñoz-Suazo M.D., Navarro-Muñoz J., Díaz-Román A., Porcel-Gálvez A.M., Gil-García E. Sex differences in neuropsychological functioning among children with attention-deficit/hyperactivity disorder. Psychiatry Res. 2019;278:289–293. doi: 10.1016/j.psychres.2019.06.028. PubMed DOI
Hollis C., Hall C.L., Guo B., James M., Boadu J., Groom M.J., Brown N., Kaylor-Hughes C., Moldavsky M., Valentine A.Z., et al. The impact of a computerised test of attention and activity (QbTest) on diagnostic decision-making in children and young people with suspected attention deficit hyperactivity disorder: Single-blind randomised controlled trial. J. Child. Psychol. Psychiatry. 2018;59:1298–1308. doi: 10.1111/jcpp.12921. PubMed DOI PMC
Soker-Elimaliah S., Lehrfield A., Scarano S.R., Wagner J.B. Associations between the pupil light reflex and the broader autism phenotype in children and adults. Front. Hum. Neurosci. 2022;16:1052604. doi: 10.3389/fnhum.2022.1052604. PubMed DOI PMC
Krishnappa Babu P.R., Aikat V., Di Martino J.M., Chang Z., Perochon S., Espinosa S., Aiello R., L H Carpenter K., Compton S., Davis N., et al. Blink rate and facial orientation reveal distinctive patterns of attentional engagement in autistic toddlers: A digital phenotyping approach. Sci. Rep. 2023;13:7158. doi: 10.1038/s41598-023-34293-7. PubMed DOI PMC
Benabderrahmane B., Gharzouli M., Benlecheb A. A novel multi-modal model to assist the diagnosis of autism spectrum disorder using eye-tracking data. Health Inf. Sci. Syst. 2024;12:40. doi: 10.1007/s13755-024-00299-2. PubMed DOI PMC
Tuesta R., Harris R., Posada-Quintero H.F. Circuit and sensor design for smartphone-based electroretinography; Proceedings of the IEEE 20th International Conference on Body Sensor Networks (BSN); Chicago, IL, USA. 15–17 October 2024; p. 10780451. DOI
Cordoba N., Daza S., Constable P.A., Posada-Quintero H.F. Design of a smartphone-based clinical electroretinogram recording system; Proceedings of the IEEE International Symposium on Medical Measurements and Applications (MeMeA); Eindhoven, The Netherlands. 26–28 June 2024; pp. 1–2. DOI
Huddy O., Tomas A., Manjur S.M., Posada-Quintero H.F. Prototype for Smartphone-based Electroretinogram; Proceedings of the IEEE 19th International Conference on Body Sensor Networks (BSN); Boston, MA, USA. 9–11 October 2023; pp. 1–4. DOI
Zhdanov A., Dolganov A., Zanca D., Borisov V., Ronkin M. Advanced analysis of electroretinograms based on wavelet scalogram processing. Appl. Sci. 2022;12:12365. doi: 10.3390/app122312365. DOI
Kulyabin M., Zhdanov A., Dolganov A., Ronkin M., Borisov V., Maier A. Enhancing electroretinogram classification with multi-wavelet analysis and visual transformer. Sensors. 2023;23:8727. doi: 10.3390/s23218727. PubMed DOI PMC
Zhdanov A., Constable P., Manjur S.M., Dolganov A., Posada-Quintero H.F., Lizunov A. OculusGraphy: Signal analysis of the electroretinogram in a rabbit model of endophthalmitis using discrete and continuous wavelet transforms. Bioengineering. 2023;10:708. doi: 10.3390/bioengineering10060708. PubMed DOI PMC
Sarossy M., Crowston J., Kumar D., Weymouth A., Wu Z. Time-frequency analysis of ERG with discrete wavelet transform and matching pursuits for glaucoma. Transl. Vis. Sci. Technol. 2022;11:19. doi: 10.1167/tvst.11.10.19. PubMed DOI PMC
Dorfman A.L., Gauvin M., Vatcher D., Little J.M., Polomeno R.C., Lachapelle P. Ring analysis of multifocal oscillatory potentials (mfOPs) in cCSNB suggests near-normal ON-OFF pathways at the fovea only. Doc. Ophthalmol. 2020;141:99–109. doi: 10.1007/s10633-020-09755-2. PubMed DOI
Brandao L.M., Monhart M., Schötzau A., Ledolter A.A., Palmowski-Wolfe A.M. Wavelet decomposition analysis in the two-flash multifocal ERG in early glaucoma: A comparison to ganglion cell analysis and visual field. Doc. Ophthalmol. 2017;135:29–42. doi: 10.1007/s10633-017-9593-y. PubMed DOI PMC
Ramsay J.O., Silverman B.W. Functional Data Analysis. Springer; New York, NY, USA: 2005.
Ramsay J.O. When the data are functions. Psychometrika. 1982;47:379–396. doi: 10.1007/BF02293704. DOI
Brabec M., Constable P.A., Thompson D.A., Marmolejo-Ramos F. Group comparisons of the individual electroretinogram time trajectories for the ascending limb of the b-wave using a raw and registered time series. BMC Res. Notes. 2023;16:238. doi: 10.1186/s13104-023-06535-4. PubMed DOI PMC
Maturo F., Verde R. Pooling random forest and functional data analysis for biomedical signals supervised classification: Theory and application to electrocardiogram data. Stat. Med. 2022;41:2247–2275. doi: 10.1002/sim.9353. PubMed DOI PMC
Kulyabin M., Zhdanov A., Maier A., Loh L., Estevez J.J., Constable P.A. Generating synthetic light-adapted electroretinogram waveforms using artificial intelligence to improve classification of retinal conditions in under-represented populations. J. Ophthalmol. 2024;2024:1990419. doi: 10.1155/2024/1990419. PubMed DOI PMC
Kulyabin M., Constable P.A., Zhdanov A., Lee I.O., Thompson D.A., Maier A. Attention to the electroretinogram: Gated Multilayer Perceptron for ASD classification. IEEE Access. 2024;12:52352–52362. doi: 10.1109/ACCESS.2024.3386638. DOI
Masland R.H. The neuronal organization of the retina. Neuron. 2012;76:266–280. doi: 10.1016/j.neuron.2012.10.002. PubMed DOI PMC
Bhatt Y., Hunt D.M., Carvalho L.S. The origins of the full-field flash electroretinogram b-wave. Front. Mol. Neurosci. 2023;16:1153934. doi: 10.3389/fnmol.2023.1153934. PubMed DOI PMC
Thompson D.A., Feather S., Stanescu H.C., Freudenthal B., Zdebik A.A., Warth R., Ognjanovic M., Hulton S.A., Wassmer E., Russell-Eggitt I., et al. Altered electroretinograms in patients with KCNJ10 mutations and EAST syndrome. J. Physiol. 2011;589:1681–1689. doi: 10.1113/jphysiol.2010.198531. PubMed DOI PMC
Kaneda M. Signal processing in the mammalian retina. J. Nippon. Med. Sch. 2013;80:16–24. doi: 10.1272/jnms.80.16. PubMed DOI
Severns M.L., Johnson M.A. The variability of the b-wave of the electroretinogram with stimulus luminance. Doc. Ophthalmol. 1993;84:291–299. doi: 10.1007/BF01203661. PubMed DOI
Hanna M.C., Calkins D.J. Expression and sequences of genes encoding glutamate receptors and transporters in primate retina determined using 3’-end amplification polymerase chain reaction. Mol. Vis. 2006;12:961–976. PubMed
Hanna M.C., Calkins D.J. Expression of genes encoding glutamate receptors and transporters in rod and cone bipolar cells of the primate retina determined by single-cell polymerase chain reaction. Mol. Vis. 2007;13:2194–2208. PubMed
Bush R.A., Sieving P.A. A proximal retinal component in the primate photopic ERG a-wave. Investig. Ophthalmol. Vis. Sci. 1994;35:635–645. PubMed
Robson J.G., Saszik S.M., Ahmed J., Frishman L.J. Rod and cone contributions to the a-wave of the electroretinogram of the macaque. J. Physiol. 2003;547:509–530. doi: 10.1113/jphysiol.2002.030304. PubMed DOI PMC
Friedburg C., Allen C.P., Mason P.J., Lamb T.D. Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram. J. Physiol. 2004;556:819–834. doi: 10.1113/jphysiol.2004.061523. PubMed DOI PMC
Diamond J.S. Inhibitory interneurons in the retina: Types, circuitry, and function. Annu. Rev. Vis. Sci. 2017;3:1–24. doi: 10.1146/annurev-vision-102016-061345. PubMed DOI
Wachtmeister L. Some aspects of the oscillatory response of the retina. Prog. Brain Res. 2001;131:465–474. doi: 10.1016/s0079-6123(01)31037-3. PubMed DOI
Wachtmeister L. Oscillatory potentials in the retina: What do they reveal. Prog. Retin. Eye Res. 1998;17:485–521. doi: 10.1016/S1350-9462(98)00006-8. PubMed DOI
Frishman L., Sustar M., Kremers J., McAnany J.J., Sarossy M., Tzekov R., Viswanathan S. ISCEV extended protocol for the photopic negative response (PhNR) of the full-field electroretinogram. Doc. Ophthalmol. 2018;136:207–211. doi: 10.1007/s10633-018-9638-x. PubMed DOI PMC
Viswanathan S., Frishman L.J., Robson J.G., Walters J.W. The photopic negative response of the flash electroretinogram in primary open angle glaucoma. Invest. Ophthalmol. Vis. Sci. 2001;42:514–522. PubMed
Asi H., Perlman I. Relationships between the electroretinogram a-wave, b-wave and oscillatory potentials and their application to clinical diagnosis. Doc. Ophthalmol. 1992;79:125–139. doi: 10.1007/BF00156572. PubMed DOI
Robson A.G., Nilsson J., Li S., Jalali S., Fulton A.B., Tormene A.P., Holder G.E., Brodie S.E. ISCEV guide to visual electrodiagnostic procedures. Doc. Ophthalmol. 2018;136:1–26. doi: 10.1007/s10633-017-9621-y. PubMed DOI PMC
American Psychiatric Association . DSM IV Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association; Washington, DC, USA: 1994.
American Psychiatric Association . In: Diagnostic and Statistical Manual of Mental Disorders V. Adamczyk R., editor. American Psychiatric Association; Arlington, VA, USA: 2013.
Gotham K., Risi S., Pickles A., Lord C. The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity. J. Autism Dev. Disord. 2007;37:613–627. doi: 10.1007/s10803-006-0280-1. PubMed DOI
Schopler E., Van Bourgondien M.E., Wellman G.J., Love S.R. Childhood Autism Rating Scale, Second Edition (CARS-2) Western Psychological Services; Torrance, CA, USA: 2010.
Hobby A.E., Kozareva D., Yonova-Doing E., Hossain I.T., Katta M., Huntjens B., Hammond C.J., Binns A.M., Mahroo O.A. Effect of varying skin surface electrode position on electroretinogram responses recorded using a handheld stimulating and recording system. Doc. Ophthalmol. 2018;137:79–86. doi: 10.1007/s10633-018-9652-z. PubMed DOI PMC
Al Abdlseaed A., McTaggart Y., Ramage T., Hamilton R., McCulloch D.L. Light- and dark-adapted electroretinograms (ERGs) and ocular pigmentation: Comparison of brown- and blue-eyed cohorts. Doc. Ophthalmol. 2010;121:135–146. doi: 10.1007/s10633-010-9240-3. PubMed DOI