{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:45:44Z","timestamp":1760150744795,"version":"build-2065373602"},"reference-count":47,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2023,12,25]],"date-time":"2023-12-25T00:00:00Z","timestamp":1703462400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Portuguese Foundation for Science and Technology (FCT)","doi-asserted-by":"publisher","award":["UIDP&B\/04950\/2020","2020.05578.BD"],"award-info":[{"award-number":["UIDP&B\/04950\/2020","2020.05578.BD"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Imaging"],"abstract":"<jats:p>Background: Retinal texture has gained momentum as a source of biomarkers of neurodegeneration, as it is sensitive to subtle differences in the central nervous system from texture analysis of the neuroretina. Sex differences in the retina structure, as detected by layer thickness measurements from optical coherence tomography (OCT) data, have been discussed in the literature. However, the effect of sex on retinal interocular differences in healthy adults has been overlooked and remains largely unreported. Methods: We computed mean value fundus images for the neuroretina layers as imaged by OCT of healthy individuals. Texture metrics were obtained from these images to assess whether women and men have the same retina texture characteristics in both eyes. Texture features were tested for group mean differences between the right and left eye. Results: Corrected texture differences exist only in the female group. Conclusions: This work illustrates that the differences between the right and left eyes manifest differently in females and males. This further supports the need for tight control and minute analysis in studies where interocular asymmetry may be used as a disease biomarker, and the potential of texture analysis applied to OCT imaging to spot differences in the retina.<\/jats:p>","DOI":"10.3390\/jimaging10010006","type":"journal-article","created":{"date-parts":[[2023,12,25]],"date-time":"2023-12-25T23:00:12Z","timestamp":1703545212000},"page":"6","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["When Sex Matters: Differences in the Central Nervous System as Imaged by OCT through the Retina"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5821-7964","authenticated-orcid":false,"given":"Ana","family":"Nunes","sequence":"first","affiliation":[{"name":"Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, 3000-548 Coimbra, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2176-3923","authenticated-orcid":false,"given":"Pedro","family":"Serranho","sequence":"additional","affiliation":[{"name":"Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, 3000-548 Coimbra, Portugal"},{"name":"Department of Sciences and Technology, Universidade Aberta, 1269-001 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9465-4413","authenticated-orcid":false,"given":"Pedro","family":"Guimar\u00e3es","sequence":"additional","affiliation":[{"name":"Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, 3000-548 Coimbra, Portugal"}]},{"given":"Jo\u00e3o","family":"Ferreira","sequence":"additional","affiliation":[{"name":"Faculty of Sciences and Technology, University of Coimbra, 3030-201 Coimbra, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4364-6373","authenticated-orcid":false,"given":"Miguel","family":"Castelo-Branco","sequence":"additional","affiliation":[{"name":"Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, 3000-548 Coimbra, Portugal"},{"name":"Clinical Academic Center of Coimbra (CACC), Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6677-2754","authenticated-orcid":false,"given":"Rui","family":"Bernardes","sequence":"additional","affiliation":[{"name":"Coimbra Institute for Biomedical Imaging and Translational Research (CIBIT), Institute of Nuclear Sciences Applied to Health (ICNAS), University of Coimbra, 3000-548 Coimbra, Portugal"},{"name":"Clinical Academic Center of Coimbra (CACC), Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,12,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nrneurol.2012.227","article-title":"The retina as a window to the brain\u2014From eye research to CNS disorders","volume":"9","author":"London","year":"2013","journal-title":"Nat. Rev. Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"116","DOI":"10.17691\/stm2015.7.1.14","article-title":"Retinal optical coherence tomography in neurodegenerative diseases (review)","volume":"7","author":"Svetozarskiy","year":"2015","journal-title":"Sovrem. Tehnol. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"723","DOI":"10.3233\/JAD-190152","article-title":"Interplay between macular retinal changes and white matter integrity in early Alzheimer\u2019s disease","volume":"70","author":"Alves","year":"2019","journal-title":"J. Alzheimers Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1499","DOI":"10.1007\/s11357-020-00252-7","article-title":"Retinal biomarkers for Alzheimer\u2019s disease and vascular cognitive impairment and dementia (VCID): Implication for early diagnosis and prognosis","volume":"42","author":"Ungvari","year":"2020","journal-title":"GeroScience"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1002\/jnr.23895","article-title":"Sex differences in the human visual system","volume":"95","author":"Vanston","year":"2017","journal-title":"J. Neurosci. Res."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Hougaard, A., Jensen, B.H., Amin, F.M., Rostrup, E., Hoffmann, M.B., and Ashina, M. (2015). Cerebral asymmetry of fMRI-BOLD responses to visual stimulation. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0126477"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1167\/iovs.62.4.9","article-title":"Ocular dominance and functional asymmetry in visual attention networks","volume":"62","author":"Liu","year":"2021","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1080\/02713680802323140","article-title":"Analysis of macular thickness in British population using optical coherence tomography (OCT): An emphasis on interocular symmetry","volume":"33","author":"Hegde","year":"2008","journal-title":"Curr. Eye Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1177\/1120672118795062","article-title":"Normative posterior pole asymmetry analysis data in healthy Caucasian population","volume":"29","author":"Altan","year":"2019","journal-title":"Eur. J. Ophthalmol."},{"key":"ref_10","first-page":"127","article-title":"Effects of age and gender on macular thickness in healthy subjects using spectral optical coherence tomography\/scanning laser ophthalmoscopy","volume":"38","author":"Sukgen","year":"2018","journal-title":"Int. Ophthalmol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Ly, A., Banh, J., Luu, P., Huang, J., Yapp, M., and Zangerl, B. (2019). Interocular asymmetry of the superonasal retinal nerve fibre layer thickness and blood vessel diameter in healthy subjects. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0226728"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3875","DOI":"10.1167\/iovs.14-15663","article-title":"Normal value ranges for central retinal thickness asymmetry in healthy Caucasian adults measured by SPECTRALIS SD-OCT posterior pole asymmetry analysis","volume":"56","author":"Jacobsen","year":"2015","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1136\/bjophthalmol-2013-304345","article-title":"Interocular symmetry in retinal and optic nerve parameters in children as measured by spectral domain optical coherence tomography","volume":"98","author":"Antonios","year":"2014","journal-title":"Br. J. Ophthalmol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"955","DOI":"10.4103\/ijo.IJO_71_17","article-title":"Interocular symmetry of retinal nerve fiber layer and optic nerve head parameters measured by Cirrus high-definition optical coherence tomography in a normal pediatric population","volume":"65","author":"Pawar","year":"2017","journal-title":"Indian J. Ophthalmol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1038\/s41598-021-04563-3","article-title":"Interocular symmetry of optical coherence tomography parameters in healthy children and adolescents","volume":"12","author":"Song","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Adhi, M., Aziz, S., Muhammad, K., and Adhi, M.I. (2012). Macular thickness by age and gender in healthy eyes using spectral domain optical coherence tomography. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0037638"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"8769","DOI":"10.1167\/iovs.11-8388","article-title":"Effects of age, sex, and axial length on the three-dimensional profile of normal macular layer structures","volume":"52","author":"Ooto","year":"2011","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"213","DOI":"10.3109\/02713683.2014.952828","article-title":"Effects of sex and age on the normal retinal and choroidal structures on optical coherence tomography","volume":"40","author":"Ooto","year":"2015","journal-title":"Curr. Eye Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1364\/JOSAA.23.000521","article-title":"Bimodal spatial distribution of macular pigment: Evidence of a gender relationship","volume":"23","author":"Delori","year":"2006","journal-title":"J. Opt. Soc. Am. A"},{"key":"ref_20","first-page":"162","article-title":"Retinal thickness in Alzheimer\u2019s disease: A systematic review and meta-analysis","volume":"6","author":"Haan","year":"2017","journal-title":"Alzheimers Dement. Diagn. Assess. Dis. Monit."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s00401-016-1613-6","article-title":"Ocular indicators of Alzheimer\u2019s: Exploring disease in the retina","volume":"132","author":"Hart","year":"2016","journal-title":"Acta Neuropathol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1093\/brain\/awp068","article-title":"The retina in Parkinson\u2019s disease","volume":"132","author":"Archibald","year":"2009","journal-title":"Brain"},{"key":"ref_23","first-page":"433","article-title":"Potential role of retina as a progression of Parkinson\u2019s disease","volume":"4","author":"Tian","year":"2011","journal-title":"Int. J. Ophthalmol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Varga, B.E., Gao, W., Laurik, K.L., T\u00e1trai, E., Sim\u00f3, M., Somfai, G.M., and DeBuc, D.C. (2015). Investigating tissue optical properties and texture descriptors of the retina in patients with multiple sclerosis. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0143711"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Tazarjani, H.D., Amini, Z., Kafieh, R., Ashtari, F., and Sadeghi, E. (2021). Retinal OCT texture analysis for differentiating healthy controls from multiple sclerosis (MS) with\/without optic neuritis. BioMed Res. Int., 2021.","DOI":"10.1155\/2021\/5579018"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"66","DOI":"10.3389\/fendo.2018.00066","article-title":"Gonadal hormones and retinal disorders: A review","volume":"9","author":"Nuzzi","year":"2018","journal-title":"Front. Endocrinol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Nuzzi, R., and Caselgrandi, P. (2022). Sex hormones and their effects on ocular disorders and pathophysiology: Current aspects and our experience. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23063269"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"7521","DOI":"10.1038\/s41598-018-25298-8","article-title":"Sex-related differences in vision are heterogeneous","volume":"8","author":"Shaqiri","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1016\/S0002-9394(99)00481-X","article-title":"Interocular difference in progression of glaucoma correlates with interocular differences in retrobulbar circulation","volume":"129","author":"Schuman","year":"2000","journal-title":"Am. J. Ophthalmol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5536","DOI":"10.1038\/s41598-021-84937-9","article-title":"A multicenter study of interocular symmetry of corneal biometrics in Chinese myopic patients","volume":"11","author":"Xu","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1167\/iovs.61.14.23","article-title":"Assessing interocular symmetry of the foveal cone mosaic","volume":"61","author":"Cava","year":"2020","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Anantrasirichai, N., Achim, A., Morgan, J.E., Erchova, I., and Nicholson, L. (2013, January 7\u201311). SVM-based texture classification in optical coherence tomography. Proceedings of the 2013 IEEE 10th International Symposium on Biomedical Imaging, San Francisco, CA, USA.","DOI":"10.1109\/ISBI.2013.6556778"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Nunes, A., Silva, G., Duque, C., Janu\u00e1rio, C., Santana, I., Ambr\u00f3sio, A.F., Castelo-Branco, M., and Bernardes, R. (2019). Retinal texture biomarkers may help to discriminate between Alzheimer\u2019s, Parkinson\u2019s, and healthy controls. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0218826"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1109\/TIT.1962.1057698","article-title":"Visual pattern discrimination","volume":"8","author":"Julesz","year":"1962","journal-title":"IRE Trans. Inf. Theory"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Landy, M., and Movshon, J.A. (1991). Computational Models of Visual Processing, MIT Press.","DOI":"10.7551\/mitpress\/2002.001.0001"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1109\/TSMC.1973.4309314","article-title":"Textural features for image classification","volume":"SMC-3","author":"Haralick","year":"1973","journal-title":"IEEE Trans. Syst. Man Cybern."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1148\/radiology.213.2.r99nv49317","article-title":"Journey toward computer-aided diagnosis: Role of image texture analysis","volume":"213","author":"Tourassi","year":"1999","journal-title":"Radiology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1016\/j.crad.2004.07.008","article-title":"Texture analysis of medical images","volume":"59","author":"Castellano","year":"2004","journal-title":"Clin. Radiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1007\/s12553-020-00428-3","article-title":"Sexual dimorphism of the adult human retina assessed by optical coherence tomography","volume":"10","author":"Nunes","year":"2020","journal-title":"Health Technol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"World Medical Association (2013). World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA, 310, 2191\u20132194.","DOI":"10.1001\/jama.2013.281053"},{"key":"ref_41","first-page":"119","article-title":"Optimal surface segmentation in volumetric images\u2014A graph-theoretic approach","volume":"28","author":"Li","year":"2005","journal-title":"IEEE Trans. Pattern Anal. Mach. Intell."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1436","DOI":"10.1109\/TMI.2009.2016958","article-title":"Automated 3-D intraretinal layer segmentation of macular spectral-domain optical coherence tomography images","volume":"28","author":"Garvin","year":"2009","journal-title":"IEEE Trans. Med. Imaging"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1109\/RBME.2010.2084567","article-title":"Retinal imaging and image analysis","volume":"3","author":"Garvin","year":"2010","journal-title":"IEEE Rev. Biomed. Eng."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.compmedimag.2014.02.003","article-title":"Ocular fundus reference images from optical coherence tomography","volume":"38","author":"Rodrigues","year":"2014","journal-title":"Comput. Med. Imaging Graph."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1109\/36.752194","article-title":"Texture analysis of SAR sea ice imagery using gray level co-occurrence matrices","volume":"37","author":"Soh","year":"1999","journal-title":"IEEE Trans. Geosci. Remote Sens."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"45","DOI":"10.5589\/m02-004","article-title":"An analysis of co-occurrence texture statistics as a function of grey level quantization","volume":"28","author":"Clausi","year":"2002","journal-title":"Can. J. Remote Sens."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1111\/1467-9868.00346","article-title":"A direct approach to false discovery rates","volume":"64","author":"Storey","year":"2002","journal-title":"J. R. Stat. Soc. Ser. 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