{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T21:52:10Z","timestamp":1787003530519,"version":"build-2736575974"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,7,17]],"date-time":"2017-07-17T00:00:00Z","timestamp":1500249600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,7,17]],"date-time":"2017-07-17T00:00:00Z","timestamp":1500249600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Glaucoma is a disease characterized by pathologic changes in inner retinal layers, which are comprised of retinal ganglion cells (RGCs). As retinal ganglion cells (RGCs) cross over other retinal neurons that are connected by synapses, it is meaningful to investigate the outer retinal changes in glaucoma. We evaluated the association between thicknesses of segmented retinal layers in macular region and severity of visual field loss in open-angle glaucoma (OAG). This study involved 103 glaucomatous eyes. Retinal nerve fiber layer (RNFL), ganglion cell layer (GCL), inner plexiform layer (IPL), inner nuclear layer (INL), outer plexiform layer (OPL), and outer nuclear layer (ONL) thicknesses were measured at the macular level using the Spectral-domain optical coherence tomography with segmentation software. The functional losses were measured using 24-2 standard automated perimetry. Macular structure losses were positively correlated with functional loss for RNFL, GCL, and IPL (\n                    <jats:italic>R<\/jats:italic>\n                    \u2009=\u20090.550, 0.637, and 0.649, respectively,\n                    <jats:italic>P<\/jats:italic>\n                    \u2009&lt;\u20090.001) and negatively correlated with INL (\n                    <jats:italic>R<\/jats:italic>\n                    \u2009=\u2009\u22120.295,\n                    <jats:italic>P<\/jats:italic>\n                    \u2009=\u20090.041). By multivariate regression analysis, INL thickness was significantly associated with visual field mean deviation (dB) and optic disc hemorrhage. These finding carefully suggest reactive responses of neuronal or glial cells located in the INL occur during glaucoma progression.\n                  <\/jats:p>","DOI":"10.1038\/s41598-017-05282-4","type":"journal-article","created":{"date-parts":[[2017,7,11]],"date-time":"2017-07-11T05:32:31Z","timestamp":1499751151000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Relationship between Retinal Inner Nuclear Layer Thickness and Severity of Visual Field Loss in Glaucoma"],"prefix":"10.1038","volume":"7","author":[{"given":"Eun Kyoung","family":"Kim","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hae-Young Lopilly","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chan Kee","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,7,17]]},"reference":[{"key":"5282_CR1","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1001\/archopht.118.2.235","volume":"118","author":"TM Nork","year":"2000","unstructured":"Nork, T. M. et al. Swelling and loss of photoreceptors in chronic human and experimental glaucomas. Arch Ophthalmol. \n                           118, 235\u2013245 (2000).","journal-title":"Arch Ophthalmol."},{"key":"5282_CR2","first-page":"2532","volume":"33","author":"S Panda","year":"1992","unstructured":"Panda, S. & Jonas, J. B. Decreased photoreceptor count in human eyes with secondary angle-closure glaucoma. Invest Ophthalmol Vis Sci. \n                           33, 2532\u20132536 (1992).","journal-title":"Invest Ophthalmol Vis Sci."},{"key":"5282_CR3","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1136\/bjo.85.4.397","volume":"85","author":"IM Velten","year":"2001","unstructured":"Velten, I. M., Korth, M. & Horn, F. K. The a-wave of the dark adapted electroretinogram in glaucomas: are photoreceptors affected? Br J Ophthalmol. \n                           85, 397\u2013402 (2001).","journal-title":"Br J Ophthalmol."},{"key":"5282_CR4","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1097\/00061198-200004000-00006","volume":"9","author":"K Holopigian","year":"2000","unstructured":"Holopigian, K., Greenstein, V. C., Seiple, W., Hood, D. C. & Ritch, R. Electrophysiologic assessment of photoreceptor function in patients with primary open-angle glaucoma. J Glaucoma. \n                           9, 163\u2013168 (2000).","journal-title":"J Glaucoma."},{"key":"5282_CR5","first-page":"125","volume":"37","author":"LJ Frishman","year":"1996","unstructured":"Frishman, L. J. et al. The scotopic electroretinogram of macaque after retinal ganglion cell loss from experimental glaucoma. Invest Ophthalmol Vis Sci. \n                           37, 125\u2013141 (1996).","journal-title":"Invest Ophthalmol Vis Sci."},{"key":"5282_CR6","doi-asserted-by":"publisher","first-page":"628","DOI":"10.1093\/brain\/awp001","volume":"132","author":"P Jindahra","year":"2009","unstructured":"Jindahra, P., Petrie, A. & Plant, G. T. Retrograde trans-synaptic retinal ganglion cell loss identified by optical coherence tomography. Brain. \n                           132, 628\u2013634 (2009).","journal-title":"Brain."},{"key":"5282_CR7","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.jaapos.2014.10.025","volume":"19","author":"J Abbasian","year":"2015","unstructured":"Abbasian, J. et al. Macular optical coherence tomography in patients with unilateral optic nerve hypoplasia. J AAPOS. \n                           19, 57\u201361 (2015).","journal-title":"J AAPOS."},{"key":"5282_CR8","doi-asserted-by":"publisher","first-page":"1292","DOI":"10.1016\/j.ophtha.2012.11.021","volume":"120","author":"HL Park","year":"2013","unstructured":"Park, H. L., Park, Y. G., Cho, A. H. & Park, C. K. Transneuronal retrograde degeneration of the retinal ganglion cells in patients with cerebral infarction. Ophthalmology. \n                           120, 1292\u20131299 (2013).","journal-title":"Ophthalmology."},{"key":"5282_CR9","doi-asserted-by":"publisher","first-page":"2305","DOI":"10.1016\/j.ophtha.2009.05.025","volume":"116","author":"O Tan","year":"2009","unstructured":"Tan, O. et al. Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography. Ophthalmology. \n                           116, 2305\u20132314 (2009).","journal-title":"Ophthalmology."},{"key":"5282_CR10","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1001\/archophthalmol.2009.145","volume":"127","author":"M Wang","year":"2009","unstructured":"Wang, M. et al. Measurement of local retinal ganglion cell layer thickness in patients with glaucoma using frequency domain optical coherence tomography. Arch Ophthalmol. \n                           127, 875\u2013881 (2009).","journal-title":"Arch Ophthalmol."},{"key":"5282_CR11","doi-asserted-by":"publisher","first-page":"1437","DOI":"10.1001\/archopht.1978.03910060185017","volume":"96","author":"MA Mosier","year":"1978","unstructured":"Mosier, M. A., Lieberman, M. F., Green, W. R. & Knox, D. L. Hypoplasia of the optic nerve. Arch Ophthalmol. \n                           96, 1437\u20131442 (1978).","journal-title":"Arch Ophthalmol."},{"key":"5282_CR12","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1016\/j.media.2014.03.004","volume":"18","author":"F Rathke","year":"2014","unstructured":"Rathke, F., Schmidt, S. & Schnorr, C. Probabilistic intra-retinal layer segmentation in 3-D OCT images using global shape regularization. Med Image Anal. \n                           18, 781\u2013794 (2014).","journal-title":"Med Image Anal."},{"key":"5282_CR13","unstructured":"Hodapp, E., Parish, R. K., II, Anderson, D. R. Syntax of referencing in Clinical decisions in glaucoma. 52\u201361 (The C.V. Mosby Co., 1993)."},{"key":"5282_CR14","doi-asserted-by":"publisher","first-page":"1330","DOI":"10.1016\/j.ophtha.2015.03.020","volume":"122","author":"A Pilat","year":"2015","unstructured":"Pilat, A., Sibley, D., McLean, R. J., Proudlock, F. A. & Gottlob, I. High-resolution imaging of the optic nerve and retina in optic nerve hypoplasia. Ophthalmology. \n                           122, 1330\u20131339 (2015).","journal-title":"Ophthalmology."},{"key":"5282_CR15","doi-asserted-by":"publisher","first-page":"1809","DOI":"10.1016\/S0161-6420(00)00284-0","volume":"107","author":"DF Garway-Heath","year":"2000","unstructured":"Garway-Heath, D. F., Poinoosawmy, D., Fitzke, F. W. & Hitchings, R. A. Mapping the visual field to the optic disc in normal tension glaucoma eyes. Ophthalmology. \n                           107, 1809\u20131815 (2000).","journal-title":"Ophthalmology."},{"key":"5282_CR16","doi-asserted-by":"publisher","first-page":"2012","DOI":"10.1167\/iovs.04-0335","volume":"46","author":"H Ishikawa","year":"2005","unstructured":"Ishikawa, H. et al. Macular segmentation with optical coherence tomography. Invest Ophthalmol Vis Sci. \n                           46, 2012\u20132017 (2005).","journal-title":"Invest Ophthalmol Vis Sci."},{"key":"5282_CR17","doi-asserted-by":"publisher","first-page":"1892","DOI":"10.1167\/iovs.15-18119","volume":"57","author":"LJ Wilsey","year":"2016","unstructured":"Wilsey, L. J., Reynaud, J., Cull, G., Burgoyne, C. F. & Fortune, B. Macular structure and function in nonhuman primate experimental glaucoma. Invest Ophthalmol Vis Sci. \n                           57, 1892\u20131900 (2016).","journal-title":"Invest Ophthalmol Vis Sci."},{"key":"5282_CR18","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1167\/tvst.4.4.9","volume":"4","author":"C Dysli","year":"2015","unstructured":"Dysli, C., Enzmann, V., Sznitman, R. & Zinkernagel, M. S. Quantitative analysis of mouse retinal layers using automated segmentation of spectral domain optical coherence tomography images. Transl Vis Sci Technol. \n                           4, 9, doi:10.1167\/tvst.4.4.9 (2015).","journal-title":"Transl Vis Sci Technol."},{"key":"5282_CR19","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1016\/j.ajo.2004.03.019","volume":"138","author":"G Wollstein","year":"2004","unstructured":"Wollstein, G. et al. Optical coherence tomography (OCT) macular and peripapillary retinal nerve fiber layer measurements and automated visual fields. Am J Ophthalmol. \n                           138, 218\u2013225 (2004).","journal-title":"Am J Ophthalmol."},{"key":"5282_CR20","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1034\/j.1600-0420.80.s236.44.x","volume":"236","author":"A Giovannini","year":"2002","unstructured":"Giovannini, A., Amato, G. & Mariotti, C. The macular thickness and volume in glaucoma: an analysis in normal and glaucomatous eyes using OCT. Acta Ophthalmol Scand Suppl. \n                           236, 34\u201336 (2002).","journal-title":"Acta Ophthalmol Scand Suppl."},{"key":"5282_CR21","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1001\/archopht.121.1.41","volume":"121","author":"DS Greenfield","year":"2003","unstructured":"Greenfield, D. S., Bagga, H. & Knighton, R. W. Macular thickness changes in glaucomatous optic neuropathy detected using optical coherence tomography. Arch Ophthalmol. \n                           121, 41\u201346 (2003).","journal-title":"Arch Ophthalmol."},{"key":"5282_CR22","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/S0161-6420(02)01564-6","volume":"110","author":"V Guedes","year":"2003","unstructured":"Guedes, V. et al. Optical coherence tomography measurement of macular and nerve fiber layer thickness in normal and glaucomatous human eyes. Ophthalmology. \n                           110, 177\u2013189 (2003).","journal-title":"Ophthalmology."},{"key":"5282_CR23","first-page":"395","volume":"34","author":"Y Glovinsky","year":"1993","unstructured":"Glovinsky, Y., Quigley, H. A. & Pease, M. E. Foveal ganglion cell loss is size dependent in experimental glaucoma. Invest Ophthalmol Vis Sci. \n                           34, 395\u2013400 (1993).","journal-title":"Invest Ophthalmol Vis Sci."},{"key":"5282_CR24","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1016\/j.preteyeres.2009.07.001","volume":"28","author":"A Bringmann","year":"2009","unstructured":"Bringmann, A. et al. Cellular signaling and factors involved in M\u00fcller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res. \n                           28, 423\u2013451 (2009).","journal-title":"Prog Retin Eye Res."},{"key":"5282_CR25","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1038\/nrn3723","volume":"15","author":"D Goldman","year":"2014","unstructured":"Goldman, D. M\u00fcller glial cell reprogramming and retina regeneration. Nat Rev Neurosci. \n                           15, 431\u2013442 (2014).","journal-title":"Nat Rev Neurosci."},{"key":"5282_CR26","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1371\/journal.pone.0130175","volume":"10","author":"T Hasegawa","year":"2015","unstructured":"Hasegawa, T. et al. Microcystic inner nuclear layer changes and retinal nerve fiber layer defects in eyes with glaucoma. PloS One. \n                           10, 6, doi:10.1371\/journal.pone.0130175 (2015).","journal-title":"PloS One."},{"key":"5282_CR27","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1016\/S0002-9394(01)00964-3","volume":"131","author":"S Drance","year":"2001","unstructured":"Drance, S., Anderson, D. R. & Schulzer, M., Collaborative Normal-Tension Glaucoma Study Group. Risk factors for progression of visual field abnormalities in normal-tension glaucoma. Am J Ophthalmol. \n                           131, 699\u2013708 (2001).","journal-title":"Am J Ophthalmol."},{"key":"5282_CR28","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1001\/archopht.1981.03930010635009","volume":"99","author":"HA Quigley","year":"1981","unstructured":"Quigley, H. A., Addicks, E. M., Green, W. R. & Maumenee, A. E. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol. \n                           99, 635\u2013649 (1981).","journal-title":"Arch Ophthalmol."},{"key":"5282_CR29","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1111\/j.1600-0420.2005.00590.x","volume":"84","author":"MC Grieshaber","year":"2006","unstructured":"Grieshaber, M. C., Terhorst, T. & Flammer, J. The pathogenesis of optic disc splinter hemorrhages: a new hypothesis. Acta Ophthalmol Scand. \n                           84, 62\u201368 (2006).","journal-title":"Acta Ophthalmol Scand."},{"key":"5282_CR30","doi-asserted-by":"publisher","first-page":"1926","DOI":"10.1016\/S0161-6420(97)30005-0","volume":"104","author":"K Sugiyama","year":"1997","unstructured":"Sugiyama, K. et al. The associations of optic disc hemorrhage with retinal nerve fiber layer defect and peripapillary atrophy in normal-tension glaucoma. Ophthalmology. \n                           104, 1926\u20131933 (1997).","journal-title":"Ophthalmology."},{"key":"5282_CR31","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1002\/glia.22477","volume":"61","author":"A Reichenbach","year":"2013","unstructured":"Reichenbach, A. & Bringmann, A. New functions of M\u00fcller cells. Glia. \n                           61, 651\u2013678 (2013).","journal-title":"Glia."},{"key":"5282_CR32","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1038\/85090","volume":"4","author":"AJ Fischer","year":"2001","unstructured":"Fischer, A. J. & Reh, T. A. M\u00fcller glia are a potential source of neural regeneration in the postnatal chicken retina. Nature Neurosci. \n                           4, 247\u2013252 (2001).","journal-title":"Nature Neurosci."},{"key":"5282_CR33","doi-asserted-by":"publisher","first-page":"13654","DOI":"10.1073\/pnas.0402129101","volume":"101","author":"S Ooto","year":"2004","unstructured":"Ooto, S. et al. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci USA. \n                           101, 13654\u201313659 (2004).","journal-title":"Proc Natl Acad Sci USA."},{"key":"5282_CR34","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1016\/j.ophtha.2012.08.018","volume":"120","author":"D Su","year":"2013","unstructured":"Su, D., Park, S. C., Simonson, J. L., Liebmann, J. M. & Ritch, R. Progression pattern of initial parafoveal scotomas in glaucoma. Ophthalmology. \n                           120, 520\u2013527 (2013).","journal-title":"Ophthalmology."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-05282-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-05282-4","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-05282-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T01:48:30Z","timestamp":1671760110000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-05282-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,7,17]]},"references-count":34,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["5282"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-05282-4","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,7,17]]},"assertion":[{"value":"15 February 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 May 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 July 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"5543"}}