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Visual cortex damage in a ferret model of ocular hypertension

  • Laboratory Investigation
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Abstract

Purpose

We aimed to analyze the changes in the visual cortex of a ferret model of ocular hypertension (OH) using cytochrome oxidase (CO) staining.

Study design

Experimental.

Methods

OH was induced in 9 ferrets by means of injection of cultured conjunctival cells into the anterior chamber of the right eye. Three ferrets were used as the controls. CO staining was performed to assess the metabolic intensity at the II-III and IVC layers of the visual cortex.

Results

The intensities of CO staining in the right and left II-III layers of the primary visual cortex (V1) in the OH ferrets were 39.8 ± 10.3 and 41.9 ± 9.2 arbitrary units, respectively. In the control ferrets, the intensity was 88.1 ± 8.1 arbitrary units. The intensity of CO staining of the II-III layers obtained from the OH eyes was significantly lower than that from the control eyes (unpaired t test, P < .01). The intensities of CO staining in the right and left IVC layers of V1 in the OH ferrets were 60.3 ± 12.8 and 60.0 ± 13.5 arbitrary units, respectively. In the control ferrets, the intensity was 111.4 ± 9.6 arbitrary units. The CO staining intensity of the IVC layer obtained from the OH eyes was significantly lower than that from the control eyes (unpaired t test, P < .01).

Conclusion

The CO staining intensity was reduced in the visual cortex from OH eyes. This study revealed that OH causes metabolic change in the visual cortex.

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References

  1. Weinreb RN, Friedman DS, Fechtner RD, Cioffi GA, Coleman AL, Girkin CA, et al. Risk assessment in the management of patients with ocular hypertension. Am J Ophthalmol. 2004;138:458–67.

    Article  PubMed  Google Scholar 

  2. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:262–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Collaborative Normal-Tension Glaucoma Study Group. The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol. 1998;126:498–505.

    Article  Google Scholar 

  4. The Advanced Glaucoma Intervention Study (AGIS0). The relationship between control of intraocular pressure and visual field deterioration. The AGIS Investigators. Am J Ophthalmol. 2000;130:429–40.

    Article  Google Scholar 

  5. Inoue K, Ishida K, Tomita G, Noma H. A scoping review and network meta-analysis for efficacy and safety of glaucoma medication in Japanese patients. Jpn J Ophthalmol. 2020;64:103–13.

    Article  CAS  PubMed  Google Scholar 

  6. Joh HJ, Jin SW. Comparison of different combinations of maximum medical therapy for lowering intraocular pressure in primary open angle glaucoma: 12-month retrospective consecutive case series. Jpn J Ophthalmol. 2019;63:322–7.

    Article  PubMed  Google Scholar 

  7. Omoto T, Fujishiro T, Asano-Shimizu K, Sugimoto K, Sakata R, Murata H, et al. Comparison of the short-term effectiveness and safety profile of ab interno combined trabeculotomy using 2 types of trabecular hooks. Jpn J Ophthalmol. 2020;64:407–13.

    Article  PubMed  Google Scholar 

  8. Aihara M, Kuwayama Y, Miyata K, Ohtani S, Ideta R, Hashimoto Y, et al. Twelve-month efficacy and safety of glaucoma filtration device for surgery in patients with normal-tension glaucoma. Jpn J Ophthalmol. 2019;63:402–9.

    Article  CAS  PubMed  Google Scholar 

  9. Gupta N, Ly T, Zhang Q, Kaufman PL, Weinreb RN, Yucel YH. Chronic ocular hypertension induces dendrite pathology in the lateral geniculate nucleus of the brain. Exp Eye Res. 2007;84:176–84.

    Article  CAS  PubMed  Google Scholar 

  10. Yücel Y, Zhang Q, Weinreb RN, Kaufman A, Gupta N. Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog Retin Eye Res. 2003;22:465–81.

    Article  PubMed  Google Scholar 

  11. Ito Y, Shimazawa M, Chen YN, Tsuruma K, Yamashima T, Araie M, et al. Morphological changes in the visual pathway induced by experimental glaucoma in Japanese monkeys. Exp Eye Res. 2009;89:246–55.

    Article  CAS  PubMed  Google Scholar 

  12. Sasaoka M, Nakamura K, Shimazawa M, Ito Y, Araie M, Hara H. Changes in visual fields and lateral geniculate nucleus in monkey laser-induced high intraocular pressure model. Exp Eye Res. 2008;86:770–82.

    Article  CAS  PubMed  Google Scholar 

  13. Weber AJ, Zelenak D. Experimental glaucoma in the primate induced by latex microspheres. J Neurosci Methods. 2001;111:39–48.

    Article  CAS  PubMed  Google Scholar 

  14. Yücel YH, Zhang Q, Gupta N, Kaufman PL, Weinreb RN. Loss of neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus in glaucoma. Arch Ophthalmol. 2000;118:378–84.

    Article  PubMed  Google Scholar 

  15. Fujishiro T, Kawasaki H, Aihara M, Saeki T, Ymagishi R, Atarashi T, et al. Establishment of an experimental ferret ocular hypertension model for the analysis of central visual pathway damage. Sci Rep. 2014;4:6501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Fujishiro T, Honjo M, Kawasaki H, Asaoka R, Yamagishi R, Aihara M. Structural changes and astrocyte response of the lateral geniculate nucleus in a ferret model of ocular hypertension. Int J Mol Sci. 2020;21:1339.

    Article  CAS  PubMed Central  Google Scholar 

  17. Kawasaki H, Crowley JC, Livesey FJ, Katz LC. Molecular organization of the ferret visual thalamus. J Neurosci. 2004;24:9962–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Iwai L, Ohashi Y, van der List D, Usrey WM, Miyashita Y, Kawasaki H. FoxP2 is a parvocellular-specific transcription factor in the visual thalamus of monkeys and ferrets. Cereb Cortex. 2013;23:2204–12.

    Article  PubMed  Google Scholar 

  19. Dunn DG, Harris RK, Meis JM, Sweet DE. A histomorphologic and immunohistochemical study of chordoma in twenty ferrets (Mustela putorius furo). Vet Pathol. 1991;28:467–73.

    Article  CAS  PubMed  Google Scholar 

  20. Hoffmann KP, Garipis N, Distler C. Optokinetic deficits in albino ferrets (Mustela putorius furo): a behavioral and electrophysiological study. J Neurosci. 2004;24:4061–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Christopher D. Neuroanatomy of the ferret brain with focus on the cerebral cortex. In: Fox JG, Marini RP, eds. Biology and diseases of the ferret. 3rd ed. Wiley-Blackwell; 1998:69–80.

  22. Mizuguchi K, Horiike T, Matsumoto N, Ichikawa Y, Shinmyo Y, Kawasaki H. Distribution and morphological features of microglia in the developing cerebral cortex of gyrencephalic mammals. Neurochem Res. 2018;43:1075–85.

    Article  CAS  PubMed  Google Scholar 

  23. Thompson ID, Morgan JE. The development of retinal ganglion cell decussation patterns in postnatal pigmented and albino ferrets. Eur J Neurosci. 1993;5:341–56.

    Article  CAS  PubMed  Google Scholar 

  24. Montiani-Ferreira F, Mattos BC, Russ HH. Reference values for selected ophthalmic diagnostic tests of the ferret (Mustela putorius furo). Vet Ophthalmol. 2006;9:209–13.

    Article  PubMed  Google Scholar 

  25. Sapienza JS, Porcher D, Collins BR, Gum GG, Brooks DE. Tonometry in clinically normal ferrets (Mustela putorius furo). Prog Vet Comp Ophthalmol. 1991;1:291–4.

    Google Scholar 

  26. Blanco R, Martinez-Navarrete G, Pérez-Rico C, Valiente-Soriano FJ, Aviles-Trigueros M, Vicente J, et al. A chronic ocular-hypertensive rat model induced by injection of the sclerosant agent polidocanol in the aqueous humor outflow pathway. Int J Mol Sci. 2019;20:3209.

    Article  CAS  PubMed Central  Google Scholar 

  27. Di Girolamo N, Andreani V, Guandalini A, Selleri P. Evaluation of intraocular pressure in conscious ferrets (Mustela putorius furo) by means of rebound tonometry and comparison with applanation tonometry. Vet Rec. 2013;172:396.

    Article  PubMed  Google Scholar 

  28. Hernández-Guerra AM, Rodilla V, López-Murcia MM. Ocular biometry in the adult anesthetized ferret (Mustela putorius furo). Vet Ophthalmol. 2007;10:50–2.

    Article  PubMed  Google Scholar 

  29. Cucchiaro JB. Early development of the retinal line of decussation in normal and albino ferrets. J Comp Neurol. 1991;312:193–206.

    Article  CAS  PubMed  Google Scholar 

  30. Lund JS. Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci. 1988;11:253–88.

    Article  CAS  PubMed  Google Scholar 

  31. Crawford ML, Harwerth RS, Smith EL 3rd, Shen F, Carter-Dawson L. Glaucoma in primates: cytochrome oxidase reactivity in parvo- and magnocellular pathways. Invest Ophthalmol Vis Sci. 2000;41:1791–802.

    CAS  PubMed  Google Scholar 

  32. Crawford ML, Harwerth RS, Smith EL 3rd, Mills S, Ewing B. Experimental glaucoma in primates: changes in cytochrome oxidase blobs in V1 cortex. Invest Ophthalmol Vis Sci. 2001;42:358–64.

    CAS  PubMed  Google Scholar 

  33. Wong-Riley M. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 1979;171:11–28.

    Article  CAS  PubMed  Google Scholar 

  34. Wong-Riley MTT. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 1989;12:94–101.

    Article  CAS  PubMed  Google Scholar 

  35. Wong-Riley MT, Hevner RF, Cutlan R, Earnest M, Egan R, Frost J, et al. Cytochrome oxidase in the human visual cortex: distribution in the developing and the adult brain. Vis Neurosci. 1993;10:41–58.

    Article  CAS  PubMed  Google Scholar 

  36. Wong-Riley MT, Tripathi SC, Trusk TC, Hoppe DA. Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: I. Quantitative electron-microscopic (EM) analysis of neurons. Vis Neurosci. 1989;2:483–97.

    Article  CAS  PubMed  Google Scholar 

  37. Wong-Riley MT, Trusk TC, Tripathi SC, Hoppe DA. Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: II. Quantitative electron-microscopic (EM) analysis of neuropil. Vis Neurosci. 1989;2:499–514.

    Article  CAS  PubMed  Google Scholar 

  38. Deyoe EA, Trusk TC, Wong-Riley MT. Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey. Vis Neurosci. 1995;12:629–39.

    Article  CAS  PubMed  Google Scholar 

  39. Nakagawa A, Sakai O, Tokushige H, Fujishiro T, Aihara M. Development and characterization of a new rat ocular hypertension model induced by intracameral injection of conjunctival fibroblasts. Sci Rep. 2019;9:6593.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Zhou W, Muir ER, Nagi KS, Chalfin S, Rodriguez P, Duong TQ. Retinotopic fMRI reveals visual dysfunction and functional reorganization in the visual cortex of mild to moderate glaucoma patients. J Glaucoma. 2017;26:430–7.

    Article  PubMed  Google Scholar 

  41. Wang J, Li T, Sabel BA, Chen Z, Wen H, Li J, et al. Structural brain alterations in primary open angle glaucoma: a 3T MRI study. Sci Rep. 2016;6:18969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chen Z, Wang J, Lin F, Dai H, Mu K, Zhang H. Correlation between lateral geniculate nucleus atrophy and damage to the optic disc in glaucoma. J Neuroradiol. 2013;40:281–7.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the Japan Society for the Promotion of Science, kakenhi grant number JP 19K09946.

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Correspondence to Makoto Aihara.

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T. Fujishiro, None; M. Honjo, None; H. Kawasaki, None; M. Aihara, None.

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Corresponding Author: Makoto Aihara

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Fujishiro, T., Honjo, M., Kawasaki, H. et al. Visual cortex damage in a ferret model of ocular hypertension. Jpn J Ophthalmol 66, 205–212 (2022). https://doi.org/10.1007/s10384-022-00901-8

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  • DOI: https://doi.org/10.1007/s10384-022-00901-8

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