Variability in Retinal Neuron Populations and Associated Variations in Mass Transport Systems of the Retina in Health and Aging

Overview

Journal Front Aging Neurosci

Specialty Geriatrics

Date 2022 Mar 14

PMID 35283756

Authors

Moussa A Zouache

Affiliations

Soon will be listed here.

Abstract

Aging is associated with a broad range of visual impairments that can have dramatic consequences on the quality of life of those impacted. These changes are driven by a complex series of alterations affecting interactions between multiple cellular and extracellular elements. The resilience of many of these interactions may be key to minimal loss of visual function in aging; yet many of them remain poorly understood. In this review, we focus on the relation between retinal neurons and their respective mass transport systems. These metabolite delivery systems include the retinal vasculature, which lies within the inner portion of the retina, and the choroidal vasculature located externally to the retinal tissue. A framework for investigation is proposed and applied to identify the structures and processes determining retinal mass transport at the cellular and tissue levels. Spatial variability in the structure of the retina and changes observed in aging are then harnessed to explore the relation between variations in neuron populations and those seen among retinal metabolite delivery systems. Existing data demonstrate that the relation between inner retinal neurons and their mass transport systems is different in nature from that observed between the outer retina and choroid. The most prominent structural changes observed across the eye and in aging are seen in Bruch's membrane, which forms a selective barrier to mass transfers at the interface between the choroidal vasculature and the outer retina.

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References

An D, Balaratnasingam C, Heisler M, Francke A, Ju M, McAllister I . Quantitative comparisons between optical coherence tomography angiography and matched histology in the human eye. Exp Eye Res. 2018; 170:13-19. DOI: 10.1016/j.exer.2018.02.006. View

Lin Y, Jiang H, Liu Y, Gameiro G, Gregori G, Dong C . Age-Related Alterations in Retinal Tissue Perfusion and Volumetric Vessel Density. Invest Ophthalmol Vis Sci. 2019; 60(2):685-693. PMC: 6383727. DOI: 10.1167/iovs.18-25864. View

Miller S, STEINBERG R . Active transport of ions across frog retinal pigment epithelium. Exp Eye Res. 1977; 25(3):235-48. DOI: 10.1016/0014-4835(77)90090-2. View

Abukawa H, Tomi M, Kiyokawa J, Hori S, Kondo T, Terasaki T . Modulation of retinal capillary endothelial cells by Müller glial cell-derived factors. Mol Vis. 2009; 15:451-7. PMC: 2647974. View

Spaide R . Choriocapillaris Flow Features Follow a Power Law Distribution: Implications for Characterization and Mechanisms of Disease Progression. Am J Ophthalmol. 2016; 170:58-67. DOI: 10.1016/j.ajo.2016.07.023. View

Leonelli S . The challenges of big data biology. Elife. 2019; 8. PMC: 6450665. DOI: 10.7554/eLife.47381. View

Voigt A, Mullin N, Whitmore S, DeLuca A, Burnight E, Liu X . Human photoreceptor cells from different macular subregions have distinct transcriptional profiles. Hum Mol Genet. 2021; 30(16):1543-1558. PMC: 8330894. DOI: 10.1093/hmg/ddab140. View

Legras R, Gaudric A, Woog K . Distribution of cone density, spacing and arrangement in adult healthy retinas with adaptive optics flood illumination. PLoS One. 2018; 13(1):e0191141. PMC: 5770065. DOI: 10.1371/journal.pone.0191141. View

Nivison-Smith L, Khandelwal N, Tong J, Mahajan S, Kalloniatis M, Agrawal R . Normal aging changes in the choroidal angioarchitecture of the macula. Sci Rep. 2020; 10(1):10810. PMC: 7331638. DOI: 10.1038/s41598-020-67829-2. View

10.

AMALRIC P . The choriocapillaris in the macular area. Clinical and angiographic study. Int Ophthalmol. 1983; 6(2):149-53. DOI: 10.1007/BF00127643. View

11.

Linsenmeier R, Braun R . Oxygen distribution and consumption in the cat retina during normoxia and hypoxemia. J Gen Physiol. 1992; 99(2):177-97. PMC: 2216610. DOI: 10.1085/jgp.99.2.177. View

12.

Masland R . The neuronal organization of the retina. Neuron. 2012; 76(2):266-80. PMC: 3714606. DOI: 10.1016/j.neuron.2012.10.002. View

13.

Hoh Kam J, Weinrich T, Shinhmar H, Powner M, Roberts N, Aboelnour A . Fundamental differences in patterns of retinal ageing between primates and mice. Sci Rep. 2019; 9(1):12574. PMC: 6715671. DOI: 10.1038/s41598-019-49121-0. View

14.

Straubhaar M, Orgul S, Gugleta K, Schotzau A, Erb C, Flammer J . Choroidal laser Doppler flowmetry in healthy subjects. Arch Ophthalmol. 2000; 118(2):211-5. DOI: 10.1001/archopht.118.2.211. View

15.

Rohrenbeck J, Wassle H, Boycott B . Horizontal Cells in the Monkey Retina: Immunocytochemical staining with antibodies against calcium binding proteins. Eur J Neurosci. 1989; 1(5):407-420. DOI: 10.1111/j.1460-9568.1989.tb00349.x. View

16.

Kanow M, Giarmarco M, Jankowski C, Tsantilas K, Engel A, Du J . Biochemical adaptations of the retina and retinal pigment epithelium support a metabolic ecosystem in the vertebrate eye. Elife. 2017; 6. PMC: 5617631. DOI: 10.7554/eLife.28899. View

17.

Brinks J, van Dijk E, Klaassen I, Schlingemann R, Kielbasa S, Emri E . Exploring the choroidal vascular labyrinth and its molecular and structural roles in health and disease. Prog Retin Eye Res. 2021; 87:100994. DOI: 10.1016/j.preteyeres.2021.100994. View

18.

Ping Chui T, Song H, Burns S . Individual variations in human cone photoreceptor packing density: variations with refractive error. Invest Ophthalmol Vis Sci. 2008; 49(10):4679-87. PMC: 2710765. DOI: 10.1167/iovs.08-2135. View

19.

Starita C, Hussain A, Patmore A, Marshall J . Localization of the site of major resistance to fluid transport in Bruch's membrane. Invest Ophthalmol Vis Sci. 1997; 38(3):762-7. View

20.

Wolter J . The pericytes of the choroid of the human eye. Am J Ophthalmol. 1956; 41(6):990-5. DOI: 10.1016/0002-9394(56)91048-0. View