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Experimental eye research2014; 121; 11-22; doi: 10.1016/j.exer.2014.02.008

Comparative quantitative study of astrocytes and capillary distribution in optic nerve laminar regions.

Abstract: Retinal ganglion cell (RGC) axonal structure and function in the optic nerve head (ONH) is predominantly supported by astrocytes and capillaries. There is good experimental evidence to demonstrate that RGC axons are perturbed in a non-uniform manner following ONH injury and it is likely that the pattern of RGC axonal modification bears some correlation with the quantitative properties of astrocytes and capillaries within laminar compartments. Although there have been some excellent topographic studies concerning glial and microvascular networks in the ONH our knowledge regarding the quantitative properties of these structures are limited. This report is an in-depth quantitative, structural analysis of astrocytes and capillaries in the pre laminar, lamina cribrosa and post laminar compartments of the ONH. 49 optic nerves from human (n = 10), pig (n = 12), horse (n = 6), rat (n = 11) and rabbit (n = 10) eyes are studied. Immunohistochemical and high-magnification confocal microscopy techniques are used to co-localise astrocytes, capillaries and nuclei in the mid-portion of the optic nerve. Quantitative methodology is used to determine the area occupied by astrocyte processes, microglia processes, nuclei density and the area occupied by capillaries in each laminar compartment. Comparisons are made within and between species. Relationships between ONH histomorphometry and astrocyte-capillary constitution are also explored. This study demonstrates that there are significant differences in the quantitative properties of capillaries and astrocytes between the laminar compartments of the human ONH. Astrocyte processes occupied the greatest area in the lamina cribrosa compartment of the human ONH implicating it as an area of great metabolic demands. Microglia were found to occupy only a small proportion of tissue in the rat, rabbit and pig optic nerve suggesting that the astrocyte is the predominant glia cell type in the optic nerve. This study also demonstrates that there is significant uniformity, with respect to astrocyte and capillary constitution, in the post laminar region of species with an unmyelinated anterior optic nerve. This implicates an important role served by oligodendrocytes and myelin in governing the structural characteristics of the post laminar optic nerve. Finally, this study demonstrates that eyes with similar lamina cribrosa structure do not necessarily share an identical cellular constitution with respect to astrocytes. The quantitative properties of astrocytes in the pre laminar and lamina cribrosa regions of the rat, which has a rudimentary lamina cribrosa with only a few collagenous beams, shared more similarities to the human eye than the pig or horse. The quantitative properties of astrocytes and capillaries in the laminar compartments of the ONH provide a basis for understanding the pathogenic mechanisms that are involved in diseases such as glaucoma and ischemic optic neuropathy. The findings in this study also provide valuable information about the distinct advantages of different animal models for studying human optic nerve diseases. Utilisation of structural data provided in this report together with emerging in vivo technology may potentially permit the early identification of RGC axonal injury by quantifying changes in ONH capillaries and astrocytes.
Copyright © 2014 Elsevier Ltd. All rights reserved.
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Publication Date: 2014-02-19 PubMed ID: 24560677DOI: 10.1016/j.exer.2014.02.008Google Scholar: Lookup
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  • Comparative Study
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research paper presents a detailed comparative quantitative analysis of astrocytes and capillaries in different regions of the optic nerve head (ONH) from a variety of mammals, including humans. The study sheds light on the differences in these structures across species and their potential implications for understanding optic nerve diseases such as glaucoma.

Research Methodology

  • The researchers conducted an in-depth investigation of astrocytes and capillaries in the pre laminar, lamina cribrosa, and post laminar compartments of the ONH. The sample consists of 49 optic nerves extracted from human, pig, horse, rat, and rabbit eyes.
  • Immunohistochemical and high-magnification confocal microscopy techniques were employed to pinpoint the location and interaction of astrocytes, capillaries, and nuclei in the optic nerve’s mid-portion.
  • Quantitative methods were implemented to calculate the area occupied by astrocyte processes, microglia processes, nuclei density, and the area occupied by capillaries in each laminar compartment. Differences and correlations were identified within and across species.

Findings and Implications

  • The study highlighted significant variations in the quantitative properties of astrocytes and capillaries among the laminar compartments of the human ONH. The greatest area was occupied by astrocyte processes in the lamina cribrosa compartment, hinting at high metabolic demands in this region.
  • Microglia were found to constitute only a small portion of tissue in the rat, rabbit, and pig optic nerve, which suggests that astrocytes are the dominant glia cell type in the optic nerve.
  • The research also found considerable uniformity in astrocyte and capillary constitution in the post laminar region of species with an unmyelinated anterior optic nerve. This observation implies a significant role of oligodendrocytes and myelin in determining the structural characteristics of the post laminar optic nerve.
  • The study raises an important finding that eyes with similar lamina cribrosa structure may not necessarily have identical cellular constitution regarding astrocytes. For example, pre laminar and lamina cribrosa regions of rats had a closer resemblance to the human eye than that of pigs or horses in their astrocytes’ quantitative properties.

Significance of the Study

  • This research enhances our understanding of the pathogenic mechanisms involved in diseases like glaucoma and ischemic optic neuropathy by studying the quantitative properties of astrocytes and capillaries in the ONH’s laminar compartments.
  • The findings provide vital insights on the unique advantages of different animal models for studying human optic nerve diseases. This can guide future research in choosing the most appropriate model for specific studies.
  • The data from this study, along with emerging in vivo technology, may enable the early detection of retinal ganglion cell (RGC) axonal injury by monitoring changes in ONH capillaries and astrocytes.

Cite This Article

APA
Balaratnasingam C, Kang MH, Yu P, Chan G, Morgan WH, Cringle SJ, Yu DY. (2014). Comparative quantitative study of astrocytes and capillary distribution in optic nerve laminar regions. Exp Eye Res, 121, 11-22. https://doi.org/10.1016/j.exer.2014.02.008

Publication

Experimental eye research
ISSN: 1096-0007
NlmUniqueID: 0370707
Country: England
Language: English
Volume: 121
Pages: 11-22

Researcher Affiliations

Balaratnasingam, Chandrakumar
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia; The ARC Centre of Excellence in Vision Science, The University of Western Australia, Perth, Australia.
Kang, Min H
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia; The ARC Centre of Excellence in Vision Science, The University of Western Australia, Perth, Australia.
Yu, Paula
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia; The ARC Centre of Excellence in Vision Science, The University of Western Australia, Perth, Australia.
Chan, Geoffrey
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia; The ARC Centre of Excellence in Vision Science, The University of Western Australia, Perth, Australia.
Morgan, William H
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia.
Cringle, Stephen J
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia; The ARC Centre of Excellence in Vision Science, The University of Western Australia, Perth, Australia.
Yu, Dao-Yi
  • Centre for Ophthalmology and Visual Science, The University of Western Australia, Perth, Australia; The ARC Centre of Excellence in Vision Science, The University of Western Australia, Perth, Australia. Electronic address: dyyu@cyllene.uwa.edu.au.

MeSH Terms

  • Adult
  • Animals
  • Astrocytes / cytology
  • Astrocytes / metabolism
  • Axons
  • Capillaries / anatomy & histology
  • Factor VII / metabolism
  • Female
  • Fluorescent Antibody Technique, Indirect
  • Glial Fibrillary Acidic Protein / metabolism
  • Horses
  • Humans
  • Male
  • Microscopy, Confocal
  • Middle Aged
  • Optic Disk / blood supply
  • Optic Nerve / cytology
  • Optic Nerve / metabolism
  • Rabbits
  • Rats
  • Rats, Inbred BN
  • Retinal Ganglion Cells / cytology
  • Sus scrofa
  • Young Adult

Citations

This article has been cited 23 times.
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