Fish Lenses : Anatomy and Optics

Abstract

I have investigated some of the biological regulatory mechanisms governing the development of crystalline lenses. I used fish as model animals because they possess optically interesting lenses, while the geometrical simplicity of fish lenses allows for studies that are difficult or impossible with the lenses of other animals.
First we have investigated lens optical plasticity by measuring longitudinal spherical aberration in light and dark adapted fish of two species, Atlantic and Polar cod. We noticed that Atlantic cod, native to regions with daily light/dark changes responded to light/dark adaptation by changing the optics of its lens, whereas the optics of Polar cod, living in the polar region, was unchanged on a daily basis (Paper I). However, we observed that the optics of the Polar cod lens changed annually between seasons corresponding to polar day and night (unpublished data). Our findings can be explained by the existence of two different mechanisms controlling the optics of fish lenses. A short-term one adapting the lenses to daily light/dark cycles (Atlantic cod) and a long-term one evolved for coping with long polar days and nights (Polar cod).
The second project involved investigation of the osmolality of fish larvae body fluids. We tested two levels of osmolality in two different ways. The first one involved measuring the rate of optical deterioration of excised fish lenses placed in different immersion media, the second one the quality of a whole eye fixation. In both cases, lower osmolality gave better results for fish larvae. The optical quality of larval lenses deteriorated slower and fixation preserved the larval eye in a more natural shape (Paper II). We concluded that zebrafish larvae have lower osmolality in their bodies than adult fish.
The third project was dedicated to the investigation of the cellular structure of fish lenses. First, we developed a method to visualize an equatorial cross-sections of adult fish lenses. Than we used the method to examine lenses in two size groups of fish of the same species. We measured lens fiber thickness in four relative radial positions in the lens. Our measurements showed that fish lens fiber cells have the same thickness along the radius of the lens and in both size groups. The average thickness was much lower than in other vertebrates (Paper III).
We followed up that study by measuring full thickness profile along the lens radius in nine fish species. The thickness of a fiber was independent from its radial position in the lens in all but one species. We observed that the average fiber thickness depends on species. Additionally, we developed a model for calculating historical lens fiber thicknesses necessary for the cells to reach their current refractive indices and thicknesses by cell compaction. The model showed that the cells would have to lose 66% of their volumes to reach their current sizes. This unlikely number and the constancy of cell thickness suggest that a different mechanism is at work. (Paper IV). Based on the findings from both papers, we conclude that, at least in fish, protein is transported inwards between denucleated fibers in the growing lens. The cells in the peripheral lens layers have synthetic capabilities and are most likely the source of those proteins.

Abstract (Swedish)

How fish eyes may save yours?
According to the World Health Organization, cataract was responsible for over half of the blindness world-wide in 2010. Getting a cataract means that the lens inside your eye gets clouded, preventing clear, sharp vision. Cataract can be caused by age, physical trauma, genetics, or even skin disease. It can virtually happen to everyone. It is possible to fix cataract by surgically replacing your lens with an artificial one. However, not everyone has access to such an expensive procedure. Replacing the natural lenses is also far from ideal. Artificial lenses have problems with accommodation, which is the ability to focus on objects at different distances, like looking over the horizon and reading a book. Cataract is a serious problem and its cause is often elusive. What can we do about it?
If your car breaks, you go to a mechanic who knows how to fix it. Similarly, you go to a doctor if something is wrong with your body. The major difference is that the mechanic can always ask the designer of the car; “How does it work?” It is much more difficult to ask Nature how it has shaped us. Thanks to science, it is a difficult, but not an impossible task. By unraveling the unknowns piece by piece, we can gain an understanding about how things work. The more pieces we get, the easier it becomes to figure it all out.
My work with other researchers at Lund University unraveled some of those pieces that in the future may be useful for preventing cataract. The lens develops by the same basic mechanisms in the eyes of all vertebrates, including humans. However, it is much easier to experiment on fish than on people.
What exactly have we done?
In our research, we have found out that fish can change the optics of their lenses differently depending on the geographic region they are from. Fish from the polar region, experiencing mainly the annual changes of polar day and night, change their lenses much slower than fish from regions with a daily light/dark cycle!
Another finding involved how tiny fish survive the harsh influence of… water. All animals are made of cells that contain water. Dissolved salts and other molecules keep the cells alive. How much minerals there are in the water is called osmolality. If osmolality inside a cell is higher than in the water outside, the water will rush into the cell to equalize osmolality on both sides, letting the cells swell and eventually killing them. You can imagine that this is a real problem for aquatic animals! Fish have mechanisms to keep osmolality inside their bodies higher than in the water they swim in. However, we found out that fish larvae cannot keep osmolality in their bodies on the same high level as adults, so that their bodies and lenses operate at much lower osmolality.
We also studied how the fish lens is built. As I have mentioned, the mechanisms of creating the lens are similar in all vertebrates. However, fish lenses are very hard and it has therefore been impossible to section and see inside them. There was no method for studying the cells in a fish lens. I have developed such a method and used it to look into the cellular structure of the lenses of nine fish species. We found that the cells, organized in concentric layers, have the same thickness irrespective of lens size. All layers are equally thick and the only difference between lenses of two sizes is the amount of layers. This has also been observed in other vertebrates, which further confirms that studying fish can benefit us humans. Interestingly, the layers in fish lenses were much thinner than in cattle, chicken, rabbit, and mouse. All nine fish species had layers of different sizes, which means that there are not only differences between animal groups, but also among fishes. Through computer modeling, we discovered that fish lenses change their optics by transporting proteins inside the lens. This is a very surprising observation because most of the cells in the lens are “dead”, just as the surface layers of your skin. Yet, lens cells can change their properties anyhow!
An old Chinese proverb says: “A journey of a thousand miles begins with a single step”. I would like to point out that the journey not only begins with a single step, but also consists of single steps. My research and findings, described in the book you are reading, are a few of such steps toward understanding lenses and potentially stop the leading cause of blindness; lens cataract.

• author: Kozłowski, Tomasz M
• supervisor: Ronald Kröger; Eric Warrant
• opponent: Associate Professor Lundström, Linda, KTH Royal Institute of Technology, Stockholm, Sweden
• organization: Functional zoology; Lund Vision Group (research group)
• publishing date: 2018-01
• type: Thesis
• publication status: published
• subject: Developmental Biology; Zoology; Cell Biology
• keywords: Plasticity, Development, Cellular structure, Lens fiber cells, Modeling, Laser Scanning, Schlieren photography, Fast Fourier Transform (FFT)
• pages: 110 pages
• defense location: Lecture hall “Blå hallen”, Ecology building, Sölvegatan 37, Lund
• defense date: 2018-02-23 10:00:00
• ISBN: 978-91-7753-555-3
• ISBN: 978-91-7753-556-0
• language: English
• LU publication?: yes
• id: 7ffd351e-5fcc-46e1-926f-f729df8e8edf
• date added to LUP: 2018-01-29 13:51:44
• date last changed: 2020-10-13 13:47:06