Fisheye lens: How fish keep their eyes sharp

Scientists have identified a mechanism in the eyes of fish that boosts the retina's oxygen supply more than 10-fold and enhances the fish’s ability to process visual input. The mechanism—a gas gland within the eye—may have contributed to the extraordinary adaptive radiation of fishes, which today represent half of all vertebrates in the world.

Researchers from the University of British Columbia (UBC), Aarhus University and the Scripps Institution of Oceanography published the results today in the journal journal eLife. Visual input enters our eyes as light waves that are transformed by the eye's light-absorbing retina into electrical signals that are send to the brain for interpretation. This energy-demanding process requires a lot of oxygen, which is supplied by a dense network of capillary beds in most animal tissues. The fish retina does not possess an internal capillary network, likely to reduce light absorption by blood before the photons reach the photoreceptors. Therefore, oxygen’s diffusion distance is up to 50 times higher than in the human brain, which questions how oxygen can reach the retina without the typical capillary beds.

A gas-gland within the fish eye

More than 300 million years ago, before the emergence of the first dinosaurs, fishes' oxygen-binding protein, hemoglobin, mutated to become much more sensitive to acid. Here, acidification of the blood releases a large part of hemoglobin´s oxygen into the surrounding tissues. This includes the oxygen release into the swim bladder, so fishes can remain buoyant at great depths where extreme hydrostatic pressures prevail. However, the same mechanism for oxygen delivery may also allow fishes to deliver oxygen to their capillary-poor eyes.

"It has been known for half a century that the fish eye can generate high oxygen pressures within the eye to drive oxygen diffusion into their large eyes,” says Christian Damsgaard, an assistant professor of animal physiology at Aarhus Institute of Advanced Studies and Department of Biology at Aarhus University, who is the lead-author of the new study. “However, the physiological mechanism that can generate these high oxygen pressures in the fish eye has remained highly elusive. This is what we have now identified.”

To identify the primary biochemical pathway involved in this superior mode of oxygen delivery in the fish eye, an international and interdisciplinary group of animal physiologists, molecular biologists, and pharmacologists joined forces. "Christian did an amazing job of assimilating 10 researchers from four countries to tackle this question from all angles. It’s a truly international scientific collaboration,” says UBC zoologist Colin Brauner, senior author on the paper. The research group identified a set of enzymes that first pumps acidifying protons into the blood vessels that reach the eye. Then, the enzymes transport the protons into the red blood cells, where they shred oxygen off hemoglobin into the retina. These findings suggest that the vascular beds within the fish eye acts as an acidifying gas-gland similar to that found in their swim bladder.

Oxygen boosts vision

To investigate how this newly discovered oxygen supply mechanism affects vision, the group measured the function of the retina while blocking the mechanism using pharmacological compounds. Blocking the acidification mechanism in the fish eye rapidly impaired the function of the specific areas within the retina involved in signal-processing. Next, the group compared the anatomy of the retina in over 30 fish species and showed that species with the unique acidifying vasculature had markedly enlarged those specific signal-processing areas within the retina. "These interesting findings strongly suggested that the evolutionary origin of this superior mode of oxygen delivery to the eye allowed fishes to better identify and track prey,” Damsgaard explains. "This may have led to active feeding strategies in early fish evolution and fuelled the adaptive radiation of fishes, which represent over half of all vertebrates."

A proton pump with many functions

The same proton secreting protein involved in oxygen delivery in the fish eye is also found in many other aquatic organisms. They help sharks control blood pH, improve photosynthesis in algae within corals, and help bone-eating worms dissolve bones. This suggests that the genes encoding for this proton pumping protein is found in distantly related animal species.

"I'm currently investigating if the capillary beds behind the bird eye can acidify the blood to supply oxygen in the retina similar to fishes," says Damsgaard. "Birds have the sharpest vision among animals, but it remains unknown how oxygen and energy is supplied into this highly energy-demanding tissue. I’m very interested in determining if such a mechanism for improved oxygen supply can help humans with cardiovascular diseases in the future."