Wendy Yue
PhD student
Johns Hopkins University

Kate, United Kingdom

What happens to the retina and optic nerves in deep sea fish that are blind?

Wendy Yue
HHMI predoctoral fellow,
PhD student,
Johns Hopkins University
The deep sea, defined to have a depth over 200 meters, represents one of the most unusual light habitats on Earth. Downwelling sunlight still supports some sensitive forms of vision down to the mesopelagic zone (200-1000m). However, in the bathypelagic zone (1000-4000m), bioluminescence from deep-sea organisms becomes the sole source of illumination. Both residual sunlight and bioluminescence are spectrally restricted, having a wavelength of 450-500nm (blue-green) in most cases. The eyes of deep-sea fish are therefore a living demonstration of how photic environment may shape the visual system.

Most visual animals have specialized eye structures for capturing light information. In his classic The Origin of Species (1882), Charles Darwin pictured the simplest eye to “consist of an optic nerve, surrounded by pigment-cells and covered by translucent skin, but without any lens or other refractive body”. Such prototypic eyes were indeed later found in certain classes of flatworms (planarians), one of the most primitive animals with a central nervous system. The pigment-cells of these animals are organized in a cup shape, outside of which sits the photoreceptor neurons. As light hits the photoreceptors, a light-absorbing protein known as opsin becomes excited, triggering biochemical events that produce an electrical signal. This signal then passes along the axons of the photoreceptor neurons to specific regions of the brain, in this case, to the medial region of the main brain lobes.

Other animals have evolved more sophisticated eye forms, adding various adaptive features to the prototypic eyes. Anatomically, new cell types such as lens cells and muscle cells have been introduced to aid the focusing of light onto photoreceptors for sharp image formation. Photoreceptors diverged into two main classes that differ in cell morphology and light-signaling mechanism. Rhabdomeric photoreceptors, typified by those in insect compound eyes, usually fold their surface membrane into projections called microvilli and signal via a phospholipase C pathway. Ciliary photoreceptors, present for example in mammals including human, are often characterized instead by internal membranous discs/vesicles embedded in a protruding structure called cilia, with a signaling pathway dependent on cyclic nucleotides. The membranous structures in the two classes both serve to increase surface area for efficient capturing of light, but the different signaling strategies they use may underlie variations in other important functional qualities: the sensitivities of the photoreceptors to light, their abilities to detect a broad range of intensities, and thus their usage in a particular light habitat.

Along with changes in gross eye structures and photoreceptors’ morphologies are amino acid mutations in the light-absorbing molecule, opsin, which allows it to attain properties suitable for detecting dim light, color and motion, among other attributes. For instance, zebrafish, living in shallow water, are exposed to a wide spectrum of light spanning from the UV to the red. These animals have altogether nine types of opsins, sensitive maximally to different parts of the spectrum. On the other hand, coelacanths, living in ocean up to 200m in depth, possess only two types of opsins, sensitive maximally to green light near 480nm, which corresponds to the wavelength of light available at such depths.

Evolution also saw an expansion in neural networks, both locally in the retina and centrally in the brain, for processing visual information. In humans, for example, electrical signals from the photoreceptors are processed through a neuronal network within the retina to extract and channel color and direction information to specific classes of retinal ganglion cells. The axons of these cells make up the optic nerve, projecting to areas of the brain responsible for forming images and those for other visual tasks, such as circadian regulation and reflexive control of eye pupil size.

Returning to deep-sea fish, I have not been able to find much literature describing the eyes of blind species. So, I shall try here to provide examples from sighted deep-sea fish and blind freshwater cavefish as useful reference.

Many deep-sea fish have upward-pointing eyes for detecting silhouettes of other animals against a brighter background from sunlight above. Some eyes, however, are designed to look downward into the dark to scan for bioluminescent organisms. These eyes take interesting forms: Bathylychnops exilis uses a secondary eye with its own lens and retina whereas Dolicopteryx longipes adopts a stack of reflecting plates to redirect light onto the retina. The tapetum is another adaptive feature; it is a reflective tissue located at the back of the retina, generally believed to increase the passage of light through the photoreceptors. Like most vertebrates, these fish photoreceptors are considered ciliary, and likely use the cyclic nucleotide pathway common to this class of photoreceptors. The eyes of the blind cavefish Astyanax mexicanus have a different but equally dramatic development trajectory. The lens and the retina cease growing at embryonic stages, and are overgrown so much by epidermis and connective tissues during larval stages that cavefish appears eyeless in adulthood. Whether blind deep-sea fish experience similar retinal degeneration is unknown.

Deep-sea fish opsin has been studied in a fair amount. Of the 195 different opsins from 175 species, over 85% has been reported to absorb maximally in the range of 468-494nm. Providing maximal sensitivity to bioluminescence has been argued to be the primary reason for such a spectral constraint, but other possible driving forces have also been discussed. The situation in blind cave fish may be even more intriguing. As in A. mexicanus mentioned above, Astyanax fasciatus exhibits only rudimentary eyes. However, its genome retains opsin genes with intact gene structures believed to give proteins with absorption properties different from their sighted counterparts. Whether these opsin genes are expressed any time during development is again unknown, but there have been suggestions that accumulating sporadic mutations in the genes may have rendered them non-functional.

Deep-sea fish have been thought to possess a simple neural pathway for processing visual information because their retinas are dominated by a single type of photoreceptor cell. A study on the deep-sea eel Synaphobranchus kaupi found that this may not be entirely true – the diversity of retinal neurons, if taken as a measure of complexity, may be reduced for certain neuronal classes but not others. Deep-sea fish send their optic nerve to the optic tectum of the brain. An analysis of 35 deep-sea fish species revealed that, although individual differences exist, a larger volume of the brain is generally devoted to the optic tectum than to areas processing olfactory, taste or tactile information alone, suggesting that vision may still be an important sense in these fish. Quite surprisingly, the rudimentary eye of blind cave fish does extend axons to the brain, although being much sparser and not completely myelinated. These axons can be traced to the optic tectum of the contralateral side.

The eye is certainly an amazing evolution showcase. Not mentioned here are yet other photosensitive organs, like the pineal organs common in fish, that serve non-image-forming function such as regulating circadian rhythm. Beauty is in the eyes of the beholder, but the beholders’ eyes could be beautiful too!

Major References

1. Douglas, R.H. , Partridge, J. C. & Marshall, N. J. The Eyes of Deep-Sea Fish I: Lens Pigmentation, Tapeta and Visual Pigments. Progress in Retinal and Eye Research 17, 597-636 (1998).

2. Fain, G. L., Hardie, R. C. & Laughlin, S. B. Phototransduction and the evolution of photoreceptors. Curr. Biol. 20, R114-24 (2010).

3. Jeffery, W. R. Regressive evolution in Astyanax cavefish. Annu. Rev. Genetics 43, 25-47 (2009).

4. Warrant, E. J. & Locket, N. A. Vision in the deep sea. Biological Reviews 79, 671-712 (2004).

5. Yau, K. W. & Hardie, R. C. Phototransduction motifs and variations. Cell 139, 246-64 (2009).

6. Yokoyama, S. Evolution of dim-light and color vision pigments. Annu. Rev. Genomics Hum. Genet. 9, 259-82 (2008).

10/19/12 11:15