Deconstructing the adaptations of avian color vision

Whether they are discriminating a dazzling colorful mating display or navigating through a complex environment at high speeds, most birds rely on vision as their most important sensory modality. The importance of vision in the lives of birds is reflected in the sophistication of their photoreceptors, yet the functional significance of this complexity is not well understood. We have used a variety of advanced technologies to characterize the spectral filtering and optics of avian cone photoreceptors and have revealed how these cells are precisely adapted for exquisite color discrimination.

HFSP Program Grant holders Joseph Corbo, Almut Kelber, Nicholas Roberts and colleagues
authored on Sat, 12 December 2015

The demands of the colorful and fast-paced lives of birds have driven the evolution of one of the most sophisticated visual systems among vertebrates. Compared to the human visual system, birds have a greater diversity of photoreceptors that extends avian vision into the ultraviolet and provides dimensions of color well beyond our perceptions. The structure of the individual avian cone photoreceptors is also more complex than human cones. For example, the cone photoreceptors of bird retinas contain a variety of brilliantly colored oil droplets that are matched to the specific spectral sensitivity of the opsins within each of the cone photoreceptor subtypes.

Figure: To the left is a micrograph of a flat mounted chicken retina showing the brilliantly colored oil droplets. Each cone photoreceptor subtype contains a different colored oil droplet. For example, the red droplets are found within the red-sensitive cone photoreceptors and the orange droplets within the green-sensitive cones (middle). To the right is a phase-retardation heat map of a single cone photoreceptor that shows very high phase-retardation at the oil droplet which is indicative of the high refractive index of this structure.

In our studies, we have determined that the avian cone oil droplets are pigmented with specific types of carotenoid pigments. Carotenoids endow many fruits and vegetables, such as carrots and peppers, with their distinctive colors. They also pigment the brightly colored feathers of bird species like the cardinal and canary. Within the cone oil droplets, birds mix and match various carotenoid types that absorb light in different portions of the spectrum to produce precisely matched long-pass cut-off filters that fine tune receptor sensitivity and facilitate exceptional color discrimination.    

In addition to functioning as spectral filters, the cone oil droplets are highly retractile and have the potential to concentrate and guide light through the receptor. To investigate these possibilities we have made detailed measurements of the optical properties of individual avian cone photoreceptors, including the oil droplets. Using modeling to simulate the passage of light through the cells, we discovered that the optical properties of the oil droplets along with other subcellular components of each cone photoreceptor subtype are fine-tuned to facilitate the detection of a specific range of wavelengths. Furthermore, we find that the strong absorption of light by the carotenoids impacts the expected role of the oil droplet as a light collecting lens. Taken together, our results indicate that the sophisticated morphology of avian cone photoreceptors is specifically adapted for color vision and offers a window into the amazing visual world of birds.

References

[1] A complex carotenoid palette tunes avian colour vision. Toomey, M. B., Collins, A. M., Frederiksen, R., Cornwall, M. C., Timlin, J. A. & Corbo, J. C. 2015 J. R. Soc. Interface 12, 20150563. (doi:10.1098/rsif.2015.0563).

Pubmed link [1]

[2] Optics of cone photoreceptors in the chicken (Gallus gallus domesticus ). Wilby, D., Toomey, M. B., Olsson, P., Frederiksen, R., Cornwall, M. C., Oulton, R., Kelber, A., Corbo, J. C. & Roberts, N. W. 2015 J. R. Soc. Interface 12, 20150591. (doi:10.1098/rsif.2015.0591).

Pubmed link [2]