Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics
Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri, United States of America
Abstract
The avian retina possesses one of the most sophisticated cone photoreceptor systems among vertebrates. Birds have five types of cones including four single cones, which support tetrachromatic color vision and a double cone, which is thought to mediate achromatic motion perception. Despite this richness, very little is known about the spatial organization of avian cones and its adaptive significance.
Here we show that the five cone types of the chicken independently tile the retina as highly ordered mosaics with a characteristic spacing between cones of the same type. Measures of topological order indicate that double cones are more highly ordered than single cones, possibly reflecting their posited role in motion detection. Although cones show spacing interactions that are cell type-specific, all cone types use the same density-dependent yardstick to measure intercone distance. We propose a simple developmental model that can account for these observations. We also show that a single parameter, the global regularity index, defines the regularity of all five cone mosaics. Lastly, we demonstrate similar cone distributions in three additional avian species, suggesting that these patterning principles are universal among birds. Since regular photoreceptor spacing is critical for uniform sampling of visual space, the cone mosaics of the avian retina represent an elegant example of the emergence of adaptive global patterning secondary to simple local interactions between individual photoreceptors. Our results indicate that the evolutionary pressures that gave rise to the avian retina's various adaptations for enhanced color discrimination also acted to fine-tune its spatial sampling of color and luminance.
Citation: Kram YA, Mantey S, Corbo JC (2010) Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics. PLoS ONE 5(2): e8992. doi:10.1371/journal.pone.0008992
Editor: Eric Warrant, Lund University, Sweden
Received: November 9, 2009; Accepted: January 6, 2010; Published: February 1, 2010
Copyright: © 2010 Kram et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This project was funded by a grant from the National Eye Institute (R01EY018826). Additional financial support came from a Summer Undergraduate Research Fellowship from the Howard Hughes Medical Institute and the Office of Undergraduate Research Hoopes Award at Washington University and from an undergraduate summer research fellowship from the Honors Program at the University of Michigan Flint. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: jcorbo@pathology.wustl.edu
¤ Current address: The University of Michigan Flint; Flint, Michigan, United States of America
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