title: Avian photoreceptor patterns represent a disordered hyperuniform solution to a multiscale packing problem.
abstract: Optimal spatial sampling of light rigorously requires that identical photoreceptors be arranged in perfectly regular arrays in two dimensions. Examples of such perfect arrays in nature include the compound eyes of insects and the nearly crystalline photoreceptor patterns of some fish and reptiles. Birds are highly visual animals with five different cone photoreceptor subtypes, yet their photoreceptor patterns are not perfectly regular. By analyzing the chicken cone photoreceptor system consisting of five different cell types using a variety of sensitive microstructural descriptors, we find that the disordered photoreceptor patterns are "hyperuniform" (exhibiting vanishing infinite-wavelength density fluctuations), a property that had heretofore been identified in a unique subset of physical systems, but had never been observed in any living organism. Remarkably, the patterns of both the total population and the individual cell types are simultaneously hyperuniform. We term such patterns "multihyperuniform" because multiple distinct subsets of the overall point pattern are themselves hyperuniform. We have devised a unique multiscale cell packing model in two dimensions that suggests that photoreceptor types interact with both short- and long-ranged repulsive forces and that the resultant competition between the types gives rise to the aforementioned singular spatial features characterizing the system, including multihyperuniformity. These findings suggest that a disordered hyperuniform pattern may represent the most uniform sampling arrangement attainable in the avian system, given intrinsic packing constraints within the photoreceptor epithelium. In addition, they show how fundamental physical constraints can change the course of a biological optimization process. Our results suggest that multihyperuniform disordered structures have implications for the design of materials with novel physical properties and therefore may represent a fruitful area for future research.
authors.affiliation: Princeton Institute of the Science and Technology of Materials, Princeton University, Princeton, New Jersey 08540, USA and Materials Science and Engineering, Arizona State University, Tempe, Arizona 85287, USA.
authors.forename: Yang
authors.initials: Y
authors.lastname: Jiao
authors.affiliation: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
authors.forename: Timothy
authors.initials: T
authors.lastname: Lau
authors.affiliation: Department of Systems Immunology, Helmholtz Centre for Infection Research, Braunschweig, Germany and Center for Advancing Electronics Dresden, TU Dresden, 01062, Dresden, Germany.
authors.forename: Haralampos
authors.initials: H
authors.lastname: Hatzikirou
authors.affiliation: Department of Systems Immunology, Helmholtz Centre for Infection Research, Braunschweig, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Meyer-Hermann
authors.affiliation: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
authors.lastname: Joseph C Corbo
authors.affiliation: Princeton Institute of the Science and Technology of Materials, Princeton University, Princeton, New Jersey 08540, USA and Department of Chemistry, Department of Physics, Program in Computational and Applied Mathematics, Princeton University, Princeton, New Jersey 08544, USA.
authors.forename: Salvatore
authors.initials: S
authors.lastname: Torquato
mesh_terms: D000818:Animals; D002645:Chickens / Q000502:physiology*; D003198:Computer Simulation; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D010364:Pattern Recognition, Visual / Q000502:physiology*; D017949:Retinal Cone Photoreceptor Cells / Q000502:physiology*; D013028:Space Perception / Q000502:physiology*