Many vertebrates--including various fish, amphibians and birds, but not humans-- have been proven in behavioral experiments to be capable making orienting responses based upon the angle of polarization of linearly polarized light. Although the biophysical basis of a similar capability in invertebrates is well established, there is no accepted hypothesis that explains the vertebrate ability. We hypothesize that in vertebrates the ability is conferred by the manner in which light is trapped and propagates in a unique class of photoreceptors possessed by all the vertebrates with the ability: the double cone. We propose to test the hypothesis that the double cone, with its approximately elliptical inner segment cross section, is a polarization detector both by solving numerically Maxwell's equations for modal propagation in a dielectric waveguide model of the double cones of Lepomis cyanellus (green sunfish), and by measuring directly the light power throughput through double cones as a function of input polarization. We further hypothesize that the expected weak polarization modulation of the individual double cone is greatly enhanced by a class of """"""""polarization-opponent"""""""" neurons in the inner retina which receive opposite signed inputs from double cones with their major elliptical axes arranged in orthogonal """"""""tetradic"""""""" mosaics in sunfish and other species. We propose to locate and record from these hypothetical inner retinal neurons with voltage- sensitive dyes. Finally, we hypothesize that the role of this system of polarization-opponent neurons is to serve as a common mode rejection system for randomly polarized light (such as the underwater spacelight), and to confer on the animals which possess it polarization contrast sensitivity. This latter constitutes a heretofore undescribed kind of vision in vertebrates, and should enable those possessing it to segregate objects on the basis of the polarization distribution of the light reflected from them. We propose behavioral experiments in sunfish to characterize this predicted novel visual ability. Whilst the proposed work will have no immediate transfer to the study of human vision, we expect important spinoffs in the practical implementation of waveguide theory to human vision, in understanding underwater biology and ecology, and in instrumentation for stimulating and recording from tissue-mosaics.
