Double cones as a basis for a new type of polarization vision in vertebrates

Many invertebrates and vertebrates are sensitive to the polarization of light. The biophysical basis of invertebrate polarization sensitivity is an intrinsic dichroism, the alignment of chromophores along the photoreceptor microvilli. But such dichroism to axially propagating light is not present in vertebrate photoreceptors, whose chromophores are free to rotate in the plane of the outer-segment disc membranes, and a biophysical mechanism responsible for vertebrate polarization sensitivity has not been established. We hypothesize that the roughly elliptical cross-sectioned double-cone inner segment acts as a birefringent, polarization-sensitive dielectric waveguide, and that the double cone mosaic generates a 'polarization contrast' neural image. Here we confirm three predictions derived from these hypotheses: (1) 90 degrees periodicity for polarization sensitivity; (2) polarization sensitivity maxima corresponding to the absolute orientation of the axes of the double-cone inner-segment cross-sections; and (3) action spectrum for polarization sensitivity corresponding to the absorption spectrum of the double cones. We also present evidence for a polarization-opponent neural encoding in vertebrates.