Avian Ultraviolet/Violet Cones Identified as Probable Magnetoreceptors

Abstract

BackgroundThe Radical-Pair-Model postulates that the reception of magnetic compass directions in birds is based on spin-chemical reactions in specialized photopigments in the eye, with cryptochromes discussed as candidate molecules. But so far, the exact subcellular characterization of these molecules in the retina remained unknown.Methodology/Principal FindingsWe here describe the localization of cryptochrome 1a (Cry1a) in the retina of European robins, Erithacus rubecula, and domestic chickens, Gallus gallus, two species that have been shown to use the magnetic field for compass orientation. In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina. Electron microscopy shows Cry1a in ordered bands along the membrane discs of the outer segment, and cell fractionation reveals Cry1a in the membrane fraction, suggesting the possibility that Cry1a is anchored along membranes.Conclusions/SignificanceWe provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model. Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.

Functional MRI and functional connectivity of the visual system of awake pigeons

“…In fact, birds have a vision-based magnetic compass that perceives the inclination of the earth's magnetic field and thus derives directions from the axial course of the field lines and their inclination in space [45]. This unusual functional mode arises from the underlying physical processes: the avian magnetic compass is based on a radical pair mechanism [46] in the eye, where Cryptochrome 1a, the most likely candidate receptor molecule for mediating directional information, is located along the disks of the outer segments of the UV-receptors [47]. There is evidence that this light-based magnetic system is at least to some extent a part of the imageforming visual pathway [48].…”

Cryptochrome expression in the eye of migratory birds depends on their migratory status

“…In vertebrates, the night-migrating Passeriformes [the European robin (Erithacus rubecula) and the garden warbler (Sylvia borin)], the homing pigeon (Columbia livia) and the domestic fowl (Gallus gallus) are among the most extensively studied model species because they have been shown to be able to extract compass information from the Earth's magnetic field (Wiltschko and Wiltschko, 1972;Wiltschko and Wiltschko, 2002;Mouritsen et al, 2004;Wilzeck et al, 2010;Niessner et al, 2011). In these species, experimental evidence points to CRYs as the key molecules for light-mediated, radical-pair-based magnetic compass orientation (Solov'yov et al, 2010;Mouritsen et al, 2004;Niessner et al, 2011).…”

“…In these species, experimental evidence points to CRYs as the key molecules for light-mediated, radical-pair-based magnetic compass orientation (Solov'yov et al, 2010;Mouritsen et al, 2004;Niessner et al, 2011). In both migratory species, the European robin and the garden warbler, CRYs are expressed in the retina of the eye and their magnetic orientation performances under low-intensity monochromatic light are wavelength-dependent, i.e.…”

The quantum needle of the avian magnetic compass

“…The primary sensory receptors are located in the eyes (2,3,(5)(6)(7), and directional information is processed bilaterally in a small part of the forebrain accessed via the thalamofugal visual pathway. The evidence currently points to a chemical sensing mechanism based on photo-induced radical pairs in cryptochrome flavoproteins in the retina (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). Anisotropic magnetic interactions within the radicals are thought to give rise to intracellular levels of a cryptochrome signaling state that depend on the orientation of the bird's head in the Earth's magnetic field (8,9,19).…”