Light-dependent magnetoreception in zebra finches : - from behaviour to receptor

Abstract: It is well known that animals can use a wide variety of information sources to help them orient and navigate asthey move over short or long distances. Birds can rely on information from the sun, the skylight polarizationpattern, the stars, landmarks and the Earth’s magnetic field for orientation and navigation. However, despite thebehavioural evidence supporting the use of the magnetic field as an orientation and navigation cue, the sensorymechanisms underlying magnetoreception are still missing. In this thesis, I studied one of the proposed modelsfor magnetoreception: the light-dependent magnetic compass in the zebra finch. The light-dependent magneticcompass of birds provides directional information about the spatial alignment of the geomagnetic field. It isproposed to be located in the avian retina, and be mediated by a light-induced, biochemical radical-pairmechanism involving cryptochromes as putative receptor molecules.The general goal of my thesis was to study how the light-dependent magnetic compass works in birds byinvestigating the proposed mechanism at different levels. I studied the behavioural responses of zebra finchestrained to relocate a food reward inside a 4-arm plus maze, using the magnetic field as the only cue. By testingbirds under different light conditions, I assessed the spectral properties of the magnetic compass. I showed thatthe magnetic compass of the zebra finch exhibits the same spectral properties as has been described inmigratory birds, and that the mechanism is most likely mediated by a radical-pair mechanism (Paper I). Toidentify which of the three different cryptochromes found in birds is the most likely candidate magnetoreceptor Istudied their gene expression patterns over the circadian day. My assumption was that any cryptochromerelated to circadian tasks should exhibit a daily variation, whereas one involved in magnetoreception is expectedto be expressed constantly over time. I found that Cry1 and Cry2 followed a circadian variation, whereas Cry4was expressed at equal levels over the day, irrespective of time, which suggested that Cry4 is a better candidatefor magnetoreception than the other cryptochromes (Paper II). With the findings from both the behavioural andgene expression studies supporting the involvement of cryptochromes in magnetoreception, I next investigatedthe location and distribution of Cry1 and Cry4 in the zebra finch retina using immunodetection. I found that Cry1was expressed in the basal part of the outer segments of the UV cones. Taking into account that Cry1 is likelynot involved in magnetoreception, my findings open up the possibility that Cry1 is involved in a different, yetundetermined function in the avian UV/V cones (paper III). Cry4, on the other hand, was expressed in asubpopulation of peripheral horizontal cells in the zebra finch retina. These Cry4-expressing cells form a ringaround the periphery of the retina, suggesting a new model for how the magnetic field may be perceived bybirds. It also provides novel solution to the problem how the magnetoreception system may coexist with thevisual system without interfering with each other (paper IV).Taken together, the findings presented in the chapters of this thesis show that the light-dependent magneticcompass in zebra finches works similar to other birds and involves a radical-pair mechanism probably based onCry4. The distribution of Cry4 in the zebra finch retina offers a new view on how birds, and maybe otherorganisms, can detect the Earth’s magnetic field. Cry1, on the other hand, is likely involved in a novel function inthe avian UV/V cones unrelated to magnetoreception.