Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation.
Migratory birds can use a magnetic compass for orientation during their migratory journeys covering thousands of kilometers. But how do they sense the reference direction provided by the Earth's magnetic field? Behavioral evidence and theoretical considerations have suggested that radical-pair processes in differently oriented, light-sensitive molecules of the retina could enable migratory birds to perceive the magnetic field as visual patterns. The cryptochromes (CRYs) have been suggested as the most likely candidate class of molecules, but do CRYs exist in the retina of migratory birds? Here, we show that at least one CRY1 and one CRY2 exist in the retina of migratory garden warblers and that garden-warbler CRY1 (gwCRY1) is cytosolic. We also show that gwCRY1 is concentrated in specific cells, particularly in ganglion cells and in large displaced ganglion cells, which also showed high levels of neuronal activity at night, when our garden warblers performed magnetic orientation. In addition, there seem to be striking differences in CRY1 expression between migratory and nonmigratory songbirds at night. The difference in CRY1 expression between migrants and nonmigrants is particularly pronounced in the large displaced ganglion cells known to project exclusively to a brain area where magnetically sensitive neurons have been reported. Consequently, cytosolic gwCRY1 is well placed to possibly be the primary magnetic-sensory molecule required for light-mediated magnetoreception.
Mouritsen
Henrik
H
Volkswagen Nachwuchsgruppe Animal Navigation, Institute of Biology, University of Oldenburg, D-26111 Oldenburg, Germany. henrik.mouritsen@oldenburg.de
Janssen-Bienhold
Ulrike
U
Liedvogel
Miriam
M
Feenders
Gesa
G
Stalleicken
Julia
J
Dirks
Petra
P
Weiler
Reto
R
D000595:Amino Acid Sequence; D025041:Animal Migration / Q000502:physiology*; D000818:Animals; D015415:Biomarkers / Q000378:metabolism; D015153:Blotting, Western; D004574:Electromagnetic Fields; D005136:Eye Proteins / Q000378:metabolism; D017952:Ganglia, Invertebrate / Q000166:cytology / Q000378:metabolism / Q000648:ultrastructure; D015870:Gene Expression / Q000502:physiology; D018613:Microscopy, Confocal; D008969:Molecular Sequence Data; D009474:Neurons / Q000502:physiology*; D009949:Orientation; D017956:Photoreceptor Cells, Invertebrate / Q000378:metabolism* / Q000502:physiology; D016760:Proto-Oncogene Proteins c-fos / Q000378:metabolism; D012160:Retina / Q000166:cytology / Q000378:metabolism* / Q000648:ultrastructure; D020308:Songbirds / Q000502:physiology*; D013997:Time Factors
D015415:Biomarkers; D005136:Eye Proteins; D016760:Proto-Oncogene Proteins c-fos