Visual but not trigeminal mediation of magnetic compass information in a migratory bird

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Abstract

Magnetic compass information has a key role in bird orientation, but the physiological mechanisms enabling birds to sense the Earth's magnetic field remain one of the unresolved mysteries in biology. Two biophysical mechanisms have become established as the most promising magnetodetection candidates. The iron-mineral-based hypothesis suggests that magnetic information is detected by magnetoreceptors in the upper beak and transmitted through the ophthalmic branch of the trigeminal nerve to the brain. The light-dependent hypothesis suggests that magnetic field direction is sensed by radical pair-forming photopigments in the eyes and that this visual signal is processed in cluster N, a specialized, night-time active, light-processing forebrain region. Here we report that European robins with bilateral lesions of cluster N are unable to show oriented magnetic-compass-guided behaviour but are able to perform sun compass and star compass orientation behaviour. In contrast, bilateral section of the ophthalmic branch of the trigeminal nerve in European robins did not influence the birds' ability to use their magnetic compass for orientation. These data show that cluster N is required for magnetic compass orientation in this species and indicate that it may be specifically involved in processing of magnetic compass information. Furthermore, the data strongly suggest that a vision-mediated mechanism underlies the magnetic compass in this migratory songbird, and that the putative iron-mineral-based receptors in the upper beak connected to the brain by the trigeminal nerve are neither necessary nor sufficient for magnetic compass orientation in European robins.

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Most cited references 26

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Magnetic compass of European robins.

W. Wiltschko, R. Wiltschko (1972)

The magnetic compass of European robins does not use the polarity of the magnetic field for detecting the north direction. The birds derive their north direction from interpreting the inclination of the axial direction of the magnetic field lines in space, and they take the direction on the magnetic north-south axis for "north" where field lines and gravity vector form the smaller angle.

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Migrating songbirds recalibrate their magnetic compass daily from twilight cues.

Henrik Mouritsen, Lauren Cochran, Martin Wikelski (2004)

Night migratory songbirds can use stars, sun, geomagnetic field, and polarized light for orientation when tested in captivity. We studied the interaction of magnetic, stellar, and twilight orientation cues in free-flying songbirds. We exposed Catharus thrushes to eastward-turned magnetic fields during the twilight period before takeoff and then followed them for up to 1100 kilometers. Instead of heading north, experimental birds flew westward. On subsequent nights, the same individuals migrated northward again. We suggest that birds orient with a magnetic compass calibrated daily from twilight cues. This could explain how birds cross the magnetic equator and deal with declination.

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Molecular Mapping of Movement-Associated Areas in the Avian Brain: A Motor Theory for Vocal Learning Origin

Gesa Feenders, Miriam Liedvogel, Miriam Rivas … (2008)

Vocal learning is a critical behavioral substrate for spoken human language. It is a rare trait found in three distantly related groups of birds-songbirds, hummingbirds, and parrots. These avian groups have remarkably similar systems of cerebral vocal nuclei for the control of learned vocalizations that are not found in their more closely related vocal non-learning relatives. These findings led to the hypothesis that brain pathways for vocal learning in different groups evolved independently from a common ancestor but under pre-existing constraints. Here, we suggest one constraint, a pre-existing system for movement control. Using behavioral molecular mapping, we discovered that in songbirds, parrots, and hummingbirds, all cerebral vocal learning nuclei are adjacent to discrete brain areas active during limb and body movements. Similar to the relationships between vocal nuclei activation and singing, activation in the adjacent areas correlated with the amount of movement performed and was independent of auditory and visual input. These same movement-associated brain areas were also present in female songbirds that do not learn vocalizations and have atrophied cerebral vocal nuclei, and in ring doves that are vocal non-learners and do not have cerebral vocal nuclei. A compilation of previous neural tracing experiments in songbirds suggests that the movement-associated areas are connected in a network that is in parallel with the adjacent vocal learning system. This study is the first global mapping that we are aware for movement-associated areas of the avian cerebrum and it indicates that brain systems that control vocal learning in distantly related birds are directly adjacent to brain systems involved in movement control. Based upon these findings, we propose a motor theory for the origin of vocal learning, this being that the brain areas specialized for vocal learning in vocal learners evolved as a specialization of a pre-existing motor pathway that controls movement.