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.

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.

Based on quantitative cluster analyses of 52 constitutively expressed or behaviorally regulated genes in 23 brain regions, we present a global view of telencephalic organization of birds. The patterns of constitutively expressed genes revealed a partial mirror image organization of three major cell populations that wrap above, around, and below the ventricle and adjacent lamina through the mesopallium. The patterns of behaviorally regulated genes revealed functional columns of activation across boundaries of these cell populations, reminiscent of columns through layers of the mammalian cortex. The avian functionally regulated columns were of two types: those above the ventricle and associated mesopallial lamina, formed by our revised dorsal mesopallium, hyperpallium, and intercalated hyperpallium; and those below the ventricle, formed by our revised ventral mesopallium, nidopallium, and intercalated nidopallium. Based on these findings and known connectivity, we propose that the avian pallium has four major cell populations similar to those in mammalian cortex and some parts of the amygdala: 1) a primary sensory input population (intercalated pallium); 2) a secondary intrapallial population (nidopallium/hyperpallium); 3) a tertiary intrapallial population (mesopallium); and 4) a quaternary output population (the arcopallium). Each population contributes portions to columns that control different sensory or motor systems. We suggest that this organization of cell groups forms by expansion of contiguous developmental cell domains that wrap around the lateral ventricle and its extension through the middle of the mesopallium. We believe that the position of the lateral ventricle and its associated mesopallium lamina has resulted in a conceptual barrier to recognizing related cell groups across its border, thereby confounding our understanding of homologies with mammals.

Twice each year, millions of night-migratory songbirds migrate thousands of kilometers. To find their way, they must process and integrate spatiotemporal information from a variety of cues including the Earth's magnetic field and the night-time starry sky. By using sensory-driven gene expression, we discovered that nightmigratory songbirds possess a tight cluster of brain regions highly active only during night vision. This cluster, here named ''cluster N,'' is located at the dorsal surface of the brain and is adjacent to a known visual pathway. In contrast, neuronal activation of cluster N was not increased in nonmigratory birds during the night, and it disappeared in migrants when both eyes were covered. We suggest that in night-migratory songbirds cluster N is involved in enhanced night vision, and that it could be integrating visionmediated magnetic and͞or star compass information for nighttime navigation. Our findings thus represent an anatomical and functional demonstration of a specific night-vision brain area.behavioral molecular mapping ͉ bird orientation ͉ cognition ͉ magnetic sense ͉ ZENK (zif268, Egr-1, NGF-1A, and N ight-migratory songbirds use both a geomagnetic and a star compass to orient during migration (1-6) but the underlying brain circuits are unknown. Star-compass orientation requires vision in dim light for processing constellations of the night-time starry sky. Surprisingly, magnetic-compass orientation also seems to require night vision: magnetic-compass orientation is dependent on the wavelength of the dim ambient light (4, 7), birds with their right eye covered seem unable to perform magnetic compass orientation (8), and birds can still perform magnetic compass orientation with their pineal gland removed (9). Current evidence suggests that visual sensing of the magnetic field occurs through the eyes by means of a light-activated, radical-pair based magnetodetector (4,7,(10)(11)(12)(13). Another type of magnetodetector based on magnetite seems to be predominantly involved in detecting changes in magnetic intensity and͞or inclination (4, 14-16). Together, these findings predict that processing of both magnetic-and star-compass information during night-time migration requires specialized night-time visual processing in night-migratory songbirds. We tested this hypothesis by using sensory-driven gene expression (17) to identify brain regions involved in night-and day-time vision in migratory and nonmigratory songbirds. Our results suggest that night-migratory songbirds do indeed possess a brain area specialized for night vision. MethodsTest Subjects. We examined two distantly related species of wild-caught night-migratory songbirds [garden warblers (GWs), Sylvia borin; and European robins (ERs), Erithacus rubecula] and two distantly related species of nonmigratory songbirds [zebra finches (ZFs), Taeniopygia guttata; and canaries (CNs), Serinus canaria]. The GWs, ERs, and ZFs were kept inside a wooden building under the local photoperiod for at least 5 days before the experiment. Behaviora...