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Abstract:
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.
