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.
Highlights
Vocal learning is the ability to imitate vocalization from others, and is a critical behavioral substrate for spoken human language
The areas of robust movement-associated activation were closest to the vocal nuclei, and we investigated this activation further in a non-migratory songbird, the zebra finch (Taeniopygia guttata), for which the vocal system has been studied in detail
The anatomical extent of the movementassociated areas are larger than the vocal nuclei, which is consistent with a greater amount of musculature involved in the control of limb and body movements relative to that for the syrinx
Summary
Vocal learning is the ability to imitate vocalization from others, and is a critical behavioral substrate for spoken human language. None of these cerebral vocal nuclei have been found to date in vocal nonlearners, such as in the suboscine songbirds closely related to songbirds [13,14], the interrelated doves [15,16], and the distantly related galliforms ([17], Fig. 1B). According to the dominant hypothesis [4,14], within the past 65 million years 3 out of 23 avian orders independently evolved seven similar cerebral vocal nuclei for a complex behavior ([7], Fig. 1A, red dots) The reason for these remarkable similarities had remained mysterious, but they suggest that the evolution of brain structures for vocal learning is under strong genetic or epigenetic constraints. Of the multiple hypotheses proposed for the evolution of vocal learning [14,22,23], including for spoken language, our findings support those that suggest a motor origin [10,24,25]
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