The Oscine Song System Considered in the Context of the Avian Brain: Lessons Learned from Comparative Neurobiology

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Abstract
The oscine song system has emerged as one of the leading model systems for studying motor learning in vertebrates, combining an easily recorded behavior with a discrete neural substrate. That neural substrate seems to be distinct from other structures in the avian brain and thus is often studied in isolation. However, the song system is unlikely to have evolved ex nihilo, and should share some features with the parts of the avian brain from which it evolved. Identification of its evolutionary precursors should help us apply what we know about the song system to other vertebrate motor systems, and vice versa. Here, I review the homologies between parts of the avian and mammalian telencephala and explain where the song system nuclei reside in this context. The organization of the song system is then compared to other parts of the avian brain and the brains of nonoscine birds. Study of the nonoscine brain has revealed a ‘general motor pathway’ from caudolateral neostriatum (NCL) to intermediate archistriatum (Ai) that resembles the song system motor pathway in its anatomical organization. No part of this motor pathway projects directly to brainstem vocal or respiratory centers in nonoscines, but it does innervate a wide variety of motor and premotor neuron populations that mediate other behaviors. This general motor pathway may be accompanied by an ‘anterior forebrain pathway’ , suggesting that the song system is simply a specialization of a part of this preexisting circuit. This hypothesis has implications for how accessory structures of the song system (e.g. HVc shelf, LMAN shell) are regarded, can help explain how the forebrain vocal control systems of three avian taxa (parrots, hummingbirds, and songbirds) could have evolved independently yet be so similar in organization, and makes testable predictions concerning the anatomy of the song system and the nonoscine brain.