Neural song control system of hummingbirds: Comparison to swifts, vocal learning (Songbirds) and nonlearning (Suboscines) passerines, and vocal learning (Budgerigars) and nonlearning (Dove, owl, gull, quail, chicken) nonpasserines

Abstract

Males of certain hummingbird species such as Anna's hummingbirds (Calypte anna) learn their song during postnatal development. Here we report that male Anna's hummingbirds and male Amazilia hummingbirds (Amazilia amazilia), two singing hummingbird species, possess forebrain areas that are similar in morphological appearance, location, and connectivity to the song control areas RA (nucleus robustus archistriatalis), HVC (nucleus hyperstriatalis ventrale, pars caudale, or higher vocal center), and LMAN (lateral part of nucleus mangnocellularis anterioris) of oscine passerines (songbirds). The vocal control areas of songbirds are further defined by the expression of androgen receptors. Similarly, the singing hummingbird species express androgen receptors in the LMAN-like area and in the HVC-like area. The hummingbird RA projects to the medullary syringeal motonucleus nXIIts (nucleus hypoglossus pars tracheosyringealis) and the respiratory premotonucleus RAm (nucleus retroambigualis). The HVC-, RA-, and LMAN-like areas are rudimentary in adult male ruby-throated hummingbirds (Archilochus colubris) and Allen's hummingbirds (Selasphorus sasin) and not distinguishable in female hummingbirds, none of which sing. Vocal-area-like forebrain areas (delineated by the cytoarchitecture or androgen receptor expression) were not found in vocal nonlearning swifts and suboscines, the taxonomic sister groups of hummingbirds and songbirds, respectively. These areas were also missing in owls, ring doves, gulls, and gallinaceous species, nonpasserines that do not learn vocalizations. Budgerigars (vocal learners) are known to have forebrain vocal areas, but these areas do not express sex steroid receptors. These data suggest that hummingbirds and songbirds belong to two groups of birds that have common forebrain circuits. Parts of this circuit are organized as nuclear-like structures (LMAN, HVC, RA) in species that learn to sing.