Abstract
The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot “core” song system is similar to the song systems of songbirds and hummingbirds, whereas the “shell” song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.
Highlights
We performed a series of experiments that led us to conclude that brain regions that include song nuclei of parrots have three concentric levels of specializations: (1) the inner core song nuclei; (2) the outer shell song nuclei that surround the cores; and (3) the outer non-vocal motor regions that surround the song nuclei shells
We found that PVALB expression revealed core and shell regions of expression that included the posterior song nuclei central nucleus of the lateral nidopallium (NLC) and central nucleus of the anterior arcopallium (AAC) and surrounding motor areas relative to the surrounding nidopallium (N) and arcopallium (A), respectively (Fig 2a; serial sections in 2b)
The FOXP1 transcription factor, a co-factor of FOXP2 that is required for speech and song acquisition in humans and songbirds [53], was reported to be differentially expressed in the NLC analog of vocal learners [35,54]; we found here that it is expressed in a gradient of higher to lower expression from the NLC core to the shell, but only for the part of the shell that corresponds to the vocalizing-driven song nucleus (Fig 7c and 7d)
Summary
We performed a series of experiments that led us to conclude that brain regions that include song nuclei of parrots have three concentric levels of specializations: (1) the inner core song nuclei; (2) the outer shell song nuclei that surround the cores; and (3) the outer non-vocal motor regions that surround the song nuclei shells. When analyzed in the context of our differential and functionally-defined (vocalizing-driven) gene expression profiles and Nissl-defined patterns, we found that targeted biocytin injections into the AAC core (Fig 11a) with very little leakage in the shell retrogradely labeled a high density of cell bodies and some anterogradely labeled fibers within the PVALB-defined (from strongest to weakest) NLC core, MO core, and NAO core relative to the shell regions (Fig 11b– 11j; Table 2). Doi:10.1371/journal.pone.0118496.g018 not with brain section size alone, indicative of another variable, perhaps behavior, that its size could be associated with
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