暂无摘要。

Vocal learning is a complex acquired social behavior that has been found only in very few animals. The process of animal vocal learning requires the participation of sensorimotor function. By accepting external auditory input and cooperating with repeated vocal imitation practice, a stable pattern of vocal information output is eventually formed. In parallel evolutionary branches, humans and songbirds share striking similarities in vocal learning behavior. For example, their vocal learning processes involve auditory feedback, complex syntactic structures, and sensitive periods. At the same time, they have evolved the hierarchical structure of special forebrain regions related to vocal motor control and vocal learning, which are organized and closely associated to the auditory cortex. By comparing the location, function, genome, and transcriptome of vocal learning-related brain regions, it was confirmed that songbird singing and human language-related neural control pathways have certain analogy. These common characteristics make songbirds an ideal animal model for studying the neural mechanisms of vocal learning behavior. The neural process of human language learning may be explained through similar neural mechanisms, and it can provide important insights for the treatment of language disorders.

Only a few distantly related mammals and birds have the trait of complex vocal learning, which is the ability to imitate novel sounds. This ability is critical for speech acquisition and production in humans, and is attributed to specialized forebrain vocal control circuits that have several unique connections relative to adjacent brain circuits. As a result, it has been hypothesized that there could exist convergent changes in genes involved in neural connectivity of vocal learning circuits. In support of this hypothesis, expanding on our related study (Pfenning et al. [2014] Science 346: 1256846), here we show that the forebrain part of this circuit that makes a relatively rare direct connection to brainstem vocal motor neurons in independent lineages of vocal learning birds (songbird, parrot, and hummingbird) has specialized regulation of axon guidance genes from the SLIT-ROBO molecular pathway. The SLIT1 ligand was differentially downregulated in the motor song output nucleus that makes the direct projection, whereas its receptor ROBO1 was developmentally upregulated during critical periods for vocal learning. Vocal nonlearning bird species and male mice, which have much more limited vocal plasticity and associated circuits, did not show comparable specialized regulation of SLIT-ROBO genes in their nonvocal motor cortical regions. These findings are consistent with SLIT and ROBO gene dysfunctions associated with autism, dyslexia, and speech sound language disorders and suggest that convergent evolution of vocal learning was associated with convergent changes in the SLIT-ROBO axon guidance pathway.

BACKGROUND: Parrots belong to a group of behaviorally advanced vertebrates and have an advanced ability of vocal learning relative to other vocal-learning birds. They can imitate human speech, synchronize their body movements to a rhythmic beat, and understand complex concepts of referential meaning to sounds. However, little is known about the genetics of these traits. Elucidating the genetic bases would require whole genome sequencing and a robust assembly of a parrot genome.
RESULTS: We present a genomic resource for the budgerigar, an Australian Parakeet (Melopsittacus undulatus) -- the most widely studied parrot species in neuroscience and behavior. We present genomic sequence data that includes over 300× raw read coverage from multiple sequencing technologies and chromosome optical maps from a single male animal. The reads and optical maps were used to create three hybrid assemblies representing some of the largest genomic scaffolds to date for a bird; two of which were annotated based on similarities to reference sets of non-redundant human, zebra finch and chicken proteins, and budgerigar transcriptome sequence assemblies. The sequence reads for this project were in part generated and used for both the Assemblathon 2 competition and the first de novo assembly of a giga-scale vertebrate genome utilizing PacBio single-molecule sequencing.
CONCLUSIONS: Across several quality metrics, these budgerigar assemblies are comparable to or better than the chicken and zebra finch genome assemblies built from traditional Sanger sequencing reads, and are sufficient to analyze regions that are difficult to sequence and assemble, including those not yet assembled in prior bird genomes, and promoter regions of genes differentially regulated in vocal learning brain regions. This work provides valuable data and material for genome technology development and for investigating the genomics of complex behavioral traits.

Birdsong learning bears many similarities to human speech acquisition. Although the anterior forebrain pathway (AFP) is believed to be involved in birdsong learning, the underlying neural mechanisms are unclear. We produced two types of abnormal song learning: young birds untutored from adult \"song tutors\", or birds deafened by bilateral cochlear removal before the onset of sensory learning. We then studied how ultrastructure and electrophysiological activity changed in an AFP nucleus, Area X, among these birds at adulthood. Our results showed that, although the size of Area X did not change significantly, the numbers of synapses per unit area and compound synapses and the percent of concave synapses increased significantly in the untutored or deafened birds. The percent of perforated synapses or axo-spinous synapses decreased compared to the normally reared birds, suggesting a decreased efficiency of synaptic transmission in the untutored or deafened birds. We then identified several types of spontaneously firing cells in Area X. Cells with fast and slow firing rates did not show significant electrophysiological differences among the groups, but cells with moderate firing rates, most likely DLM-projecting neurons, fired at significantly lower rates in the untutored and deafened birds. In addition, cells firing irregularly were only found in the deafened birds. Thus, the decreased or irregular electrophysiological activity in the untutored or deafened birds, together with the corresponding ultrastructural findings, could be implicated in the abnormal song production in these two types of birds.