Songbird: a unique animal model for studying the molecular basis of disorders of vocal development and communication

Abstract

Like humans, songbirds are one of the few animal groups that learn vocalization. Vocal learning requires coordination of auditory input and vocal output using auditory feedback to guide one's own vocalizations during a specific developmental stage known as the critical period. Songbirds are good animal models for understand the neural basis of vocal learning, a complex form of imitation, because they have many parallels to humans with regard to the features of vocal behavior and neural circuits dedicated to vocal learning. In this review, we will summarize the behavioral, neural, and genetic traits of birdsong. We will also discuss how studies of birdsong can help us understand how the development of neural circuits for vocal learning and production is driven by sensory input (auditory information) and motor output (vocalization).

Fig. 1.

Song learning and species differences in song pattern. (A) Examples of song development in a zebra finch. The zebra finch is known as a closed-ended learner, meaning that once a stable species-specific song pattern “motif” is developed, the song structure remains unchanged throughout life [8, 22, 74]. This stereotypy of crystallized song enables precise quantification of the similarities and differences in vocal development and song patterns between experiments, allowing for examination of genetic and epigenetic factors that contribute to the acquisition and maintenance of complex vocal patterns. (B, C) Examples of adult song patterns of two Bengalese finches (B) and two Java sparrows (C).

Fig. 2.

Examples of song development and syllable scatter plots [duration versus mean frequency modulation (FM)] in an intact, a socially isolated, an early-deafened, and an adult-deafened bird. (A, B) Colored portions (blue and green) highlight stable song motifs. The intact and socially isolated birds exhibited song stability around dph 110. The crystallized song pattern of the socially isolated bird is similar to that of the intact (normal) bird, except for a prolonged and variable syllable (green bracket). (C) Orange shading highlights stable song motifs. (D) Song before and after adult deafening. Blue shading indicates crystallized motifs, which developed at dph 100–150.

Fig. 3.

Schematic diagrams of the brain areas involved in vocal learning and production. (modified from Horita and Wada, 2011 [20], and Pfenning et al., 2014 [50]). (A, B) Upper drawings illustrate a brain section from a male zebra finch (A) and a human (B). Solid black arrows denote connections within the posterior vocal motor circuit (from HVC to RA to brainstem motor nuclei). White arrows denote connections within the basal ganglia–forebrain circuit. Dashed black arrows denote connections between the two circuits. Red arrows show the direct connections found only in vocal learners, which project from vocal motor cortex regions to brain stem vocal motor neurons. (C, D) Lower drawings illustrate comparative and simplified connectivity of anterior and posterior vocal circuits in a songbird (C) and a human (D). DLM: dorsal lateral medial nucleus of the thalamus, DM: dorsal medial nucleus of the midbrain, HVC: a vocal nucleus (no acronym), LMAN: lateral MAN, MAN: magnocellular nucleus of the anterior nidopallium, nXIIts: twelfth nucleus, tracheosyringeal part, RA: robust nucleus of the arcopallium, Ram/Pam: nucleus retroambiguus/parambiguus.

Fig. 4.

A schematic highlighting the use of songbirds as a research model for disorders of vocal development and communication.