Learning to breathe and sing: development of respiratory-vocal coordination in young songbirds

Abstract

How do animals with learned vocalizations coordinate vocal production with respiration? Songbirds such as the zebra finch learn their songs, beginning with highly variable babbling vocalizations known as subsong. After several weeks of practice, zebra finches are able to produce a precisely timed pattern of syllables and silences, precisely coordinated with expiratory and inspiratory pulses (Franz M, Goller F. J Neurobiol 51: 129-141, 2002). While respiration in adult song is well described, relatively little is known about respiratory patterns in subsong or about the processes by which respiratory and vocal patterns become coordinated. To address these questions, we recorded thoracic air sac pressure in juvenile zebra finches prior to the appearance of any consistent temporal or acoustic structure in their songs. We found that subsong contains brief inspiratory pulses (50 ms) alternating with longer pulses of sustained expiratory pressure (50-500 ms). In striking contrast to adult song, expiratory pulses often contained multiple (0-8) variably timed syllables separated by expiratory gaps and were only partially vocalized. During development, expiratory pulses became shorter and more stereotyped in duration with shorter and fewer nonvocalized parts. These developmental changes eventually resulted in the production of a single syllable per expiratory pulse and a single inspiratory pulse filling each gap, forming a coordinated sequence similar to that of adult song. To examine the role of forebrain song-control nuclei in the development of respiratory patterns, we performed pressure recordings before and after lesions of nucleus HVC (proper name) and found that this manipulation reverses the developmental trends in measures of the respiratory pattern.

Vocal motor changes beyond the sensitive period for song plasticity

“…Such changes are analogous to developmental changes in syllable timing and suggest a shared mechanism underlying temporal changes in juvenile and adult songbirds (Glaze and Troyer 2013). For example, because intersyllable gaps coincide with short inspirations during song reviewed in Goller and Cooper 2004;Veit et al 2011), the shortening of gaps could indicate that birds are more efficient at replenishing their air supply with shorter inspirations.…”

The autonomic nervous system is the engine for vocal development through social feedback

“…This rhythmicity suggests that this output is driven by the oscillatory activity of the nervous system. As in developing songbirds [30], the temporal structure of babbling output by infants is tightly locked to respiration in marmoset monkey infants [26**], with respiration providing the power for generating vocal sounds [31]. Approximately every second, an utterance phase-locked to the respiratory rhythm is produced.…”

The respiratory-vocal system of songbirds

“…Instead, they produce multiple syllables separated by silent gaps within a single long EP, a pattern that is never observed in older birds. HVC lesions in young birds that have just mastered the one-to-one relationship between EPs and syllables causes then to relapse into the more immature vocal patterns that lack vocal-respiratory coordination (Veit et al, 2011). Together, these finding suggest not only that HVC plays a fundamental role in controlling the overall timing of song but that it also plays a critical role in establishing the coordination between vocal muscular control and breathing.…”