Songbirds use pulse tone register in two voices to generate low-frequency sound

Abstract

The principal physical mechanism of sound generation is similar in songbirds and humans, despite large differences in their vocal organs. Whereas vocal fold dynamics in the human larynx are well characterized, the vibratory behaviour of the sound-generating labia in the songbird vocal organ, the syrinx, is unknown. We present the first high-speed video records of the intact syrinx during induced phonation. The syrinx of anaesthetized crows shows a vibration pattern of the labia similar to that of the human vocal fry register. Acoustic pulses result from short opening of the labia, and pulse generation alternates between the left and right sound sources. Spontaneously calling crows can also generate similar pulse characteristics with only one sound generator. Airflow recordings in zebra finches and starlings show that pulse tone sounds can be generated unilaterally, synchronously or by alternating between the two sides. Vocal fry-like dynamics therefore represent a common production mechanism for low-frequency sounds in songbirds. These results also illustrate that complex vibration patterns can emerge from the mechanical properties of the coupled sound generators in the syrinx. The use of vocal fry-like dynamics in the songbird syrinx extends the similarity to this unusual vocal register with mammalian sound production mechanisms.

Evolution of Vocal Diversity through Morphological Adaptation without Vocal Learning or Complex Neural Control

“…If the frequencies are more similar to each other, the two sources become “locked” and the resulting vibrations are of lower frequency than if the labial source were to vibrate on its own (Figure 2C, “locking”). This is consistent with the observed shift to higher frequencies after membrane disabling across species (Figure 3), as well as reduced pulse-like quality of the vibrations (Figure 4) [20, 21]. The pulsatile oscillations arise from the nonlinear interaction of two oscillators, the MT and the labia.…”

“…Ultimately, these acoustic features could be attributed to the increased resistance across the tracheophone syrinx when the MT are engaged as they cause a narrowing of the trachea. While oscines achieve some of these acoustic features through neuromuscular control of their two sound sources [20, 21, 23–26], suboscines do not have the same level of neuromuscular control [12, 28] and instead likely rely on intrinsic, morphological qualities such as the MT to achieve these acoustic features. Our data support this, and consistently indicate that the intact MT enable the generation of higher amplitudes, increased pulse-like quality, and lower frequencies.…”

“…Instead, even the two labial sound sources appear to interact and “lock”. This is in contrast to oscines, in which the two labial sound generators are used to simultaneously generate independent tones [15, 23, 30], while the two sources can also be “locked” during generation of pulse tones [20, 29]. Locking of oscillators in tracheophones, as in other multi-source vocal organs, facilitates generation of a variety of acoustic features, including pulse tone sounds with rich harmonic content, amplitude modulation and increased sound amplitude.…”

Mechanisms of song production in the Australian magpie

“…Other vibratory modes include a high-pitched falsetto register and a low-pitched pulse tone or vocal fry register. Evidence for a pulse tone register in songbirds was reported by Jensen et al (2007).…”

Amplitude and frequency modulation control of sound production in a mechanical model of the avian syrinx

“…Jensen et al, 2007), imaging at sufficiently high temporal resolution remains an experimental challenge. Invasive techniques that use fibre optics provide direct observations, but have the disadvantage that birds have to be anaesthetized: controlled vocalizations can only be induced with gas injections or brain stimulation (Goller and Larsen, 1997a;Goller and Larsen, 1997b;Larsen and Goller, 2002).…”