A mechanism for frequency modulation in songbirds shared with humans

Abstract

In most animals that vocalize, control of fundamental frequency is a key element for effective communication. In humans, subglottal pressure controls vocal intensity but also influences fundamental frequency during phonation. Given the underlying similarities in the biomechanical mechanisms of vocalization in humans and songbirds, songbirds offer an attractive opportunity to study frequency modulation by pressure. Here, we present a novel technique for dynamic control of subsyringeal pressure in zebra finches. By regulating the opening of a custom-built fast valve connected to the air sac system, we achieved partial or total silencing of specific syllables, and could modify syllabic acoustics through more complex manipulations of air sac pressure. We also observed that more nuanced pressure variations over a limited interval during production of a syllable concomitantly affected the frequency of that syllable segment. These results can be explained in terms of a mathematical model for phonation that incorporates a nonlinear description for the vocal source capable of generating the observed frequency modulations induced by pressure variations. We conclude that the observed interaction between pressure and frequency was a feature of the source, not a result of feedback control. Our results indicate that, beyond regulating phonation or its absence, regulation of pressure is important for control of fundamental frequencies of vocalizations. Thus, although there are separate brainstem pathways for syringeal and respiratory control of song production, both can affect airflow and frequency. We hypothesize that the control of pressure and frequency is combined holistically at higher levels of the vocalization pathways.

Figure 1.

Novel method for manipulation of vocal output. A, The miniature valve. Current through a solenoid rapidly moves a magnet to open or close a hole that connects the air sac system with the atmosphere. The direction of the current flow sets the direction of movement of the magnet. Absent any current, the valve is closed (i.e., the air sac system is sealed). B, Implanted bird carrying a backpack with the valve attached. C, D, Spectrograph, sonograph, and air sac pressure of a bird before (C) and after (D), valve implantation. Zero pressure represents atmospheric pressure, and the pressure values were normalized to the maximum value. The pressure patterns and song acoustics, including harmonic stacks, rapid trills, and inspiratory syllables, remain unchanged after device implantation.

Figure 2.

Complete muting of syllables. A, Effects on acoustics of syllable A (top) when a positive current step is applied, opening the tube. The air sac pressure is measured simultaneously using a pressure sensor connected to the abdominal air sac. When muting syllable A, only the magnitude of the pressure pattern is modified, leaving the shape unchanged. The bird is able to repressurize after muting syllable A and sing syllable B immediately after the current step finishes, closing the tube. B, Muting part of a syllable, followed by rapid repressurization permitting singing of the following syllable (an inspiratory syllable in this case). C, Inspiratory syllables can also be muted with this method. When the valve is closed, a rapid repressurization occurs (final dotted line).

Figure 3.

Acoustic changes driven by pressure changes. A, A decrease in the air sac pressure during vocalizing the second syllable C (harmonic stack) results in a decrease of the fundamental frequency. During intact vocalizations, when the first syllable C was not detected by the computer program, the pressure and fundamental frequency remain constant. B, The same effect is shown for syllable E, a different harmonic stack in the same bird. The panels follow the same organization as in Fig. 2.

Figure 4.

Acoustic and timing differences resulting from depressurization of the air sac system. A, The second syllable E of Bird b32 is modified in duration and fundamental frequency when the tube connected to the air sac system is opened. The opening and closing of the valve (“O” and “C” arrows, respectively) generate a click sound, shown in the sonogram as vertical lines. B, The same effect is shown for syllable C of Bird lb218.

Figure 5.

Frequency modulations in harmonic stacks resulting from pressure modulations. The average fundamental frequency is calculated for each harmonic stack in the intact and modified condition (pressure drop), identified by bird, syllable, and line color (e.g., Bird b32, syllable E, red). For each syllable, the maximum and minimum values of the fundamental frequency are also shown with black dotted lines (mean ± SD).

Figure 6.

Mathematical model for song production. A, The region of the parameter space where oscillations occur is shown with its corresponding value of fundamental frequency displayed with red dots. The black and red lines indicate bifurcations in the parameter space (Hopf and SNILC bifurcations, respectively). The blue line in the red surface indicates a possible path where tension is maintained constant while the pressure is changing, resulting in a frequency modulation. B, A path in parameter space where tension is constant and frequency of the oscillations is set through pressure. Red bars highlight that frequency modulation through pressure is more important for low-frequency sounds. C, This model also allows a change in frequency through changes in tension. D, F, The measured air sac pressure during singing was smoothed and fed as a parameter of the mathematical model (see Materials and Methods). E, G, The synthetic syllables generated with the mathematical model are very similar to the recorded ones. An intact singing bird is shown in D and E, and the same type of syllable with a depressurization of air sac system is shown in F and G. The pressure drop generates a frequency drop, more clearly observed in the upper harmonics of the sonogram.