Franz Goller

Inspiratory Muscle Activity during Bird Song

The apparently continuous flow of bird song is in reality punctuated by brief periods of silence during which there are short inspirations called minibreaths. To determine whether these minibreaths are accompanied, and thus perhaps caused, by activity in inspiratory muscles, electromyographic (EMG) activity was recorded in M. scalenus in zebra finches and in M. scalenus and Mm. levatores costarum in cowbirds, together with EMGs from the abdominal expiratory muscles, air sac pressure and tracheal airflow. EMG activity in Mm. scalenus and levatores costarum consistently preceded the onset of negative air sac pressure by approximately 11 ms during both quiet respiration and singing in both species. The electrical activity of these two muscles was very similar. Compared with during quiet respiration, the amplitude of inspiratory muscle EMG during singing was increased between five- and 12-fold and its duration was decreased from >200 ms to on average 41 ms during minibreaths, again for both species, but inspiratory muscle activity did not overlap with that of the expiratory muscles. Thus, there was no indication that the inspiratory muscles acted either to shorten the duration of expiration or to reduce the expiratory effort as might occur if both expiratory and inspiratory muscles were simultaneously active. Inspiratory and expiratory muscle activities were highly stereotyped during song to the extent that together, they defined the temporal pattern of the songs and song types of individual birds.

Superfast Vocal Muscles Control Song Production in Songbirds

Birdsong is a widely used model for vocal learning and human speech, which exhibits high temporal and acoustic diversity. Rapid acoustic modulations are thought to arise from the vocal organ, the syrinx, by passive interactions between the two independent sound generators or intrinsic nonlinear dynamics of sound generating structures. Additionally, direct neuromuscular control could produce such rapid and precisely timed acoustic features if syringeal muscles exhibit rare superfast muscle contractile kinetics. However, no direct evidence exists that avian vocal muscles can produce modulations at such high rates. Here, we show that 1) syringeal muscles are active in phase with sound modulations during song over 200 Hz, 2) direct stimulation of the muscles in situ produces sound modulations at the frequency observed during singing, and that 3) syringeal muscles produce mechanical work at the required frequencies and up to 250 Hz in vitro. The twitch kinematics of these so-called superfast muscles are the fastest measured in any vertebrate muscle. Superfast vocal muscles enable birds to directly control the generation of many observed rapid acoustic changes and to actuate the millisecond precision of neural activity into precise temporal vocal control. Furthermore, birds now join the list of vertebrate classes in which superfast muscle kinetics evolved independently for acoustic communication.

Respiratory patterns and oxygen consumption in singing zebra finches

SUMMARY Song production in birds is driven by temporally complex respiratory patterns. In zebra finches (Taeniopygia guttata), song consists of repetitions of a stereotyped sequence of distinct syllables (motif). Syllables correspond to distinct expiratory pulses, which alternate with short deep inspirations. We investigated the effect of the song motor pattern on respiration using a newly developed mask system to measure oxygen consumption while simultaneously monitoring subsyringeal air sac pressure. The metabolic cost of song is closely related to song duration (mean=85.7 μl O2 g-1 min-1 over pre-song levels) and confirms earlier estimates for this species. When motif duration is controlled for, there is only small interindividual variability in oxygen consumption per motif. The oxygen measurements were also used to evaluate various methods of estimating and reporting the metabolic cost. Up to 20s before song, respiratory activity and oxygen consumption increased. Shortly before and during the introductory notes of the song bout, respiration and oxygen consumption decreased markedly. In some individuals, significant hyperventilation occurred during song, causing almost complete apnea after the song. In three different birds, we measured tracheal airflow and air sac pressure during song. Birds with higher airflow during song relative to flow during quiet respiration had a more pronounced decrease in respiratory activity after the song bout. These results suggest that gas exchange continues in the lung during the song bout and that long expiratory pressure pulses of the song motif can lead to hyperventilation but that no oxygen debt resulted from song. This research allows a first assessment of respiratory constraints that may influence the evolution of song complexity.

Somatosensory feedback modulates the respiratory motor program of crystallized birdsong

Birdsong, like human speech, involves rapid, repetitive, or episodic motor patterns requiring precise coordination between respiratory, vocal organ, and vocal tract muscles. The song units or syllables of most adult songbirds exhibit a high degree of acoustic stereotypy that persists for days or months after the elimination of auditory feedback by deafening. Adult song is assumed to depend on central motor programs operating independently from immediate sensory feedback. Nothing is known, however, about the possible role of mechanoreceptive or other somatosensory feedback in the motor control of birdsong. Even in the case of human speech, the question of “how and when sensory information is used in normal speaking conditions…u2009remains unanswered” and controversial [Smith, A. (1992) Crit. Rev. Oral Biol. Med. 3, 233–267]. We report here evidence for somatosensory modulation of ongoing song motor patterns. These patterns include the respiratory muscles that, in both birdsong and speech, provide the power for vocalization. Perturbing respiratory pressure by a brief, irregularly timed injection of air into the cranial thoracic air sac during song elicited a compensatory reduction in the electrical activity of the abdominal expiratory muscles, both in hearing and deafened adult northern cardinals (Cardinalis cardinalis). This muscle response was absent or reduced during quiet respiration, suggesting it is specifically linked to phonation. Our findings indicate that somatosensory feedback to expiratory muscles elicits compensatory adjustments that help stabilize, in real time, the subsyringeal pressure against fluctuations caused by changes in posture or physical activity.

New perspectives on mechanisms of sound generation in songbirds.

Abstract. The physical mechanisms of sound generation in the vocal organ, the syrinx, of songbirds have been investigated mostly with indirect methods. Recent direct endoscopic observation identified vibrations of the labia as the principal sound source. This model suggests sound generation in a pulse-tone mechanism similar to human phonation with the labia forming a pneumatic valve. The classical avian model proposed that vibrations of the thin medial tympaniform membranes are the primary sound generating mechanism. As a direct test of these two hypotheses we ablated the medial tympaniform membranes in two species (cardinal and zebra finch) and found that both were still able to phonate and sing without functional membranes. Small changes in song structure (harmonic emphasis, frequency control) occurred after medial tympaniform membrane ablation and suggest that the medial tympaniform membranes play a role in adjusting tension on the labia. Such a role is consistent with the fact that the medial tympaniform membranes are directly attached to the medial labia. There is no experimental support for a third hypothesis, proposing an aerodynamic model for generation of tonal sounds. Indirect tests (song in heliox atmosphere) as well as direct (labial vibration during tonal sound) measurements of syringeal vibrations support a vibration-based sound-generating mechanism even for tonal sounds.

Species-typical songs in white-crowned sparrows tutored with only phrase pairs

Modern theories of learned vocal behaviours, such as human speech and singing in songbirds, posit that acoustic communication signals are reproduced from memory, using auditory feedback. The nature of these memories, however, is unclear. Here we propose and test a model for how complex song structure can emerge from sparse sequence information acquired during tutoring. In this conceptual model, a population of combination-sensitive (phrase-pair) detectors is shaped by early exposure to song and serves as the minimal representation of the template necessary for generating complete song. As predicted by the model, birds that were tutored with only pairs of normally adjacent song phrases were able to assemble full songs in which phrases were placed in the correct order; birds that were tutored with reverse-ordered phrase pairs sang songs with reversed phrase order. Birds that were tutored with all song phrases, but presented singly, failed to produce normal, full songs. These findings provide the first evidence for a minimal requirement of sequence information in the acoustic model that can give rise to correct song structure.

Sexual Dimorphism of the Zebra Finch Syrinx Indicates Adaptation for High Fundamental Frequencies in Males

Background In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior. Methodology/Principal Findings Here we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency. Conclusions/Significance The syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.

Functional morphology of the sound-generating labia in the syrinx of two songbird species

In songbirds, two sound sources inside the syrinx are used to produce the primary sound. Laterally positioned labia are passively set into vibration, thus interrupting a passing air stream. Together with subsyringeal pressure, the size and tension of the labia determine the spectral characteristics of the primary sound. Very little is known about how the histological composition and morphology of the labia affect their function as sound generators. Here we related the size and microstructure of the labia to their acoustic function in two songbird species with different acoustic characteristics, the white‐crowned sparrow and zebra finch. Histological serial sections of the syrinx and different staining techniques were used to identify collagen, elastin and hyaluronan as extracellular matrix components. The distribution and orientation of elastic fibers indicated that the labia in white‐crowned sparrows are multi‐layered structures, whereas they are more uniformly structured in the zebra finch. Collagen and hyaluronan were evenly distributed in both species. A multi‐layered composition could give rise to complex viscoelastic properties of each sound source. We also measured labia size. Variability was found along the dorso‐ventral axis in both species. Lateral asymmetry was identified in some individuals but not consistently at the species level. Different size between the left and right sound sources could provide a morphological basis for the acoustic specialization of each sound generator, but only in some individuals. The inconsistency of its presence requires the investigation of alternative explanations, e.g. differences in viscoelastic properties of the labia of the left and right syrinx. Furthermore, we identified attachments of syringeal muscles to the labia as well as to bronchial half rings and suggest a mechanism for their biomechanical function.

Bilaterally symmetrical respiratory activity during lateralized birdsong

We investigated whether activity of expiratory muscles reflects lateralized activity of the vocal organ during production of birdsong. Respiration and syringeal motor activity were assessed in brown thrashers by monitoring bilateral airflow and subsyringeal air sac pressure, together with the electromyographic activity of expiratory abdominal muscles and vocal output. Activity of expiratory muscles was always present on both sides, regardless of whether song was produced bilaterally or on only one side of the syrinx. The average amplitude of expiratory EMG of one side does not change significantly, even if that side is silent during phonation. The temporal pattern of the electromyogram (EMG) was similar on both sides. Bilateral bursts of EMG activity on both sides accompanied changes in the rate of syringeal airflow, even when these flow fluctuations were generated only by one side of the syrinx. Motor commands to the respiratory muscles therefore appear to be bilaterally distributed, in contrast to the lateralized motor control of the syrinx.

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

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.