Expiratory muscle activity during song production in the canary

doi:10.1016/0034-5687(90)90044-Y

Respiration Physiology

Volume 81, Issue 2, August 1990, Pages 177-187

Respiration Physiolo...

https://doi.org/10.1016/0034-5687(90)90044-Y Get rights and content

Abstract

Elaborate respiratory patterns accompany song production in male canaries (Serinus canaria). To learn how such patterns arise, electromyographic activity was measured in the expiratory muscles in the abdomen. Most song phrases are accompanied either by mini-breaths (when syllable repetition rats are 2 to 27/sec) or by pulsatile expiration (when syllable repetition rate are 30 to 38/sec). In both cases there is a one-to-one correspondence between bursts of expiratory muscle electrical activity and song syllables. Phrases with syllable repetition rates of 62–70/sec, which are rare, are accompanied by expiratory airflow that may either pulsatile or continuous. The expiratory muscles are active throughout such phrases, suggesting that the muscles of the vocal organ, the syrinx, are responsible for producing separate notes. Thus, at rates up to 38/sec, the abdominal muscles of canaries briefly for the production of each song syllable.

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A major advantage of this respiratory mode is the fact that air expired during production of the trill element can be replenished during the minibreath, thus facilitating phrase (repetition of a specific trill element) duration. The second respiratory mechanism to generate trills involves a sustained expiratory pulse, whose pressure is modulated (‘pulsatile trill’) by phasic modulation of the activity of the expiratory muscles (e.g. Goller & Suthers, 1999; Hartley, 1990). Trill elements are generated at the peaks of this pressure modulation, and silent periods correspond to the troughs.
Birdsong is an important signal used in intra- and intersexual communication in a reproductive context. Strong sexual and natural selective forces act on this behaviour, such that singing individuals can be viewed as vocal athletes whose performance is critical for reproductive success. In this review, I argue and illustrate how a solid understanding of song production mechanisms can enhance our investigations of performance. From a production perspective, temporal and spectral features of song are relatively well understood and therefore are discussed in detail. Performance ranges of temporal and frequency characteristics can be broad, but often involve different production mechanisms, with different constraints and trade-offs underlying their generation. Based on these multifaceted features, I argue that song may be perceived as an ‘acoustic gestalt’, which for each syllable represents a specific location in a complex multidimensional parameter space characterized by differential contributions of individual features. Derived from this view, I also propose that individual males may be showing specialization for exceptional performance of some, but not all, features of song. To illustrate this possibility for a future research focus, I quantify some song features of seven male European robins, and, although the data set is limited, it shows that different individuals exhibit different performance levels across a number of song features.
Female Songbirds: The unsung drivers of courtship behavior and its neural substrates
2019, Behavioural Processes
Citation Excerpt :
Like mammals, birds have a caudal medullary nucleus (called nucleus retroambigualis, or RAm) whose neurons discharge rhythmically in phase with expiration and whose spinal projections target motoneurons innervating muscles involved in expiration (Wild 1993a,b; Wild 1994; Wild et al., 2009). Because almost all vocalizations are produced during expiration, and the expiratory muscles are instrumental to the compression of the air sacs that produces the expiratory air flow correlated with syllabic production (Hartley, 1990), it follows that RAm likely plays a key role in song and call production, in addition to its vital role in respiration – although recordings from RAm during singing or calling are not yet available. Similarities of respiratory-vocal control in birds and mammals extend beyond RAm, particularly in the midbrain, where birds have an area, known as DM (dorsomedial nucleus of the intercollicular complex), that is considered equivalent to the lateral or ventrolateral parts of the periaqueductal gray (PAG) of mammals (Kingsbury et al., 2012; Wild et al., 1997).
Songbirds hold a prominent role in the fields of neurobiology, evolution, and social behavior. Many of these fields have assumed that females lacked the ability to produce song and have therefore treated song as a male-specific behavior. Consequently, much of our understanding regarding the evolution and neural control of song behavior has been driven by these assumptions. Here we review literature from diverse fields to provide a broader perspective of the role of females in vocal communication and courtship. Recent evidence indicates that song evolved in both males and females and instances of female song are still common. The specialized neural circuit known as the “song system,” which is necessary for singing in males, is also present in females, including those that do not sing, implying broader functions that include evaluating male song and controlling courtship behavior. In addition to having flexible, individualized preferences, females actively shape their social network through their interactions with males, females, and juveniles. We suggest that by developing more accurate hypotheses concerning the role of females we may better understand the evolution and neural mechanisms of song production and courtship behavior.
Attractive males are less than adequate dads in a multimodal signalling passerine
2015, Animal Behaviour
Citation Excerpt :
Blue-black grassquits produce a trill-like song with a buzzy subunit (Fandiño-Mariño & Vielliard, 2004). Buzz subunits are emitted faster than trilled songs and seem to be vocalized only during expiratory bursts, contrasting with the rapid inspiration and expiration pattern of trill units in trilled songs (Hartley, 1990; Podos, 1997). Recent studies suggest that buzz rates can be constrained by trade-offs as usually occurs with trilled songs (Weiss, Kiefer, & Kipper, 2012), which leads to the possibility of buzz songs signalling male quality and influencing mating success (Trillo & Vehrencamp, 2005; Weiss et al., 2012).
Parental attractiveness influences paternal and maternal efforts in a wide range of animals that exhibit biparental care. However, we still lack an understanding concerning the direction of the covariance between attractiveness and parental effort, perhaps because studies typically consider only one or a subset of multiple attractiveness signals. In this study we investigated predictions of four hypotheses about the relationship between attractiveness traits (plumage coloration, song and leap display traits) and parental effort (feeding rates) in a wild population of the blue-black grassquit, Volatinia jacarina, a Neotropical sexually dichromatic bird with biparental care. Paternal effort was negatively correlated with male blue-black coloration (UV chroma) and maternal effort was positively correlated with male provisioning rate. Thus, more attractive males relative to the UV chroma are worse fathers relative to less attractive males in this trait. However, female provisioning rate was positively correlated with another male attractive trait: the blue-black plumage coverage. The song, leap display and other features of male coloration were not associated with either male or female parental effort. Taken together, these results support the parental–mating trade-off hypothesis for paternal behaviour, which predicts that attractive males should invest less in current offspring in order to acquire extrapair matings. Also, our results partially support the positive differential allocation hypothesis: although females invested highly in offspring of males with more blue-black plumage coverage, they did not compensate for the low investment of males with UV-shifted blue-black plumage. We highlight the need for future studies to consider multiple sexual traits in order to investigate the relationship between attractiveness and parental investment.
The respiratory-vocal system of songbirds: Anatomy, physiology, and neural control
2014, Progress in Brain Research
Citation Excerpt :
This is especially apparent in songbirds such as the zebra finch whose song is highly stereotyped (Franz and Goller, 2002), where the precise pattern of air sac pressure modulation can be observed even when syringeal resistance is controlled for by pinning the lateral labia, suggesting that such modulation arises in large part from modulation of the expiratory drive by the respiratory system (Goller and Cooper, 2004, 2008; Fig. 2). Between song syllables or phrases, songbirds usually take a minibreath of about 30 ms duration, effected by inspiratory muscles (Hartley, 1990; Wild et al., 1998). The volume of air inspired in these minibreaths is sufficient to replace the air lost during the preceding syllable, thereby preventing the bird from running out of air during the song (Hartley and Suthers, 1989).
This wide-ranging review presents an overview of the respiratory-vocal system in songbirds, which are the only other vertebrate group known to display a degree of respiratory control during song rivalling that of humans during speech; this despite the fact that the peripheral components of both the respiratory and vocal systems differ substantially in the two groups. We first provide a brief description of these peripheral components in songbirds (lungs, air sacs and respiratory muscles, vocal organ (syrinx), upper vocal tract) and then proceed to a review of the organization of central respiratory-related neurons in the spinal cord and brainstem, the latter having an organization fundamentally similar to that of the ventral respiratory group of mammals. The second half of the review describes the nature of the motor commands generated in a specialized “cortical” song control circuit and how these might engage brainstem respiratory networks to shape the temporal structure of song. We also discuss a bilaterally projecting “respiratory-thalamic” pathway that links the respiratory system to “cortical” song control nuclei. This necessary pathway for song originates in the brainstem's primary inspiratory center and is hypothesized to play a vital role in synchronizing song motor commands both within and across hemispheres.
A species-specific view of song representation in a sensorimotor nucleus
2013, Journal of Physiology Paris
Citation Excerpt :
Two different strategies contribute to the prolonged production of various syllable types within the song (Fig. 4). One consists of replacing the air expelled during the silent intersyllable interval (Hartley and Suthers, 1989; Hartley, 1990). This alternation of expiratory and inspiratory pressure pulses (mini-breath) allows the bird to sing many seconds of uninterrupted song and can give rise to phrases with syllable repetition rates up to 30 per second (constrained by muscle size).
Songbirds constitute a powerful model system for the investigation of how complex vocal communication sounds are represented and generated, offering a neural system in which the brain areas involved in auditory, motor and auditory–motor integration are well known. One brain area of considerable interest is the nucleus HVC. Neurons in the HVC respond vigorously to the presentation of the bird’s own song and display song-related motor activity. In the present paper, we present a synthesis of neurophysiological studies performed in the HVC of one songbird species, the canary (Serinus canaria). These studies, by taking advantage of the singing behavior and song characteristics of the canary, have examined the neuronal representation of the bird’s own song in the HVC. They suggest that breeding cues influence the degree of auditory selectivity of HVC neurons for the bird’s own song over its time-reversed version, without affecting the contribution of spike timing to the information carried by these two song stimuli. Also, while HVC neurons are collectively more responsive to forward playback of the bird’s own song than to its temporally or spectrally modified versions, some are more broadly tuned, with an auditory responsiveness that extends beyond the bird’s own song. Lastly, because the HVC is also involved in song production, we discuss the peripheral control of song production, and suggest that interspecific variations in song production mechanisms could be exploited to improve our understanding of the functional role of the HVC in respiratory–vocal coordination.
Peripheral mechanisms for vocal production in birds - differences and similarities to human speech and singing
2010, Brain and Language
Song production in songbirds is a model system for studying learned vocal behavior. As in humans, bird phonation involves three main motor systems (respiration, vocal organ and vocal tract). The avian respiratory mechanism uses pressure regulation in air sacs to ventilate a rigid lung. In songbirds sound is generated with two independently controlled sound sources, which reside in a uniquely avian vocal organ, the syrinx. However, the physical sound generation mechanism in the syrinx shows strong analogies to that in the human larynx, such that both can be characterized as myoelastic-aerodynamic sound sources. Similarities include active adduction and abduction, oscillating tissue masses which modulate flow rate through the organ and a layered structure of the oscillating tissue masses giving rise to complex viscoelastic properties. Differences in the functional morphology of the sound producing system between birds and humans require specific motor control patterns. The songbird vocal apparatus is adapted for high speed, suggesting that temporal patterns and fast modulation of sound features are important in acoustic communication. Rapid respiratory patterns determine the coarse temporal structure of song and maintain gas exchange even during very long songs. The respiratory system also contributes to the fine control of airflow. Muscular control of the vocal organ regulates airflow and acoustic features. The upper vocal tract of birds filters the sounds generated in the syrinx, and filter properties are actively adjusted. Nonlinear source-filter interactions may also play a role. The unique morphology and biomechanical system for sound production in birds presents an interesting model for exploring parallels in control mechanisms that give rise to highly convergent physical patterns of sound generation. More comparative work should provide a rich source for our understanding of the evolution of complex sound producing systems.

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Respiration Physiology

Abstract

References (24)

Respiration during song in the canary (Serinuscanaria)

Comp. Biochem. Physiol.

Electromyographic studies of the effects of bodily position and anesthesia on the activity of the respiratory muscles of the domestic cock

Poultry Sci.

Electromyographic studies on the respiratory muscles of the chicken

Poultry Sci.

Respiratory gating of activity in the avian vocal control system

Brain Res.

Muscles alive

Lung-air-sac anatomy and respiratory pressures in the bird

J. Exp. Biol.

Respiratory mechanics of sound production in chickens and geese

J. Exp. Biol.

Ventilation of the lung-air sac system

Functions of the syrinx and the control of sound production

Motor unit recruitment pattern and toxic activity in respiratory muscles of Gallus domesticus

J. Neurophysiol.

Respiratory muscles

Pressure and air flow during distress calls of the starling, Sturnus vulgaris (Aves; Passeriformes)

J. Exp. Zool.

Cited by (70)

Vocal athletics – from birdsong production mechanisms to sexy songs

Female Songbirds: The unsung drivers of courtship behavior and its neural substrates

Attractive males are less than adequate dads in a multimodal signalling passerine

The respiratory-vocal system of songbirds: Anatomy, physiology, and neural control

A species-specific view of song representation in a sensorimotor nucleus

Peripheral mechanisms for vocal production in birds - differences and similarities to human speech and singing