Roderick A. Suthers

Airflow and pressure during canary song: direct evidence for mini-breaths

SummaryMale canaries (Serinus canaria) produce songs of long duration compared to the normal respiratory cycle. Each phrase in a song contains repetitions of a particular song syllable, with repetition rates for different syllables ranging from 3 to 35 notes/s. We measured tracheal airflow and air sac pressure in order to investigate respiratory dynamics during song.Song syllables (11–280 ms) are always accompanied by expiratory tracheal airflow. The silent intervals (15–90 ms) between successive syllables are accompanied by inspiration, except for a few phrases where airflow ceases instead of reversing. Thus, the mini-breath respiratory pattern is used most often by the five birds studied and pulsatile expiration is used only occasionally.Songs and phrases accompanied by minibreaths were of longer duration than those accompanied by pulsatile expiration, presumably because the animals finite vital capacity is not a limiting factor when the volume of air expired for one note is replaced by inspiration prior to the next. Pulsatile expiration was used for only a few syllable types from one bird that were produced at higher repetition rates than syllables accompanied by mini-breaths. We suggest that male canaries switch to pulsatile expiration only when the syllable repetition rate is too high (greater than about 30 Hz) for them to achieve mini-breaths.Changes in syringeal configuration that may accompany song are discussed, based on the assumption that changes in the ratio of subsyringeal (air sac) pressure to tracheal flow rate reflect changes in syringeal resistance.

PERIPHERAL CONTROL AND LATERALIZATION OF BIRDSONG

Recent studies on several species of oscine songbirds show that they achieve their varied vocal performances through coordinated activity of respiratory, syringeal, and other vocal tract muscles in ways that take maximum advantage of the acoustic flexibility made possible by the presence of two independently controlled sound sources in their bipartite syrinx (vocal organ). During song, special motor programs to respiratory muscles alter the pattern of ventilation to maintain the supply of respiratory air and oxygen to permit songs of long duration, high syllable repetition rates, or maximum spectral complexity. Each side of the syrinx receives its own motor program that, together with that sent to respiratory muscles, determines the acoustic properties of the ipsilaterally produced sound. The acoustic expression of these bilaterally distinct, phonetic motor patterns depends on the action of dorsal syringeal adductor muscles that, by opening or closing the ipsilateral side of the syrinx to airflow, determine the amount each side contributes to song. The syringeally generated sound is further modified by muscles that control the shape of the vocal tract. Different species have adopted different motor strategies that use the left and right sides of the syrinx in patterns of unilateral, bilateral, alternating, or sequential phonation to achieve the differing temporal and spectral characteristics of their songs. As a result, the degree of song lateralization probably varies between species to form a continuum from unilateral dominance to bilateral equality.

Producing Song: The Vocal Apparatus

Abstract: In order to achieve the goal of understanding the neurobiology of birdsong, it is necessary to understand the peripheral mechanisms by which song is produced. This paper reviews recent advances in the understanding of syringeal and respiratory motor control and how birds utilize these systems to create their species‐typical sounds. Songbirds have a relatively homogeneous duplex vocal organ in which sound is generated by oscillation of a pair of thickened labia on either side of the syrinx. Multiple pairs of syringeal muscles provide flexible, independent control of sound frequency and amplitude, and each side of the syrinx exhibits a degree of acoustic specialization. This is in contrast to many non‐songbirds, including vocal learners such as parrots, which have fewer syringeal muscles and use syringeal membranes to generate sound. In doves, at least, these membranes generate a harmonic signal in which the fundamental frequency is regulated by respiratory pressure in the air sac surrounding the syrinx and the overtones are filtered out by the vocal tract. The songs of adult songbirds are generally accompanied by precisely coordinated respiratory and syringeal motor patterns that, despite their relative stereotypy, are modulated in real time by somatosensory feedback. Comparative studies indicate songbirds have evolved species‐specific motor patterns that utilize the two sides of the syrinx in specific ways and enhance the particular acoustic effects characterizing the species song. A vocal mimic tutored with heterospecific song uses the same motor pattern as the tutor species when he accurately copies the song, suggesting that physical or physiological constraints on sound production have had a prominent role in the evolution of species‐specific motor patterns. An understanding of the relationship between the central processing and peripheral performance of song motor programs is essential for an understanding of the development, function, and evolution of these complex vocal signals.

Motor Correlates of Vocal Diversity in Songbirds

Oscine songbirds invest a substantial amount of time producing song, which has important roles in male-male competition and in attracting and stimulating a mate (Howard, 1920), as well as in species (Becker, 1982) and individual (Falls, 1982) recognition. Their diverse and often elaborate songs have placed them at the interface of neurobiology, behavior, and ecology as excellent subjects in which to study vocal communication. Toward this end, neurobiologists have made important advances in understanding the neural basis of vocal learning (e.g., Doupe, 1993; Arnold, 1992) and the central control of song production (e.g., Yu and Margoliash, 1996; Vu et al., 1994) and behavioral ecologists have gained new insights into the perceptual significance and communicative functions of song (e.g., Searcy and Yasukawa, 1996).

Old World frog and bird vocalizations contain prominent ultrasonic harmonics

Several groups of mammals such as bats, dolphins and whales are known to produce ultrasonic signals which are used for navigation and hunting by means of echolocation, as well as for communication. In contrast, frogs and birds produce sounds during night- and day-time hours that are audible to humans; their sounds are so pervasive that together with those of insects, they are considered the primary sounds of nature. Here we show that an Old World frog (Amolops tormotus) and an oscine songbird (Abroscopus albogularis) living near noisy streams reliably produce acoustic signals that contain prominent ultrasonic harmonics. Our findings provide the first evidence that anurans and passerines are capable of generating tonal ultrasonic call components and should stimulate the quest for additional ultrasonic species.

The sound emission pattern and the acoustical role of the noseleaf in the echolocating bat, Carollia perspicillata

Carollia perspicillata (Phyllostomidae) is a frugivorous bat that emits low-intensity, broadband, frequency-modulated echolocation pulses through nostrils surrounded by a noseleaf. The emission pattern of this bat is of interest because the ratio between the nostril spacing and the emitted wavelength varies during the pulse, causing complex interference patterns in the horizontal dimension. Sound pressures around the bat were measured using a movable microphone and were referenced to those at a stationary microphone positioned directly in front of the animal. Interference between the nostrils was confirmed by blocking one nostril, which eliminated sidelobes and minima in the emission pattern, and by comparison of real emission patterns with simple computer models. The positions of minima in the patterns indicate effective nostril spacings of over a half-wavelength. Displacement of the dorsal lancet of the noseleaf demonstrated that this structure directs sound in the vertical dimension.

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.

Pure-tone birdsong by resonance filtering of harmonic overtones

Pure-tone song is a common and widespread phenomenon in birds. The mechanistic origin of this type of phonation has been the subject of long-standing discussion. Currently, there are three hypotheses. (i) A vibrating valve in the avian vocal organ, the syrinx, generates a multifrequency harmonic source sound, which is filtered to a pure tone by a vocal tract filter (“source-filter” model, analogous to human speech production). (ii) Vocal tract resonances couple with a vibrating valve source, suppressing the normal production of harmonic overtones at this source (“soprano” model, analogous to human soprano singing). (iii) Pure-tone sound is produced as such by a sound-generating mechanism that is fundamentally different from a vibrating valve. Here we present direct evidence of a source-filter mechanism in the production of pure-tone birdsong. Using tracheal thermistors and air sac pressure cannulae, we recorded sound signals close to the syringeal sound source during spontaneous, pure-tone vocalizations of two species of turtledove. The results show that pure-tone dove vocalizations originate through filtering of a multifrequency harmonic sound source.

Vocal-Tract Filtering by Lingual Articulation in a Parrot

Human speech and bird vocalization are complex communicative behaviors with notable similarities in development and underlying mechanisms. However, there is an important difference between humans and birds in the way vocal complexity is generally produced. Human speech originates from independent modulatory actions of a sound source, e.g., the vibrating vocal folds, and an acoustic filter, formed by the resonances of the vocal tract (formants). Modulation in bird vocalization, in contrast, is thought to originate predominantly from the sound source, whereas the role of the resonance filter is only subsidiary in emphasizing the complex time-frequency patterns of the source (e.g., but see ). However, it has been suggested that, analogous to human speech production, tongue movements observed in parrot vocalizations modulate formant characteristics independently from the vocal source. As yet, direct evidence of such a causal relationship is lacking. In five Monk parakeets, Myiopsitta monachus, we replaced the vocal source, the syrinx, with a small speaker that generated a broad-band sound, and we measured the effects of tongue placement on the sound emitted from the beak. The results show that tongue movements cause significant frequency changes in two formants and cause amplitude changes in all four formants present between 0.5 and 10 kHz. We suggest that lingual articulation may thus in part explain the well-known ability of parrots to mimic human speech, and, even more intriguingly, may also underlie a speech-like formant system in natural parrot vocalizations.

Motor control of birdsong

One of the challenges when considering the motor control of birdsong is to understand how such a wide variety of temporally and spectrally diverse vocalizations are learned and produced. A better understanding of central neural processing, together with direct endoscopic observations and physiological studies of peripheral motor function during singing, has resulted in the formation of new theoretical models of song production. Recent work suggests that it may be more profitable to focus on the temporal relationship between control parameters than to attempt to directly correlate neural processing with details of the acoustic output.