Song-like activation of syringeal and respiratory muscles during sleep in canaries.

Sleep replay activity involves the reactivation of brain structures with patterns similar to those observed during waking behavior. In this study, we demonstrate that adult male canaries exhibit spontaneous, song-like peripheral reactivation during night sleep. Our findings include: (1) the presence of activity in respiratory muscles, leading to song-like air sac pressure patterns of low amplitude, (2) the simultaneous occurrence of respiratory replay events and reactivation of syringeal muscles, and (3) the reactivation of syringeal muscles without concurrent respiratory system activity. This song-like reactivation of peripheral motor systems enables the identification of specific motor patterns, with replay events preserving individual morphological and temporal properties. The activation of peripheral motor systems in songbirds and the differences in activation patterns between species give unique insights into the fictive behavioral output of activation of a complex learned motor behavior during sleep, shedding light on the neural control mechanisms and potential functions.

Replay of innate vocal patterns during night sleep in suboscines.

Activation of forebrain circuitry during sleep has been variably characterized as 'pre- or replay' and has been linked to memory consolidation. The evolutionary origins of this mechanism, however, are unknown. Sleep activation of the sensorimotor pathways of learned birdsong is a particularly useful model system because the muscles controlling the vocal organ are activated, revealing syringeal activity patterns for direct comparison with those of daytime vocal activity. Here, we show that suboscine birds, which develop their species-typical songs innately without the elaborate forebrain-thalamic circuitry of the vocal learning taxa, also engage in replay during sleep. In two tyrannid species, the characteristic syringeal activation patterns of the song could also be identified during sleep. Similar to song-learning oscines, the burst structure was more variable during sleep than daytime song production. In kiskadees (Pitangus sulphuratus), a second vocalization, which is part of a multi-modal display, was also replayed during sleep along with one component of the visual display. These data show unambiguously that variable 'replay' of stereotyped vocal motor programmes is not restricted to programmes confined within forebrain circuitry. The proposed effects on vocal motor programme maintenance are, therefore, building on a pre-existing neural mechanism that predates the evolution of learned vocal motor behaviour.

Birds breathe at an aerodynamic resonance.

We present a dynamical model for the avian respiratory system and report the measurement of its variables in normal breathing canaries (Serinus canaria). Fitting the parameters of the model, we are able to show that the birds in our study breathe at an aerodynamic resonance of their respiratory system. For different respiratory regimes, such as singing, where rapid respiratory gestures are used, the nonlinearities of the model lead to a shift in its resonances toward higher frequency values.

Unusual Avian Vocal Mechanism Facilitates Encoding of Body Size.

In this work we study the sound production mechanism of the raspy sounding song of the white-tipped plantcutter (Phytotoma rutila), a species with a most unusual vocalization. The biomechanics involved in the production of this song, and scaling arguments, allowed us to predict the precise way in which body size is encoded in its vocalizations. We tested this prediction through acoustic analysis of recorded songs, computational modeling of its unusual vocal strategy, and inspection of museum specimens captured across southeastern and south-central South America.

Dynamics behind rough sounds in the song of the Pitangus sulphuratus.

The complex vocalizations found in different bird species emerge from the interplay between morphological specializations and neuromuscular control mechanisms. In this work we study the dynamical mechanisms used by a nonlearner bird from the Americas, the suboscine Pitangus sulphuratus, in order to achieve a characteristic timbre of some of its vocalizations. By measuring syringeal muscle activity, air sac pressure, and sound as the bird sings, we are able to show that the birds of this species manage to lock the frequency difference between two sound sources. This provides a precise control of sound amplitude modulations, which gives rise to a distinct timbral property.

Gating related activity in a syringeal muscle allows the reconstruction of zebra finches songs.

Birdsong production involves the simultaneous and precise control of a set of muscles that change the configuration and dynamics of the vocal organ. Although it has been reported that each one of the different muscles is primarily involved in the control of one acoustic feature, recent advances have shown that they act synergistically to achieve the dynamical state necessary for phonation. In this work, we present a set of criteria that allow the extraction of gating-related information from the electromyographic activity of the syringealis ventralis muscle, a muscle that has been shown to be involved in frequency modulation. Using dynamical models of the muscle and syringeal dynamics, we obtain a full reconstruction of the zebra finch song using only the activity of this muscle.

From electromyographic activity to frequency modulation in zebra finch song.

Behavior emerges from the interaction between the nervous system and peripheral devices. In the case of birdsong production, a delicate and fast control of several muscles is required to control the configuration of the syrinx (the avian vocal organ) and the respiratory system. In particular, the syringealis ventralis muscle is involved in the control of the tension of the vibrating labia and thus affects the frequency modulation of the sound. Nevertheless, the translation of the instructions (which are electrical in nature) into acoustical features is complex and involves nonlinear, dynamical processes. In this work, we present a model of the dynamics of the syringealis ventralis muscle and the labia, which allows calculating the frequency of the generated sound, using as input the electrical activity recorded in the muscle. In addition, the model provides a framework to interpret inter-syllabic activity and hints at the importance of the biomechanical dynamics in determining behavior.

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

The evolution of complex behavior is driven by the interplay of morphological specializations and neuromuscular control mechanisms [1-3], and it is often difficult to tease apart their respective contributions. Avian vocal learning and associated neural adaptations are thought to have played a major role in bird diversification [4-8], whereas functional significance of substantial morphological diversity of the vocal organ remains largely unexplored. Within the most species-rich order, Passeriformes, "tracheophones" are a suboscine group that, unlike their oscine sister taxon, does not exhibit vocal learning [9] and is thought to phonate with tracheal membranes [10, 11] instead of the two independent sources found in other passerines [12-14]. Here we show tracheophones possess three sound sources, two oscine-like labial pairs and the unique tracheal membranes, which collectively represent the largest described number of sound sources for a vocal organ. Birds with experimentally disabled tracheal membranes were still able to phonate. Instead of the main sound source, the tracheal membranes constitute a morphological specialization, which, through interaction with bronchial labia, contributes to different acoustic features such as spectral complexity, amplitude modulation, and enhanced sound amplitude. In contrast, these same features arise in oscines from neuromuscular control of two labial sources [15-17]. These findings are supported by a modeling approach and provide a clear example for how a morphological adaptation of the tracheophone vocal organ can generate specific, complex sound features. Morphological specialization therefore constitutes an alternative path in the evolution of acoustic diversity to that of oscine vocal learning and complex neural control.

A circular model for song motor control in Serinus canaria.

Song production in songbirds is controlled by a network of nuclei distributed across several brain regions, which drives respiratory and vocal motor systems to generate sound. We built a model for birdsong production, whose variables are the average activities of different neural populations within these nuclei of the song system. We focus on the predictions of respiratory patterns of song, because these can be easily measured and therefore provide a validation for the model. We test the hypothesis that it is possible to construct a model in which (1) the activity of an expiratory related (ER) neural population fits the observed pressure patterns used by canaries during singing, and (2) a higher forebrain neural population, HVC, is sparsely active, simultaneously with significant motor instances of the pressure patterns. We show that in order to achieve these two requirements, the ER neural population needs to receive two inputs: a direct one, and its copy after being processed by other areas of the song system. The model is capable of reproducing the measured respiratory patterns and makes specific predictions on the timing of HVC activity during their production. These results suggest that vocal production is controlled by a circular network rather than by a simple top-down architecture.

Motor control of sound frequency in birdsong involves the interaction between air sac pressure and labial tension.

Frequency modulation is a salient acoustic feature of birdsong. Its control is usually attributed to the activity of syringeal muscles, which affect the tension of the labia responsible for sound production. We use experimental and theoretical tools to test the hypothesis that for birds producing tonal sounds such as domestic canaries (Serinus canaria), frequency modulation is determined by both the syringeal tension and the air sac pressure. For different models, we describe the structure of the isofrequency curves, which are sets of parameters leading to sounds presenting the same fundamental frequencies. We show how their shapes determine the relative roles of syringeal tension and air sac pressure in frequency modulation. Finally, we report experiments that allow us to unveil the features of the isofrequency curves.

Temperature induced syllable breaking unveils nonlinearly interacting timescales in birdsong motor pathway.

The nature of telencephalic control over premotor and motor circuits is debated. Hypotheses range from complete usurping of downstream circuitry to highly interactive mechanisms of control. We show theoretically and experimentally, that telencephalic song motor control in canaries is consistent with a highly interactive strategy. As predicted from a theoretical model of respiratory control, mild cooling of a forebrain nucleus (HVC) led to song stretching, but further cooling caused progressive restructuring of song, consistent with the hypothesis that respiratory gestures are subharmonic responses to a timescale present in the output of HVC. This interaction between a life-sustaining motor function (respiration) and telencephalic song motor control suggests a more general mechanism of how nonlinear integration of evolutionarily new brain structures into existing circuitry gives rise to diverse, new behavior.

Prosthetic avian vocal organ controlled by a freely behaving bird based on a low dimensional model of the biomechanical periphery.

Because of the parallels found with human language production and acquisition, birdsong is an ideal animal model to study general mechanisms underlying complex, learned motor behavior. The rich and diverse vocalizations of songbirds emerge as a result of the interaction between a pattern generator in the brain and a highly nontrivial nonlinear periphery. Much of the complexity of this vocal behavior has been understood by studying the physics of the avian vocal organ, particularly the syrinx. A mathematical model describing the complex periphery as a nonlinear dynamical system leads to the conclusion that nontrivial behavior emerges even when the organ is commanded by simple motor instructions: smooth paths in a low dimensional parameter space. An analysis of the model provides insight into which parameters are responsible for generating a rich variety of diverse vocalizations, and what the physiological meaning of these parameters is. By recording the physiological motor instructions elicited by a spontaneously singing muted bird and computing the model on a Digital Signal Processor in real-time, we produce realistic synthetic vocalizations that replace the bird's own auditory feedback. In this way, we build a bio-prosthetic avian vocal organ driven by a freely behaving bird via its physiologically coded motor commands. Since it is based on a low-dimensional nonlinear mathematical model of the peripheral effector, the emulation of the motor behavior requires light computation, in such a way that our bio-prosthetic device can be implemented on a portable platform.

Reconstruction of physiological instructions from Zebra finch song.

We reconstruct the physiological parameters that control an avian vocal organ during birdsong production using recorded song. The procedure involves fitting the time dependent parameters of an avian vocal organ model. Computationally, the model is implemented as a dynamical system ruling the behavior of the oscillating labia that modulate the air flow during sound production, together with the equations describing the dynamics of pressure fluctuations in the vocal tract. We tested our procedure for Zebra finch song with, simultaneously recorded physiological parameters: air sac pressure and the electromyographic activity of the left and right ventral syringeal muscles. A comparison of the reconstructed instructions with measured physiological parameters during song shows a high degree of correlation. Integrating the model with reconstructed parameters leads to the synthesis of highly realistic songs.

Hormonal acceleration of song development illuminates motor control mechanism in canaries.

In songbirds, the ontogeny of singing behavior shows strong parallels with human speech learning. As in humans, development of learned vocal behavior requires exposure to an acoustic model of species-typical vocalizations, and, subsequently, a sensorimotor practice period after which the vocalization is produced in a stereotyped manner. This requires mastering motor instructions driving the vocal organ and the respiratory system. Recently, it was shown that, in the case of canaries (Serinus canaria), the diverse syllables, constituting the song, are generated with air sac pressure patterns with characteristic shapes, remarkably, those belonging to a very specific mathematical family. Here, we treated juvenile canaries with testosterone at the onset of the sensorimotor practice period. This hormone exposure accelerated the development of song into stereotyped adultlike song. After 20 days of testosterone treatment, subsyringeal air sac pressure patterns of song resembled those produced by adults, while those of untreated control birds of the same age did not. Detailed temporal structure and modulation patterns emerged rapidly with testosterone treatment, and all previously identified categories of adult song were observed. This research shows that the known effect of testosterone on the neural circuits gives rise to the stereotyped categories of respiratory motor gestures. Extensive practice of these motor patterns during the sensorimotor phase is not required for their expression.

Physiologically driven avian vocal synthesizer.

In this work, we build an electronic syrinx, i.e., a programmable electronic device capable of integrating biomechanical model equations for the avian vocal organ in order to synthesize song. This vocal prosthesis is controlled by the bird's neural instructions to respiratory and the syringeal motor systems, thus opening great potential for studying motor control and its modification by sensory feedback mechanisms. Furthermore, a well-functioning subject-controlled vocal prosthesis can lay the foundation for similar devices in humans and thus provide directly health-related data and procedures.

Frequency modulation during song in a suboscine does not require vocal muscles.

The physiology of sound production in suboscines is poorly investigated. Suboscines are thought to develop song innately unlike the closely related oscines. Comparing phonatory mechanisms might therefore provide interesting insight into the evolution of vocal learning. Here we investigate sound production and control of sound frequency in the Great Kiskadee (Pitangus sulfuratus) by recording air sac pressure and vocalizations during spontaneously generated song. In all the songs and calls recorded, the modulations of the fundamental frequency are highly correlated to air sac pressure. To test whether this relationship reflects frequency control by changing respiratory activity or indicates synchronized vocal control, we denervated the syringeal muscles by bilateral resection of the tracheosyringeal nerve. After denervation, the strong correlation between fundamental frequency and air sac pressure patterns remained unchanged. A single linear regression relates sound frequency to air sac pressure in the intact and denervated birds. This surprising lack of control by syringeal muscles of frequency in Kiskadees, in strong contrast to songbirds, poses the question of how air sac pressure regulates sound frequency. To explore this question theoretically, we assume a nonlinear restitution force for the oscillating membrane folds in a two mass model of sound production. This nonlinear restitution force is essential to reproduce the frequency modulations of the observed vocalizations.

Nonlinear model predicts diverse respiratory patterns of birdsong.

A central aspect of the motor control of birdsong production is the capacity to generate diverse respiratory rhythms, which determine the coarse temporal pattern of song. The neural mechanisms that underlie this diversity of respiratory gestures and the resulting acoustic syllables are largely unknown. We show that the respiratory patterns of the highly complex and variable temporal organization of song in the canary (Serinus canaria) can be generated as solutions of a simple model describing the integration between song control and respiratory centers. This example suggests that subharmonic behavior can play an important role in providing a complex variety of responses with minimal neural substrate.