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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.
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Vocal behavior plays a crucial evolutionary role. In the case of birds, song is critically important in courtship, male-male competition and other key behaviors linked to reproduction. However, under natural conditions, a variety of avian species live in close proximity and share an 'acoustic landscape'. Therefore, they need to be able to differentiate their calls or songs from those of other species and also from those of other individuals of the same species. To do this efficiently, birds display a remarkable diversity of sounds. For example, in the case of vocal learners, such as oscine passerines (i.e. songbirds), complex sequences and subtle acoustic effects are produced through the generation of complex neuromuscular instructions driving the vocal organ, which is remarkably conserved across approximately 4000 oscine species. By contrast, the majority of the sister clade of oscines, the suboscine passerines, are thought not to be vocal learners. Despite this, different suboscine species can generate a rich variety of songs and quite subtle acoustic effects. In the last few years, different suboscine species have been shown to possess morphological adaptations that allow them to produce a diversity of acoustic characteristics. Here, we briefly review the mechanisms of sound production in birds, before considering three suboscine species in more detail. The examples discussed in this Review, integrating biological experiments and biomechanical modeling using non-linear dynamical systems, illustrate how a morphological adaptation can produce complex acoustic properties without the need for complex neuromuscular control.
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Aves Canoras , Som , Masculino , Animais , Aclimatação , Acústica , Evolução Biológica , CorteRESUMO
Resumen Igual que es posible trazar una historia de los cantos de las aves, de su recepción por y su relación con los seres humanos, también se puede especular sobre si esos cantos pueden funcionar como historia, viva, sonora, en qué grado y modos, así como en qué diferiría esa historia aviar de la humana o si podría enriquecerla. Muchas aves, después de todo, transmiten y aprenden sus cantos unas de otras, construyen sobre ellos y los complican, recogiendo otros sonidos que asumen e incorporan, sonidos humanos incluidos. Crean así paisajes sonoros que no siempre quedan de fondo: en ocasiones, reclaman su relevancia y toman el primer plano, en la historia y como historia.
Abstract Just as it is possible to trace a history of the songs of birds, of their reception by human beings, and of how humans relate to them, it is also possible to speculate on whether these songs can function as history, a living, resounding history, to which degree and in which ways. As well as on how that avian story would differ from the human one, or if it could enrich it. Many birds, after all, learn their songs from each other, they build on and complicate them, picking up other sounds they incorporate, human sounds included. Thus, they create soundscapes that are not always in the background: sometimes, they claim their relevance and take the foreground, in history and as history.
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Vocalização Animal , Aves , Interação Humano-Animal , História do Século XXI , Pandemias , COVID-19RESUMO
Birdsong is a complex vocal behavior, which emerges out of the interaction between a nervous system and a highly nonlinear vocal device, the syrinx. In this work we discuss how low dimensional dynamical systems, interpretable in terms of the biomechanics involved, are capable of synthesizing realistic songs. We review the experimental and conceptual steps that lead to the formulation of low dimensional dynamical systems for the song system and describe the tests that quantify their success. In particular, we show how to evaluate computational models by comparing the responses of highly selective neurons to the bird's own song and to synthetic copies generated mathematically. Beyond testing the hypothesis behind the model's construction, these low dimensional models allow designing precise stimuli in order to explore the sensorimotor integration of acoustic signals.
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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.
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Aves Canoras , Vocalização Animal , Animais , Aprendizagem , Prosencéfalo , SonoRESUMO
Many bird species adjust their songs to noisy urban conditions by which they reduce masking and counteract the detrimental impact on signal efficiency. Different species vary in their response to level fluctuations of ambient noise, but it remains unclear why they vary. Here, we investigated whether noise-dependent flexibility may relate to singing style and signal function of the flexible acoustic trait. Species with highly variable songs may generally be more flexible and strongly repetitive singers may be more limited to stray from their stringent patterns. We exposed males of four passerine species with contrasting singing styles (repertoire size, immediate or eventual variety singing and syllable diversity) to three experimental sound conditions: 1) continuous urban noise; 2) intermittent white noise and 3) conspecific song playback. We found no spectral or temporal changes in response to experimental noise exposure in any of the four species, but significant temporal adjustment to conspecific playback in one of them. We argue that the consistency in song frequency and timing may have signal value, independent of singing style, and therefore be an explanation for the general lack of noise-dependent flexibility in the four species of the current study.
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Aves/fisiologia , Ruído , Som , Vocalização Animal/fisiologia , Acústica , Animais , Meio Ambiente , MéxicoRESUMO
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.
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Tentilhões/fisiologia , Modelos Biológicos , Músculo Esquelético/fisiologia , Vocalização Animal/fisiologia , Acústica , Animais , Fenômenos Biomecânicos , Eletromiografia , Tentilhões/anatomia & histologia , Músculo Esquelético/anatomia & histologia , Dinâmica não Linear , Espectrografia do SomRESUMO
Songbirds are a well-established animal model to study the neural basis of learning, perception and production of complex vocalizations. In this system, telencephalic neurons in HVC present a state-dependent, highly selective response to auditory presentations of the bird's own song (BOS). This property provides an opportunity to study the neural code behind a complex motor behavior. In this work, we explore whether changes in the temporal structure of the sound envelope can drive changes in the neural responses of highly selective HVC units. We generated an envelope-modified BOS (MOD) by reversing each syllable's envelope but leaving the overall temporal structure of syllable spectra unchanged, which resulted in a subtle modification for each song syllable. We conducted in vivo electrophysiological recordings of HVC neurons in anaesthetized zebra finches (Taeniopygia guttata). Units analyzed presented a high BOS selectivity and lower response to MOD, but preserved the profile response shape. These results show that the temporal evolution of the sound envelope is being sensed by the avian song system and suggest that the biomechanical properties of the vocal apparatus could play a role in enhancing subtle sound differences.
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Percepção Auditiva/fisiologia , Encéfalo/fisiologia , Tentilhões/fisiologia , Neurônios/fisiologia , Vocalização Animal , Estimulação Acústica , Potenciais de Ação , Anestesia , Animais , Masculino , Microeletrodos , Espectrografia do SomRESUMO
Birdsong emerges when a set of highly interconnected brain areas manage to generate a complex output. This consists of precise respiratory rhythms as well as motor instructions to control the vocal organ configuration. In this way, during birdsong production, dedicated cortical areas interact with life-supporting ones in the brainstem, such as the respiratory nuclei. We discuss an integrative view of this interaction together with a widely accepted "top-down" representation of the song system. We also show that a description of this neural network in terms of dynamical systems allows to explore songbird production and processing by generating testable predictions.
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Vocal communication is an unique example, where the nonlinear nature of the periphery can give rise to complex sounds even when driven by simple neural instructions. In this work we studied the case of two close-related bird species, Patagioenas maculosa and Patagioenas picazuro, whose vocalizations differ only in the timbre. The temporal modulation of the fundamental frequency is similar in both cases, differing only in the existence of sidebands around the fundamental frequency in the P. maculosa. We tested the hypothesis that the qualitative difference between these vocalizations lies in the nonlinear nature of the syrinx. In particular, we propose that the roughness of maculosa's vocalizations is due to an asymmetry between the right and left vibratory membranes, whose nonlinear dynamics generate the sound. To test the hypothesis, we generated a biomechanical model for vocal production with an asymmetric parameter Q with which we can control the level of asymmetry between these membranes. Using this model we generated synthetic vocalizations with the principal acoustic features of both species. In addition, we confirmed the anatomical predictions by making post mortem inspection of the syrinxes, showing that the species with tonal song (picazuro) has a more symmetrical pair of membranes compared to maculosa.
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Columbidae , Modelos Teóricos , Vocalização Animal , Animais , Fenômenos Biomecânicos , Columbidae/anatomia & histologia , Columbidae/fisiologia , Simulação por Computador , Masculino , Dinâmica não Linear , Espectrografia do Som , Especificidade da Espécie , VibraçãoRESUMO
Central neurons express a variety of neuronal types and ion channels that promote firing heterogeneity among their distinct neuronal populations. Action potential (AP) phasic firing, produced by low-threshold voltage-activated potassium currents (VAKCs), is commonly observed in mammalian brainstem neurons involved in the processing of temporal properties of the acoustic information. The avian caudomedial nidopallium (NCM) is an auditory area analogous to portions of the mammalian auditory cortex that is involved in the perceptual discrimination and memorization of birdsong and shows complex responses to auditory stimuli We performed in vitro whole-cell patch-clamp recordings in brain slices from adult zebra finches (Taeniopygia guttata) and observed that half of NCM neurons fire APs phasically in response to membrane depolarizations, while the rest fire transiently or tonically. Phasic neurons fired APs faster and with more temporal precision than tonic and transient neurons. These neurons had similar membrane resting potentials, but phasic neurons had lower membrane input resistance and time constant. Surprisingly phasic neurons did not express low-threshold VAKCs, which curtailed firing in phasic mammalian brainstem neurons, having similar VAKCs to other NCM neurons. The phasic firing was determined not by VAKCs, but by the potassium background leak conductances, which was more prominently expressed in phasic neurons, a result corroborated by pharmacological, dynamic-clamp, and modeling experiments. These results reveal a new role for leak currents in generating firing diversity in central neurons.
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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.