Preparing to sing: respiratory patterns underlying motor readiness for song.

Evidence for motor preparation and planning comes from neural activity preceding neural commands to activate the effectors; such preparatory activity is observed in pallial areas controlling learned motor behaviors. Vocal learning in songbirds is an example of a learned, sequential motor behavior that is a respiratory motor act and where there is evidence for neuromuscular planning. Respiration is the foundation of vocalization, elucidating the neural control of song motor planning requires studying respiratory antecedents of song initiation. Despite the importance of respiration in song production, few studies have investigated respiratory antecedents of impending vocalizations. Therefore, we investigated respiratory patterns in male zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) prior to, during, and following song bouts. In both species, compared with quiet respiration, song respiratory patterns were generated with higher amplitude, faster tempo, and ∼70% of the respiratory cycle is in the expiratory phase. In female-directed and isolation song, both species show a change in the respiratory tempo and the proportion of time spent inhaling prior to song. Following song, only zebra finches show systematic changes in respiratory patterns; they spend a greater proportion of the respiratory cycle in the expiratory phase for 1 s after song, which is likely due to hyperventilation during song. Accelerated respiratory rhythms before song may reflect the motor preparation for the upcoming song production; species differences in preparatory motor activity could be related to the degree to which motor planning is required; finally, song termination may be dictated by respiratory demands.NEW & NOTEWORTHY Motor planning for vocal production in birdsong manifests as an adaptation of respiratory characteristics prior to song. The songbird's respiratory system anticipates the upcoming song production by accelerating the respiratory tempo and increasing the proportion of time spent inhaling.

Multifunctional bilateral muscle control of vocal output in the songbird syrinx.

Songbirds produce complex vocalizations by coordinating neuromuscular control of syrinx, respiratory system, and upper vocal tract. The functional roles of syringeal muscles have been documented mainly with correlative data, which have suggested that synergistic activation plays a role in the fine control of vocal features. However, the specific involvement of individual muscles in achieving this fine control is still largely unknown. Here we investigate the contributions of the two main airflow controlling muscles, the dorsal and ventral tracheobronchial muscles in the zebra finch, through a new approach. Ablation of the muscle insertion on the cartilage framework reveals detailed insights into their respective roles in the fine control of song features. Unilateral ablation of a tracheobronchial muscle resulted in mostly subtle changes of the air sac pressure pattern and song features. Effects of ablation varied with the acoustic elements, thus indicating a context-dependent specific synergistic activation of muscles. High-frequency notes were most affected by the ablation, highlighting the importance of coordinated bilateral control. More pronounced effects on song features and air sac pressure were observed after bilateral ablation of the dorsal tracheobronchial muscles. The results illustrate that the gating muscles serve multiple functions in control of acoustic features and that each feature arises through context-dependent, synergistic activation patterns of syringeal muscles. Although many changes after the ablation are subtle, they fall within the perceptual range and thus may control behaviorally relevant features of sound. These data therefore provide important specific details about the underlying motor code for song production.NEW & NOTEWORTHY A new experimental approach was used to analyze the involvement of individual muscles in birdsong vocal control. Ablation of tracheobronchial muscles showed how these muscles contribute in manner specific to the acoustic structure of sound segments and how disruption of airflow regulation affects bilateral coordination. The results of this study illustrate that the gating muscles serve multiple functions in control of acoustic features and give further insight into the complex motor control of birdsong.

Minimum conditions for the induction of cortical spreading depression in brain slices.

Cortical spreading depression (CSD) occurs during various forms of brain injury such as stroke, subarachnoid hemorrhage, and brain trauma, but it is also thought to be the mechanism of the migraine aura. It is therefore expected to occur over a range of conditions including the awake behaving state. Yet it is unclear how such a massive depolarization could occur under relatively benign conditions. Using a microfluidic device with focal stimulation capability in a mouse brain slice model, we varied extracellular potassium concentration as well as the area exposed to increased extracellular potassium to determine the minimum conditions necessary to elicit CSD. Importantly, we focused on potassium levels that are physiologically plausible (≤145 mM; the intracellular potassium concentration). We found a strong correlation between the threshold concentration and the slice area exposed to increased extracellular potassium: minimum area of exposure was needed with the highest potassium concentration, while larger areas were needed at lower concentrations. We also found that moderate elevations of extracellular potassium were able to elicit CSD in relatively small estimated tissue volumes that might be activated under noninjury conditions. Our results thus show that CSD may be inducible under the conditions that expected in migraine aura as well as those related to brain trauma.

Interaction between telencephalic signals and respiratory dynamics in songbirds.

The mechanisms by which telencephalic areas affect motor activities are largely unknown. They could either take over motor control from downstream motor circuits or interact with the intrinsic dynamics of these circuits. Both models have been proposed for telencephalic control of respiration during learned vocal behavior in birds. The interactive model postulates that simple signals from the telencephalic song control areas are sufficient to drive the nonlinear respiratory network into producing complex temporal sequences. We tested this basic assumption by electrically stimulating telencephalic song control areas and analyzing the resulting respiratory patterns in zebra finches and in canaries. We found strong evidence for interaction between the rhythm of stimulation and the intrinsic respiratory rhythm, including naturally emerging subharmonic behavior and integration of lateralized telencephalic input. The evidence for clear interaction in our experimental paradigm suggests that telencephalic vocal control also uses a similar mechanism. Furthermore, species differences in the response of the respiratory system to stimulation show parallels to differences in the respiratory patterns of song, suggesting that the interactive production of respiratory rhythms is manifested in species-specific specialization of the involved circuitry.

Age-related changes in the Bengalese finch song motor program.

It is well established that there are remarkable similarities between song learning in oscine birds and acquisition of speech in young children. Human speech shows marked changes with senescence, but few studies have evaluated how song changes with advanced age in songbirds. To investigate the effect of old age on song, we compared song of old Bengalese finches (Lonchura striata domestica) with that of middle-aged birds. The main observed difference was a decrease in the song tempo, largely due to an increased intersyllable duration. Aging also affected the acoustic characteristics of the song, causing a decrease in pitch and in the range of frequency modulations. Gross morphological measurements of selected vocal muscles did not show detectable changes over this age range, suggesting that song deterioration may be due to neural deterioration. The age-induced temporal and acoustic changes in song parallel the acoustic changes that occur in human speech, suggesting songbirds as a suitable model for aging studies on learned vocal behavior.

Disrupting vagal feedback affects birdsong motor control.

Coordination of different motor systems for sound production involves the use of feedback mechanisms. Song production in oscines is a well-established animal model for studying learned vocal behavior. Whereas the online use of auditory feedback has been studied in the songbird model, very little is known about the role of other feedback mechanisms. Auditory feedback is required for the maintenance of stereotyped adult song. In addition, the use of somatosensory feedback to maintain pressure during song has been demonstrated with experimentally induced fluctuations in air sac pressure. Feedback information mediating this response is thought to be routed to the central nervous system via afferent fibers of the vagus nerve. Here, we tested the effects of unilateral vagotomy on the peripheral motor patterns of song production and the acoustic features. Unilateral vagotomy caused a variety of disruptions and alterations to the respiratory pattern of song, some of which affected the acoustic structure of vocalizations. These changes were most pronounced a few days after nerve resection and varied between individuals. In the most extreme cases, the motor gestures of respiration were so severely disrupted that individual song syllables or the song motif were atypically terminated. Acoustic changes also suggest altered use of the two sound generators and upper vocal tract filtering, indicating that the disruption of vagal feedback caused changes to the motor program of all motor systems involved in song production and modification. This evidence for the use of vagal feedback by the song system with disruption of song during the first days after nerve cut provides a contrast to the longer-term effects of auditory feedback disruption. It suggests a significant role for somatosensory feedback that differs from that of auditory feedback.

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.

Acquisition of an acoustic template leads to refinement of song motor gestures.

Vocal learning, a key behavior in human speech development, occurs only in a small number of animal taxa. Ontogeny of vocal behavior in humans and songbirds involves acquisition of an acoustic model, which guides the development of self-generated vocalizations (sensorimotor period). How vocal development proceeds in the absence of an acoustic model is largely unknown and cannot be studied directly in humans. Here we explored the effects of an acoustic model on song motor control by comparing peripheral motor gestures (respiration and syringeal muscles) of tutored birds with those of birds raised in acoustic isolation. Although the overall use of syringeal muscles during song was similar in both groups, tutored birds displayed enhanced temporal patterns of activation in respiratory and syringeal motor gestures. Muscle activation was more uniformly distributed throughout the song of tutored birds than that of untutored birds. Similarly, the respiratory effort was similar for both groups, but the expiratory pulses of song contained more modulations and temporal complexity in tutored birds. These results indicate that the acquisition of an acoustic template guides a refinement of experience-independent motor gestures by increasing temporal fine structure, but there is no difference in bilateral activation patterns for a given sound between the two groups. Nevertheless, these subtle temporal changes in muscle activation give rise to pronounced acoustic differences between the songs of the tutored and untutored birds. Experience with song during ontogeny therefore guides a more refined use of experience-independent motor programs.

Topologically inequivalent orbits induced by noise.

In this Letter we extend the concept of stochastic resonance. We show that in forced excitable systems noise can be responsible for the appearance of recurrences presenting a robust topological organization inequivalent to the periodic orbits of the deterministic system. As in stochastic resonance, these new structures are most pronounced at an optimal noise intensity.