Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia-forebrain circuit.

The plasticity of nervous systems allows animals to quickly adapt to a changing environment. In particular, seasonal plasticity of brain structure and behavior is often critical to survival or mating in seasonal climates. Songbirds provide striking examples of seasonal changes in neural circuits and vocal behavior and have emerged as a leading model for adult brain plasticity. While seasonal plasticity and the well-characterized process of juvenile song learning may share common neural mechanisms, the extent of their similarity remains unclear. Especially, it is unknown whether the basal ganglia (BG)-forebrain loop which implements song learning in juveniles by driving vocal exploration participates in seasonal plasticity. To address this issue, we performed bilateral lesions of the output structure of the song-related BG-forebrain circuit (the magnocellular nucleus of the anterior nidopallium) in canaries during the breeding season, when song is most stereotyped, and just after resuming singing in early fall, when canaries sing their most variable songs and may produce new syllable types. Lesions drastically reduced song acoustic variability, increased song and phrase duration, and decreased syntax variability in early fall, reverting at least partially seasonal changes observed between the breeding season and early fall. On the contrary, lesions did not affect singing behavior during the breeding season. Our results therefore indicate that the BG-forebrain pathway introduces acoustic and syntactic variability in song when canaries resume singing in early fall. We propose that BG-forebrain circuits actively participate in seasonal plasticity by injecting variability in behavior during non-breeding season. SIGNIFICANCE STATEMENT: The study of seasonal plasticity in temperate songbirds has provided important insights into the mechanisms of structural and functional plasticity in the central nervous system. The precise function and mechanisms of seasonal song plasticity however remain poorly understood. We show here that a basal ganglia-forebrain circuit involved in the acquisition and maintenance of birdsong is actively inducing song variability outside the breeding season, when singing is most variable, while having little effect on the stereotyped singing during the breeding season. Our results suggest that seasonal plasticity reflects an active song-maintenance process akin to juvenile learning, and that basal ganglia-forebrain circuits can drive plasticity in a learned vocal behavior during the non-injury-induced degeneration and reconstruction of the neural circuit underlying its production.

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.

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

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.

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.

Low-dimensional dynamical model for the diversity of pressure patterns used in canary song.

During song production, oscine birds produce large air sac pressure pulses. During those pulses, energy is transferred to labia located at the juncture between the bronchii and the trachea, inducing the high frequency labial oscillations which are responsible for airflow modulations, i.e., the uttered sound. In order to generate diverse syllables, canaries (Serinus canaria) use a set of air sac pressure patterns with characteristic shapes. In this work we show that these different shapes can be approximated by the subharmonic solutions of a forced normal form. This simple model is built from identifying dynamical elements which allow to reproduce the shape of the pressure pattern corresponding to one syllable type. Remarkably, integrating that simple model for other parameters allows to recover the other pressure patterns used during song. Interpreting the diversity of these physiological gestures as subharmonic solutions of a simple nonlinear system allows us to account simultaneously for their morphological features as well as for the syllabic timing and suggests a strategy for the generation of complex motor patterns.