Vocal Babbling Research Articles

Early corticosterone increases vocal complexity in a wild parrot: An organizational role of the hypothalamic-pituitary-adrenal axis in vocal learning?

The neuroendocrinology of vocal learning is exceptionally well known in passerine songbirds. Despite huge life history, genetic and ecological variation across passerines, song learning tends to occur as a result of rises in gonadal and non-gonadal sex steroids that shape telencephalic vocal control circuits and song. Parrots are closely related but independently evolved different cerebral circuits for vocal repertoire acquisition in both sexes that serve a broader suite of social functions and do not appear to be shaped by early androgens or estrogens; instead, parrots begin a plastic phase in vocal development at an earlier life history stage that favors the growth, maturation, and survival functions of corticosteroids. As evidence, corticosterone (CORT) supplements given to wild green-rumped parrotlets (Forpus passerinus) during the first week of vocal babbling resulted in larger vocal repertoires in both sexes in the remaining days before fledging. Here, we replicate this experiment but began treatment 1 week before in development, analyzing both experiments in one model and a stronger test of the organizational effects of CORT on repertoire acquisition. Early CORT treatment resulted in significantly larger repertoires compared to late treatment. Both treatment groups showed weak negative effects on the early, reduplicated stage of babbling and strong, positive effects of CORT on the later, variegated stage. Results are consistent with more formative effects of corticosteroids at earlier developmental stages and a role of the hypothalamic-pituitary-adrenal axis (HPA) in vocal repertoire acquisition. Given the early emergence of speech in human ontogeny, parrots are a promising model for understanding the putative role of the HPA axis in the construction of neural circuits that support language acquisition.

A predisposed motor bias shapes individuality in vocal learning.

The development of individuality during learned behavior is a common trait observed across animal species; however, the underlying biological mechanisms remain understood. Similar to human speech, songbirds develop individually unique songs with species-specific traits through vocal learning. In this study, we investigate the developmental and molecular mechanisms underlying individuality in vocal learning by utilizing F1 hybrid songbirds (Taeniopygia guttata cross with Taeniopygia bichenovii), taking an integrating approach combining experimentally controlled systematic song tutoring, unbiased discriminant analysis of song features, and single-cell transcriptomics. When tutoring with songs from both parental species, F1 hybrid individuals exhibit evident diversity in their acquired songs. Approximately 30% of F1 hybrids selectively learn either song of the two parental species, while others develop merged songs that combine traits from both species. Vocal acoustic biases during vocal babbling initially appear as individual differences in songs among F1 juveniles and are maintained through the sensitive period of song vocal learning. These vocal acoustic biases emerge independently of the initial auditory experience of hearing the biological father's and passive tutored songs. We identify individual differences in transcriptional signatures in a subset of cell types, including the glutamatergic neurons projecting from the cortical vocal output nucleus to the hypoglossal nuclei, which are associated with variations of vocal acoustic features. These findings suggest that a genetically predisposed vocal motor bias serves as the initial origin of individual variation in vocal learning, influencing learning constraints and preferences.

Vocal babbling in a wild parrot shows life history and endocrine affinities with human infants.

Prelinguistic babbling is a critical phase in infant language development and is best understood in temperate songbirds where it occurs primarily in males at reproductive maturity and is modulated by sex steroids. Parrots of both sexes are icons of tropical vocal plasticity, but vocal babbling is unreported in this group and whether the endocrine system is involved is unknown. Here we show that vocal babbling is widespread in a wild parrot population in Venezuela, ensues in both sexes during the nestling stage, occurs amidst a captive audience of mixed-aged siblings, and is modulated by corticosteroids. Spectrographic analysis and machine learning found phoneme diversity and combinatorial capacity increased precipitously for the first week, thereafter, crystalizing into a smaller repertoire, consistent with the selective attrition model of language development. Corticosterone-treated nestlings differed from unmanipulated birds and sham controls in several acoustic properties and crystallized a larger repertoire post-treatment. Our findings indicate babbling occurs during an early life-history stage in which corticosteroids help catalyse the transition from a universal learning programme to one finely tuned for the prevailing ecological environment, a potentially convergent scenario in human prelinguistic development.

Vocal learning in songbirds requires cholinergic signaling in a motor cortex-like nucleus.

Cholinergic inputs to cortex modulate plasticity and sensory processing, yet little is known about their role in motor control. Here, we show that cholinergic signaling in a songbird vocal motor cortical area, the robust nucleus of the arcopallium (RA), is required for song learning. Reverse microdialysis of nicotinic and muscarinic receptor antagonists into RA in juvenile birds did not significantly affect syllable timing or acoustic structure during vocal babbling. However, chronic blockade over weeks reduced singing quantity and impaired learning, resulting in an impoverished song with excess variability, abnormal acoustic features, and reduced similarity to tutor song. The demonstration that cholinergic signaling in a motor cortical area is required for song learning motivates the songbird as a tractable model system to identify roles of the basal forebrain cholinergic system in motor control. NEW & NOTEWORTHY Cholinergic inputs to cortex are evolutionarily conserved and implicated in sensory processing and synaptic plasticity. However, functions of cholinergic signals in motor areas are understudied and poorly understood. Here, we show that cholinergic signaling in a songbird vocal motor cortical area is not required for normal vocal variability during babbling but is essential for developmental song learning. Cholinergic modulation of motor cortex is thus required for learning but not for the ability to sing.

Emergent Jaw Predominance in Vocal Development Through Stochastic Optimization

Infant vocal babbling strongly relies on jaw oscillations, especially at the stage of canonical babbling, which underlies the syllabic structure of world languages. In this paper, we propose, model and analyze an hypothesis to explain this predominance of the jaw in early babbling. This hypothesis states that general stochastic optimization principles, when applied to learning sensorimotor control, automatically generate ordered babbling stages with a predominant exploration of jaw movements in early stages. The reason is that those movements impact the auditory effects more than other articulators. In previous computational models, such general principles were shown to selectively freeze and free degrees of freedom in a model reproducing the proximo-distal development observed in infant arm reaching. The contribution of this paper is to show how, using the same methods, we are able to explain such patterns in vocal development. We present three experiments. The two first ones show that the recruitment order of articulators emerging from stochastic optimization depends on the target sound to be achieved but that on average the jaw is largely chosen as the first recruited articulator. The third experiment analyses in more detail how the emerging recruitment order is shaped by the dynamics of the optimization process.

Statistical learning in songbirds: from self-tutoring to song culture.

At the onset of vocal development, both songbirds and humans produce variable vocal babbling with broadly distributed acoustic features. Over development, these vocalizations differentiate into the well-defined, categorical signals that characterize adult vocal behaviour. A broadly distributed signal is ideal for vocal exploration, that is, for matching vocal production to the statistics of the sensory input. The developmental transition to categorical signals is a gradual process during which the vocal output becomes differentiated and stable. But does it require categorical input? We trained juvenile zebra finches with playbacks of their own developing song, produced just a few moments earlier, updated continuously over development. Although the vocalizations of these self-tutored (ST) birds were initially broadly distributed, birds quickly developed categorical signals, as fast as birds that were trained with a categorical, adult song template. By contrast, siblings of those birds that received no training (isolates) developed phonological categories much more slowly and never reached the same level of category differentiation as their ST brothers. Therefore, instead of simply mirroring the statistical properties of their sensory input, songbirds actively transform it into distinct categories. We suggest that the early self-generation of phonological categories facilitates the establishment of vocal culture by making the song easier to transmit at the micro level, while promoting stability of shared vocabulary at the group level over generations.This article is part of the themed issue ‘New frontiers for statistical learning in the cognitive sciences’.

Familial bias and auditory feedback regulation of vocal babbling patterns during early song development.

Learned vocalizations are a crucial acoustic biosignal conveying individual traits in many species. Songbirds learn song patterns by listening to a tutor song and performing vocal practice during a sensitive developmental period. However, when and how individual differences in song patterns develop remain unknown. Here, we report that individual differences in vocal output exist even at the earliest song development stage, called subsong. Experiments involving the manipulation of both breeding pairs and song tutoring conditions revealed that the parental pair combination contributes to generating familial differences in syllable duration and variability in the subsong of offspring. Furthermore, after deafening, juveniles immediately changed their subsong by shortening the syllable durations but maintained the individual variability of their subsong temporal patterns, suggesting both auditory-sensitive modification and independent intrinsic regulation of vocal output. These results indicate that the temporal patterns of subsong are not merely disordered vocalization but are regulated by familial bias with sensitivity to auditory feedback, thus generating individual variability at the initiation of vocal development.

Origins of basal ganglia output signals in singing juvenile birds.

Across species, complex circuits inside the basal ganglia (BG) converge on pallidal output neurons that exhibit movement-locked firing patterns. Yet the origins of these firing patterns remain poorly understood. In songbirds during vocal babbling, BG output neurons homologous to those found in the primate internal pallidal segment are uniformly activated in the tens of milliseconds prior to syllable onsets. To test the origins of this remarkably homogenous BG output signal, we recorded from diverse upstream BG cell types during babbling. Prior to syllable onsets, at the same time that internal pallidal segment-like neurons were activated, putative medium spiny neurons, fast spiking and tonically active interneurons also exhibited transient rate increases. In contrast, pallidal neurons homologous to those found in primate external pallidal segment exhibited transient rate decreases. To test origins of these signals, we performed recordings following lesion of corticostriatal inputs from premotor nucleus HVC. HVC lesions largely abolished these syllable-locked signals. Altogether, these findings indicate a striking homogeneity of syllable timing signals in the songbird BG during babbling and are consistent with a role for the indirect and hyperdirect pathways in transforming cortical inputs into BG outputs during an exploratory behavior.

Emergence of Context-Dependent Variability across a Basal Ganglia Network

Context dependence is a key feature of cortical-basal ganglia circuit activity, and in songbirds the cortical outflow of a basal ganglia circuit specialized for song, LMAN, shows striking increases in trial-by-trial variability and bursting when birds sing alone rather than to females. To reveal where this variability and its social regulation emerge, we recorded stepwise from corticostriatal (HVC) neurons and their target spiny and pallidal neurons in Area X. We find that corticostriatal and spiny neurons both show precise singing-related firing across both social settings. Pallidal neurons, in contrast, exhibit markedly increased trial-by-trial variation when birds sing alone, created by highly variable pauses in firing. This variability persists even when recurrent inputs from LMAN are ablated. These data indicate that variability and its context sensitivity emerge within the basal ganglia network, suggest a network mechanism for this emergence, and highlight variability generation and regulation as basal ganglia functions.

Vocal Exploration Is Locally Regulated during Song Learning

Exploratory variability is essential for sensorimotor learning, but it is not known how and at what timescales it is regulated. We manipulated song learning in zebra finches to experimentally control the requirements for vocal exploration in different parts of their song. We first trained birds to perform a one-syllable song, and once they mastered it, we added a new syllable to the song model. Remarkably, when practicing the modified song, birds rapidly alternated between high and low acoustic variability to confine vocal exploration to the newly added syllable. Furthermore, even within syllables, acoustic variability changed independently across song elements that were only milliseconds apart. Analysis of the entire vocal output during learning revealed that the variability of each song element decreased as it approached the target, correlating with momentary local distance from the target and less so with the overall distance within a syllable. We conclude that vocal error is computed locally in subsyllabic timescales and that song elements can be learned and crystallized independently. Songbirds have dedicated brain circuitry for vocal babbling in the anterior forebrain pathway (AFP), which generates exploratory song patterns that drive premotor neurons at the song nucleus RA. We hypothesize that either AFP adjusts the gain of vocal exploration in fine timescales or that the sensitivity of RA premotor neurons to AFP/HVC inputs varies across song elements.

Vocal babbling in songbirds requires the basal ganglia-recipient motor thalamus but not the basal ganglia

Young songbirds produce vocal "babbling," and the variability of their songs is thought to underlie a process of trial-and-error vocal learning. It is known that this exploratory variability requires the "cortical" component of a basal ganglia (BG) thalamocortical loop, but less understood is the role of the BG and thalamic components in this behavior. We found that large bilateral lesions to the songbird BG homolog Area X had little or no effect on song variability during vocal babbling. In contrast, lesions to the BG-recipient thalamic nucleus DLM (medial portion of the dorsolateral thalamus) largely abolished normal vocal babbling in young birds and caused a dramatic increase in song stereotypy. These findings support the idea that the motor thalamus plays a key role in the expression of exploratory juvenile behaviors during learning.

A Specialized Forebrain Circuit for Vocal Babbling in the Juvenile Songbird

Young animals engage in variable exploratory behaviors essential for the development of neural circuitry and adult motor control, yet the neural basis of these behaviors is largely unknown. Juvenile songbirds produce subsong-a succession of primitive vocalizations akin to human babbling. We found that subsong production in zebra finches does not require HVC (high vocal center), a key premotor area for singing in adult birds, but does require LMAN (lateral magnocellular nucleus of the nidopallium), a forebrain nucleus involved in learning but not in adult singing. During babbling, neurons in LMAN exhibited premotor correlations to vocal output on a fast time scale. Thus, juvenile singing is driven by a circuit distinct from that which produces the adult behavior-a separation possibly general to other developing motor systems.

Characteristics of the rhythmic organization of vocal babbling: Implications for an amodal linguistic rhythm

Vocal babbling involves production of rhythmic sequences of a mouth close–open alternation giving the perceptual impression of a sequence of consonant–vowel syllables. Petitto and co-workers have argued vocal babbling rhythm is the same as manual syllabic babbling rhythm, in that it has a frequency of 1 cycle per second. They also assert that adult speech and sign language display the same frequency. However, available evidence suggests that the vocal babbling frequency approximates 3 cycles per second. Both adult spoken language and sign language show higher frequencies than babbling in their respective modalities. No information is currently available on the basic rhythmic parameter of intercyclical variability in either modality. A study of reduplicative babbling by 4 infants and 4 adults producing reduplicated syllables confirms the 3 per second vocal babbling rate, as well as a faster rate in adults, and provides new information on intercyclical variability.

How do deaf infants attain first signs?

In this study the development and alternation of nonreferential gestures were examined longitudinally in terms of the acquisition of Japanese sign language. Parent–child free‐play sessions in their home were videotaped at every monthly visit. Hand activities produced by two deaf infants of deaf parents are described and analyzed. Nonreferential gestures were observed frequently just before the occurrences of the first signs. They consisted of many rhythmic and repetitious movements. Nonreferential gestures became more complex and the number of them also increased as infants grew up. The comparison of nonreferential gestures and first signs revealed the continuity between them in terms of movements. In conclusion, nonreferential gestures are equivalent to a manual analog of vocal babbling.

Silent mandibular oscillations in vocal babbling.

Early babbling has been characterized as being fundamentally a mandibular oscillation: the infant's repeated lowering and raising of its mandible yields a perceived contrast between consonants produced in a closed vocal tract configuration and vowels produced with an open tract. We wondered whether babblers produce rhythmic mandibular oscillations without phonation and, if so, whether there might be a relationship between such 'jaw wags' and early speech. We report two studies: the first is a longitudinal, observational study of 14 infants, some of whom were hearing and some Deaf. Seven infants (3 hearing, 3 Deaf, and 1 hearing-impaired) produced numerous speech-like, rhythmic jaw wags without phonation; sometimes jaw wags formed a single utterance with phonated babbling. Most jaw wags reported here were produced when these infants were ages 8-13 months. The second study, a survey of 90 parents of 4- to 10-month-old hearing infants, suggests that silent babbles may be a widespread phenomenon of early speech development.

Babbling in the Manual Mode: Evidence for the Ontogeny of Language

Infant vocal babbling has been assumed to be a speech-based phenomenon that reflects the maturation of the articulatory apparatus responsible for spoken language production. Manual babbling has now been reported to occur in deaf children exposed to signed languages from birth. The similarities between manual and vocal babbling suggest that babbling is a product of an amodal, brain-based language capacity under maturational control, in which phonetic and syllabic units are produced by the infant as a first step toward building a mature linguistic system. Contrary to prevailing accounts of the neurological basis of babbling in language ontogeny, the speech modality is not critical in babbling. Rather, babbling is tied to the abstract linguistic structure of language and to an expressive capacity capable of processing different types of signals (signed or spoken).