BACKGROUND: Most vocal learning species exhibit an early critical period during which their vocal control neural circuitry facilitates the acquisition of new vocalizations. Some taxa, most notably humans and parrots, retain some degree of neurobehavioral plasticity throughout adulthood, but both the extent of this plasticity and the neurogenetic mechanisms underlying it remain unclear. Differential expression of the transcription factor FoxP2 in both songbird and parrot vocal control nuclei has been identified previously as a key pattern facilitating vocal learning. We hypothesize that the resilience of vocal learning to cognitive decline in open-ended learners will be reflected in an absence of age-related changes in neural FoxP2 expression. We tested this hypothesis in the budgerigar (Melopsittacus undulatus), a small gregarious parrot in which adults converge on shared call types in response to shifts in group membership. We formed novel flocks of 4 previously unfamiliar males belonging to the same age class, either \"young adult\" (6 mo - 1 year) or \"older adult\" (≥ 3 year), and then collected audio-recordings over a 20-day learning period to assess vocal learning ability. Following behavioral recording, immunohistochemistry was performed on collected neural tissue to measure FoxP2 protein expression in a parrot vocal learning center, the magnocellular nucleus of the medial striatum (MMSt), and its adjacent striatum.
RESULTS: Although older adults show lower vocal diversity (i.e. repertoire size) and higher absolute levels of FoxP2 in the MMSt than young adults, we find similarly persistent downregulation of FoxP2 and equivalent vocal plasticity and vocal convergence in the two age cohorts. No relationship between individual variation in vocal learning measures and FoxP2 expression was detected.
CONCLUSIONS: We find neural evidence to support persistent vocal learning in the budgerigar, suggesting resilience to aging in the open-ended learning program of this species. The lack of a significant relationship between FoxP2 expression and individual variability in vocal learning performance suggests that other neurogenetic mechanisms could also regulate this complex behavior.

The basal ganglia have been implicated in auditory-dependent vocal learning and plasticity in human and songbirds, but the underlying neural phenotype remains to be clarified. Here, using confocal imaging and three-dimensional electron microscopy, we investigated striatal structural plasticity in response to hearing loss in Area X, the avian vocal basal ganglia, in adult male zebra finch (Taeniopygia guttata). We observed a rapid elongation of dendritic spines, by approximately 13%, by day 3 after deafening, and a considerable increase in spine synapse density, by approximately 61%, by day 14 after deafening, compared with the controls with an intact cochlea. These findings reveal structural sensitivity of Area X to auditory deprivation and suggest that this striatal plasticity might contribute to deafening-induced changes to learned vocal behavior.

Cortical-basal ganglia (CBG) circuits are critical for motor learning and performance, and are a major site of pathology. In songbirds, a CBG circuit regulates moment-by-moment variability in song and also enables song plasticity. Studies have shown that variable burst firing in LMAN, the output nucleus of this CBG circuit, actively drives acute song variability, but whether and how LMAN drives long-lasting changes in song remains unclear. Here, we ask whether chronic pharmacological augmentation of LMAN bursting is sufficient to drive plasticity in birds singing stereotyped songs. We show that altered LMAN activity drives cumulative changes in acoustic structure, timing, and sequencing over multiple days, and induces repetitions and silent pauses reminiscent of human stuttering. Changes persisted when LMAN was subsequently inactivated, indicating plasticity in song motor regions. Following cessation of pharmacological treatment, acoustic features and song sequence gradually recovered to their baseline values over a period of days to weeks. Together, our findings show that augmented bursting in CBG circuitry drives plasticity in well-learned motor skills, and may inform treatments for basal ganglia movement disorders.

Duetting, or the stereotypical, repeated and often coordinated vocalizations between 2 individuals arose independently multiple times in the Order Primates. Across primate species, there exists substantial variation in terms of timing, degree of overlap, and sex-specificity of duet contributions. There is increasing evidence that primates can modify the timing of their duet contributions relative to their partner, and this vocal flexibility may have been an important precursor to the evolution of human language. Here, we present the results of a fine-scale analysis of Gursky\'s spectral tarsier Tarsius spectrumgurskyae duet phrases recorded in North Sulawesi, Indonesia. Specifically, we aimed to investigate individual-level variation in the female and male contributions to the duet, quantify individual- and pair-level differences in duet timing, and measure temporal precision of duetting individuals relative to their partner. We were able to classify female duet phrases to the correct individual with an 80% accuracy using support vector machines, whereas our classification accuracy for males was lower at 64%. Females were more variable than males in terms of timing between notes. All tarsier phrases exhibited some degree of overlap between callers, and tarsiers exhibited high temporal precision in their note output relative to their partners. We provide evidence that duetting tarsier individuals can modify their note output relative to their duetting partner, and these results support the idea that flexibility in vocal exchanges-a precursor to human language-evolved early in the primate lineage and long before the emergence of modern humans.

Humans exhibit a high level of vocal plasticity in speech production, which allows us to acquire both native and foreign languages and dialects, and adapt to local accents in social communication. In comparison, non-human primates exhibit limited vocal plasticity, especially in adulthood, which would limit their ability to adapt to different social and environmental contexts in vocal communication. Here, we quantitatively examined the ability of adult common marmosets ( Callithrix jacchus), a highly vocal New World primate species, to modulate their vocal production in social contexts. While recent studies have demonstrated vocal learning in developing marmosets, we know much less about the extent of vocal learning and plasticity in adult marmosets. We found, in the present study, that marmosets were able to adaptively modify the spectrotemporal structure of their vocalizations when they encountered interfering sounds. Our experiments showed that marmosets shifted the spectrum of their vocalizations away from the spectrum of the interfering sounds in order to avoid the overlap. More interestingly, we found that marmosets made predictive and long-lasting spectral shifts in their vocalizations after they had experienced a particular type of interfering sound. These observations provided evidence for directional control of the vocalization spectrum and long-term vocal plasticity by adult marmosets. The findings reported here have important implications for the ability of this New World primate species in voluntarily and adaptively controlling their vocal production in social communication.

Natural background noises are common in the acoustic environments in which most organisms have evolved. Therefore, the vocalization and sound perception systems of vocal animals are inherently equipped to overcome natural background noise. Human-generated noises, however, pose new challenges that can hamper audiovocal communication. The mechanisms animals use to cope with anthropogenic noise disturbances have been extensively explored in a variety of taxa. Bats emit echolocation pulses primarily to orient, locate and navigate, while social calls are used to communicate with conspecifics. Previous studies have shown that bats alter echolocation pulse parameters in response to background noise interference. In contrast to high-frequency echolocation pulses, relatively low-frequency components within bat social calls overlap broadly with ambient noise frequencies. However, how bats structure their social calls in the presence of anthropogenic noise is not known. Here, we hypothesized that bats leverage vocal plasticity to facilitate vocal exchanges within a noisy environment. To test this hypothesis, we subjected the Asian particolored bat, Vespertilio sinensis, to prerecorded traffic noise. We observed a significant decrease in vocal complexity (i.e., an increased frequency of monosyllabic calls) in response to traffic noise. However, an increase in the duration and frequency of social calls, as have been observed in other species, was not evident. This suggests that signal simplification may increase communication efficacy in noisy environments. Moreover, V. sinensis also increased call amplitude in response to increased traffic noise, consistent with the predictions of the Lombard effect.

The study of non-human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non-human primates. An increasing body of research, however, suggests that various species of non-human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non-human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception-production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non-human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre-adaptations that may have paved the way for language evolution.

The neural basis of how learned vocalizations change during development and in adulthood represents a major challenge facing cognitive neuroscience. This plasticity in the degree to which learned vocalizations can change in both humans and songbirds is linked to the actions of sex steroid hormones during ontogeny but also in adulthood in the context of seasonal changes in birdsong. We investigated the role of steroid hormone signaling in the brain on distinct features of birdsong using adult male canaries (Serinus canaria), which show extensive seasonal vocal plasticity as adults. Specifically, we bilaterally implanted the potent androgen receptor antagonist flutamide in two key brain regions that control birdsong. We show that androgen signaling in the motor cortical-like brain region, the robust nucleus of the arcopallium (RA), controls syllable and trill bandwidth stereotypy, while not significantly affecting higher order features of song such syllable-type usage (i.e., how many times each syllable type is used) or syllable sequences. In contrast, androgen signaling in the premotor cortical-like brain region, HVC (proper name), controls song variability by increasing the variability of syllable-type usage and syllable sequences, while having no effect on syllable or trill bandwidth stereotypy. Other aspects of song, such as the duration of trills and the number of syllables per song, were also differentially affected by androgen signaling in HVC versus RA. These results implicate androgens in regulating distinct features of complex motor output in a precise and nonredundant manner.SIGNIFICANCE STATEMENT Vocal plasticity is linked to the actions of sex steroid hormones, but the precise mechanisms are unclear. We investigated this question in adult male canaries (Serinus canaria), which show extensive vocal plasticity throughout their life. We show that androgens in two cortex-like vocal control brain regions regulate distinct aspects of vocal plasticity. For example, in HVC (proper name), androgens regulate variability in syntax but not phonology, whereas androgens in the robust nucleus of the arcopallium (RA) regulate variability in phonology but not syntax. Temporal aspects of song were also differentially affected by androgen signaling in HVC versus RA. Thus, androgen signaling may reduce vocal plasticity by acting in a nonredundant and precise manner in the brain.

It has been observed in many songbird species that populations in noisy urban areas sing with a higher minimum frequency than do matched populations in quieter, less developed areas. However, why and how this divergence occurs is not yet understood. We experimentally tested whether chronic noise exposure during vocal learning results in songs with higher minimum frequencies in great tits (Parus major), the first species for which a correlation between anthropogenic noise and song frequency was observed. We also tested vocal plasticity of adult great tits in response to changing background noise levels by measuring song frequency and amplitude as we changed noise conditions. We show that noise exposure during ontogeny did not result in songs with higher minimum frequencies. In addition, we found that adult birds did not make any frequency or song usage adjustments when their background noise conditions were changed after song crystallization. These results challenge the common view of vocal adjustments by city birds, as they suggest that either noise itself is not the causal force driving the divergence of song frequency between urban and forest populations, or that noise induces population-wide changes over a time scale of several generations rather than causing changes in individual behaviour.

Deafening elicits a deterioration of learned vocalization, in both humans and songbirds. In songbirds, learned vocal plasticity has been shown to depend on the basal ganglia-cortical circuit, but the underlying cellular basis remains to be clarified. Using confocal imaging and electron microscopy, we examined the effect of deafening on dendritic spines in avian vocal motor cortex, the robust nucleus of the arcopallium (RA), and investigated the role of the basal ganglia circuit in motor cortex plasticity. We found rapid structural changes to RA dendritic spines in response to hearing loss, accompanied by learned song degradation. In particular, the morphological characters of RA spine synaptic contacts between 2 major pathways were altered differently. However, experimental disruption of the basal ganglia circuit, through lesions in song-specialized basal ganglia nucleus Area X, largely prevented both the observed changes to RA dendritic spines and the song deterioration after hearing loss. Our results provide cellular evidence to highlight a key role of the basal ganglia circuit in the motor cortical plasticity that underlies learned vocal plasticity.