Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain

Songbirds and humans share the ability to adaptively modify their vocalizations based on sensory feedback. Prior studies have focused primarily on the role that auditory feedback plays in shaping vocal output throughout life. In contrast, it is unclear whether and how non-auditory information drives vocal plasticity. Here, we first used a reinforcement learning paradigm to establish that non-auditory feedback can drive vocal learning in adult songbirds. We then assessed the role of a songbird basal ganglia-thalamocortical pathway critical to auditory vocal learning in this novel form of vocal plasticity. We found that both this circuit and its dopaminergic inputs are necessary for non-auditory vocal learning, demonstrating that this pathway is not specialized exclusively for auditory-driven vocal learning. The ability of this circuit to use both auditory and non-auditory information to guide vocal learning may reflect a general principle for the neural systems that support vocal plasticity across species.

Vocal plasticity in harbour seal pups

Vocal plasticity can occur in response to environmental and biological factors, including conspecifics' vocalizations and noise. Pinnipeds are one of the few mammalian groups capable of vocal learning, and are therefore relevant to understanding the evolution of vocal plasticity in humans and other animals. Here, we investigate the vocal plasticity of harbour seals ( Phoca vitulina ), a species with vocal learning abilities observed in adulthood but not puppyhood. To evaluate early mammalian vocal development, we tested 1–3 weeks-old seal pups. We tailored noise playbacks to this species and age to induce seal pups to shift their fundamental frequency ( f 0 ), rather than adapt call amplitude or temporal characteristics. We exposed individual pups to low- and high-intensity bandpass-filtered noise, which spanned—and masked—their typical range of f 0 ; simultaneously, we recorded pups' spontaneous calls. Unlike most mammals, pups modified their vocalizations by lowering their f 0 in response to increased noise. This modulation was precise and adapted to the particular experimental manipulation of the noise condition. In addition, higher levels of noise induced less dispersion around the mean f 0 , suggesting that pups may have actively focused their phonatory efforts to target lower frequencies. Noise did not seem to affect call amplitude. However, one seal showed two characteristics of the Lombard effect known for human speech in noise: significant increase in call amplitude and flattening of spectral tilt. Our relatively low noise levels may have favoured f 0 modulation while inhibiting amplitude adjustments. This lowering of f 0 is unusual, as most animals commonly display no such f 0 shift. Our data represent a relatively rare case in mammalian neonates, and have implications for the evolution of vocal plasticity and vocal learning across species, including humans. This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part I)’.

Seasonal regulation of singing-driven gene expression associated with song plasticity in the canary, an open-ended vocal learner

Songbirds are one of the few animal taxa that possess vocal learning abilities. Different species of songbirds exhibit species-specific learning programs during song acquisition. Songbirds with open-ended vocal learning capacity, such as the canary, modify their songs during adulthood. Nevertheless, the neural molecular mechanisms underlying open-ended vocal learning are not fully understood. We investigated the singing-driven expression of neural activity-dependent genes (Arc, Egr1, c-fos, Nr4a1, Sik1, Dusp6, and Gadd45β) in the canary to examine a potential relationship between the gene expression level and the degree of seasonal vocal plasticity at different ages. The expression of these genes was differently regulated throughout the critical period of vocal learning in the zebra finch, a closed-ended song learner. In the canary, the neural activity-dependent genes were induced by singing in the song nuclei throughout the year. However, in the vocal motor nucleus, the robust nucleus of the arcopallium (RA), all genes were regulated with a higher induction rate by singing in the fall than in the spring. The singing-driven expression of these genes showed a similar induction rate in the fall between the first year juvenile and the second year adult canaries, suggesting a seasonal, not age-dependent, regulation of the neural activity-dependent genes. By measuring seasonal vocal plasticity and singing-driven gene expression, we found that in RA, the induction intensity of the neural activity-dependent genes was correlated with the state of vocal plasticity. These results demonstrate a correlation between vocal plasticity and the singing-driven expression of neural activity-dependent genes in RA through song development, regardless of whether a songbird species possesses an open- or closed-ended vocal learning capacity.

Operant control and call usage learning in African elephants

Elephants exhibit remarkable vocal plasticity, and case studies reveal that individuals of African savannah ( Loxodonta africana ) and Asian ( Elephas maximus ) elephants are capable of vocal production learning. Surprisingly, however, little is known about contextual learning (usage and comprehension learning) in elephant communication. Usage learning can be demonstrated by training animals to vocalize in an arbitrary (cue-triggered) context. Here we show that adult African savannah elephants ( n = 13) can vocalize in response to verbal cues, reliably producing social call types such as the low-frequency rumble, trumpets and snorts as well as atypical sounds using various mechanisms, thus displaying compound vocal control. We further show that rumbles emitted upon trainer cues differ significantly in structure from rumbles triggered by social contexts of the same individuals ( n = 6). Every form of social learning increases the complexity of a communication system. In elephants, we only poorly understand their vocal learning abilities and the underlying cognitive mechanisms. Among other research, this calls for controlled learning experiments in which the prerequisite is operant/volitional control of vocalizations. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Vocal repertoire and group-specific signature in the Smooth-billed Ani, Crotophaga ani Linnaeus, 1758 (Cuculiformes, Aves)

Vocal plasticity reflects the ability of animals to vary vocalizations according to context (vocal repertoire) as well as to develop vocal convergence (vocal group signature) in the interaction of members in social groups. This feature has been largely reported for oscine, psittacine and trochilid birds, but little has been investigated in birds that present innate vocalization. The smooth-billed ani (Crotophaga ani) is a social bird that lives in groups between two and twenty individuals, and which presents innate vocalization. Here we analyzed the vocal repertoire of this species during group activities, and further investigated the existence of a vocal group signature. The study was conducted in the Southeast of Brazil between May 2017 and April 2018. Two groups of smooth-billed anis were followed, Guararema and Charqueada groups, and their vocalizations were recorded and contextualized as to the performed behavior. The vocal repertoire was analyzed for its composition, context and acoustic variables. The acoustic parameters maximum peak frequency, maximum fundamental frequency, minimum frequency, maximum frequency and duration were analyzed. To verify the vocal signature of the group, we tested whether there was variation in the acoustic parameters between the monitored groups. We recorded ten vocalizations that constituted the vocal repertoire of the Smooth-billed Ani, five of which (“Ahnee”, “Whine”, “Pre-flight”, “Flight” and “Vigil”) were issued by the two groups and five exclusive to the Charqueada group. There were significant differences in the acoustic parameters for “Flight” and “Vigil” vocalizations between the groups, suggesting vocal group signature for these sounds. We established that the Smooth-billed Ani has a diverse vocal repertoire, with variations also occurring between groups of the same population. Moreover, we found evidence of vocal group signature in vocalizations used in the context of cohesion, defense and territory maintenance.

A novel theory of Asian elephant high-frequency squeak production

Background Anatomical and cognitive adaptations to overcome morpho-mechanical limitations of laryngeal sound production, where body size and the related vocal apparatus dimensions determine the fundamental frequency, increase vocal diversity across taxa. Elephants flexibly use laryngeal and trunk-based vocalizations to form a repertoire ranging from infrasonic rumbles to higher-pitched trumpets. Moreover, they are among the few evolutionarily distantly related animals (humans, pinnipeds, cetaceans, birds) capable of imitating species-atypical sounds. Yet, their vocal plasticity has so far not been related to functions within their natural communicative system, in part because not all call types have been systematically studied. Here, we reveal how Asian elephants (Elephas maximus) produce species-specific squeaks (F0 300–2300 Hz) by using acoustic camera recordings to visualize sound emission and examining this alongside acoustic, behavioral, and morphological data across seven captive groups. Results We found that squeaks were emitted through the closed mouth in synchrony with cheek depression and retraction of the labial angles. The simultaneous emission of squeaks with nasal snorts (biphonation) in one individual confirmed that squeak production was independent of nasal passage involvement and this implicated oral sound production. The squeaks’ spectral structure is incongruent with laryngeal sound production and aerodynamic whistles, pointing to tissue vibration as the sound source. Anatomical considerations suggest that the longitudinal closed lips function as the vibrators. Acoustic and temporal parameters exhibit high intra- and inter-individual variability that enables individual but no call-subtype classification. Only 19 of 56 study subjects were recorded to squeak, mostly during alarming contexts and social arousal but some also on command. Conclusion Our results strongly suggest that Asian elephants force air from the small oral cavity through the tensed lips, inducing self-sustained lip vibration. Besides human brass players, lip buzzing is not described elsewhere in the animal kingdom. Given the complexity of the proposed mechanism, the surprising absence of squeaking in most of the unrelated subjects and the indication for volitional control, we hypothesize that squeak production involves social learning. Our study offers new insights into how vocal and cognitive flexibility enables mammals to overcome size-related limitations of laryngeal sound production. This flexibility enables Asian elephants to exploit a frequency range spanning seven octaves within their communicative system.

Vocal plasticity in harbour seal pups

ABSTRACTVocal plasticity can occur in response to environmental and biological factors, including conspecifics’ vocalisations and noise. Pinnipeds are one of the few mammalian groups capable of vocal learning, and are therefore relevant to understanding the evolution of vocal plasticity in humans and other animals. Here, we investigate the vocal plasticity of harbour seals (Phoca vitulina), a species with vocal learning abilities attested in adulthood but not puppyhood. To zoom into early mammalian vocal development, we tested 1-3 weeks old seal pups. We tailored noise playbacks to this species and age to induce seal pups to shift their fundamental frequency (F0), rather than adapt call amplitude or temporal characteristics. We exposed individual pups to bandpass-filtered noise, which purposely spanned – and masked – their typical range of F0s, and simultaneously recorded pups’ spontaneous calls. Seals were able to modify their vocalisations quite unlike most mammals: They lowered their F0 in response to increased noise. This modulation was punctual and adapted to the particular noise condition. In addition, higher noise induced less dispersion around the mean F0, suggesting that pups may have been actively focusing their phonatory efforts to target lower frequencies. Noise masking did not seem to affect call amplitude. However, one seal showed two characteristics of the Lombard effect known for human speech in noise: significant increase in call amplitude and flattening of spectral tilt. Our relatively low noise levels may have favoured F0 shifts while inhibiting amplitude adjustments. This lowering of F0 is quite unusual, as other animals commonly display no F0 shift independently of noise amplitude. Our data represents a relatively rare case in mammalian neonates, and may have implications for the evolution of vocal plasticity across species, including humans.

Biophony in a noisy tropical urban forest fragment

Anthropogenic noise, which is part of an urban soundscape, can negatively affect the behaviour of wild animals. Here we investigated how biophony (animal sounds) was affected by noise in an urban Brazilian forest fragment. Our hypothesis was that noise and biophony would differ between the border and the centre of the forest fragment (i.e., lower biophony predicted in noisy areas). Two passive acoustic monitoring devices were used to record soundscapes one week per month, 24 hour per day, from May to July 2012. The Acoustic Complexity Index (ACI) was used to quantify biophony and the Power Spectral Density (PSD) to quantify urban noise. PSD and ACI were higher on the border than in the centre of the fragment. PSD was lower in July, while the ACI did not significantly vary between months. Noise levels were also higher on the border. Conversely, potential species richness was higher in the centre of the forest fragment. Higher biophony at noisy sites can be interpreted as behavioural responses of species for communicating in noisy areas. Alternatively, they could be the result of species segregation by degree of vocal plasticity or due to differences in composition of communities.

Distribution of the dwarf dog-faced bat Molossops temminckii (Chiroptera: Molossidae) in Colombia and comments on its morphometry

The genus Molossops includes two species that are restricted to South America: Molossops neglectus and Molossops temminckii. The smaller dog-faced dwarf Molossops temminckii is distributed from Colombia to Argentina and has a wide morphological variation and vocal plasticity. In Colombia, this species remains poorly known. To fill distributional gaps, we present novel records from Arauca, Atlántico, Bolívar, Córdoba, and Huila departments. We also present an analysis of the morphometric variation in South America using Principal Component Analyses. These show an external and cranial difference of specimens of Colombia in respect of other and South America populations. In Colombian landscapes dominated by the floodplain savanna of the Orinoco region, Molossops temminckii is smaller than in the other regions of the country, and the previously suggested existence of cryptic diversity within the taxon should be evaluated. Therefore, we suggest further integrative analyses to investigate a possible subspecific status of some Colombian populations.

Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds

Birdsong, like human speech, consists of a sequence of temporally precise movements acquired through vocal learning. The learning of such sequential vocalizations depends on the neural function of the motor cortex and basal ganglia. However, it is unknown how the connections between cortical and basal ganglia components contribute to vocal motor skill learning, as mammalian motor cortices serve multiple types of motor action and most experimentally tractable animals do not exhibit vocal learning. Here, we leveraged the zebra finch, a songbird, as an animal model to explore the function of the connectivity between cortex-like (HVC) and basal ganglia (area X), connected by HVC(X) projection neurons with temporally precise firing during singing. By specifically ablating HVC(X) neurons, juvenile zebra finches failed to copy tutored syllable acoustics and developed temporally unstable songs with less sequence consistency. In contrast, HVC(X)-ablated adults did not alter their learned song structure, but generated acoustic fluctuations and responded to auditory feedback disruption by the introduction of song deterioration, as did normal adults. These results indicate that the corticobasal ganglia input is important for learning the acoustic and temporal aspects of song structure, but not for generating vocal fluctuations that contribute to the maintenance of an already learned vocal pattern.