Explore the vast range of titles available.

Humans and songbirds learn to sing or speak by listening to acoustic models, forming auditory templates, and then learning to produce vocalizations that match the templates. These taxa have evolved specialized telencephalic pathways to accomplish this complex form of vocal learning, which has been reported for very few other taxa. By contrast, the acoustic structure of most animal vocalizations is produced by species-specific vocal motor programmes in the brainstem that do not require auditory feedback. However, many mammals and birds can learn to fine-tune the acoustic features of inherited vocal motor patterns based upon listening to conspecifics or noise. These limited forms of vocal learning range from rapid alteration based on real-time auditory feedback to long-term changes of vocal repertoire and they may involve different mechanisms than complex vocal learning. Limited vocal learning can involve the brainstem, mid-brain and/or telencephalic networks. Understanding complex vocal learning, which underpins human speech, requires careful analysis of which species are capable of which forms of vocal learning. Selecting multiple animal models for comparing the neural pathways that generate these different forms of learning will provide a richer view of the evolution of complex vocal learning and the neural mechanisms that make it possible. This article is part of the theme issue ‘What can animal communication teach us about human language?’

Vocal learning, in which animals modify their vocalizations based on social experience, has evolved in several lineages of mammals and birds, including humans. Despite much attention, the question of how this key cognitive trait has evolved remains unanswered. The motor theory for the origin of vocal learning posits that neural centres specialized for vocal learning arose from adjacent areas in the brain devoted to general motor learning. One prediction of this hypothesis is that visual displays that rely on complex motor patterns may also be learned in taxa with vocal learning. While learning of both spoken and gestural languages is well documented in humans, the occurrence of learned visual displays has rarely been examined in non-human animals. We tested for geographical variation consistent with learning of visual displays in long-billed hermits ( Phaethornis longirostris ), a lek-mating hummingbird that, like humans, has both learned vocalizations and elaborate visual displays. We found lek-level signatures in both vocal parameters and visual display features, including display element proportions, sequence syntax and fine-scale parameters of elements. This variation was not associated with genetic differentiation between leks. In the absence of genetic differences, geographical variation in vocal signals at small scales is most parsimoniously attributed to learning, suggesting a significant role of social learning in visual display ontogeny. The co-occurrence of learning in vocal and visual displays would be consistent with a parallel evolution of these two signal modalities in this species.

Background Understanding the neural basis of behavior requires insight into how different brain systems coordinate with each other. Existing connectomes for various species have highlighted brain systems essential to various aspects of behavior, yet their application to complex learned behaviors remains limited. Research on vocal learning in songbirds has extensively focused on the vocal control network, though recent work implicates a variety of circuits in contributing to important aspects of vocal behavior. Thus, a more comprehensive understanding of brain-wide connectivity is essential to further assess the totality of circuitry underlying this complex learned behavior. Results We present the O scine S tructural C onnectome for I nvestigating NE ural NET work ORG anization (OSCINE-NET.ORG), the first interactive mesoscale connectome for any vocal learner. This comprehensive digital map includes all known connectivity data, covering major brain superstructures and functional networks. Our analysis reveals that the songbird brain exhibits small-world properties, with highly connected communities functionally designated as motor, visual, associative, vocal, social, and auditory. Moreover, there is a small set of significant connections across these communities, including from social and auditory sub-communities to vocal sub-communities, which highlight ethologically relevant facets of vocal learning and production. Notably, the vocal community contains the majority of the canonical vocal control network, as well as a variety of other nodes that are highly interconnected with it, meriting further evaluation for their inclusion in this network. A subset of nodes forms a \"rich broker club,\" highly connected across the brain and forming a small circuit amongst themselves, indicating they may play a key role in information transfer broadly. Collectively, their bidirectional connectivity with multiple communities indicates they may act as liaisons across multiple functional circuits for a variety of complex behaviors. Conclusions OSCINE-NET.ORG offers unprecedented access to detailed songbird connectivity data, promoting insight into the neural circuits underlying complex behaviors. This data emphasizes the importance of brain-wide integration in vocal learning, facilitating a potential reevaluation of the canonical vocal control network. Furthermore, we computationally identify a small, previously unidentified circuit—one which may play an impactful role in brain-wide coordination of multiple complex behaviors.

Background Which mammals show vocal learning abilities, e.g., can learn new sounds, or learn to use sounds in new contexts? Vocal usage and comprehension learning are submodules of vocal learning. Specifically, vocal usage learning is the ability to learn to use a vocalization in a new context; vocal comprehension learning is the ability to comprehend a vocalization in a new context. Among mammals, harbor seals ( Phoca vitulina ) are good candidates to investigate vocal learning. Here, we test whether harbor seals are capable of vocal usage and comprehension learning. Results We trained two harbor seals to (i) switch contexts from a visual to an auditory cue. In particular, the seals first produced two vocalization types in response to two hand signs; they then transitioned to producing these two vocalization types upon the presentation of two distinct sets of playbacks of their own vocalizations. We then (ii) exposed the seals to a combination of trained and novel vocalization stimuli. In a final experiment, (iii) we broadcasted only novel vocalizations of the two vocalization types to test whether seals could generalize from the trained set of stimuli to only novel items of a given vocal category. Both seals learned all tasks and took ≤ 16 sessions to succeed across all experiments. In particular, the seals showed contextual learning through switching the context from former visual to novel auditory cues, vocal matching and generalization. Finally, by responding to the played-back vocalizations with distinct vocalizations, the animals showed vocal comprehension learning. Conclusions It has been suggested that harbor seals are vocal learners; however, to date, these observations had not been confirmed in controlled experiments. Here, through three experiments, we could show that harbor seals are capable of both vocal usage and comprehension learning.

Songbirds as a whole are considered to be vocal production learners, meaning that they modify the structure of their vocalizations as a result of experience with the vocalizations of others. The more than 4000 species of songbirds, however, vary greatly in crucial features of song development. Variable features include: (i) the normality of the songs of early-deafened birds, reflecting the importance of innate motor programmes in song development; (ii) the normality of the songs of isolation-reared birds, reflecting the combined importance of innate auditory templates and motor programmes; (iii) the degree of selectivity in choice of external models; (iv) the accuracy of copying from external models; and (v) whether or not learning from external models continues into adulthood. We suggest that because of this variability, some songbird species, specifically those that are able to develop songs in the normal range without exposure to external models, can be classified as limited vocal learners. Those species that require exposure to external models to develop songs in the normal range can be considered complex vocal learners. This article is part of the theme issue 'Vocal learning in animals and humans'.

Background Vocal learning is a rare, convergent trait that is fundamental to both human speech and birdsong. The Forkhead Box P2 (FOXP2) transcription factor appears necessary for both types of learned signals, as human mutations in FOXP2 result in speech deficits, and disrupting its expression in zebra finches impairs male-specific song learning. In juvenile and adult male finches, striatal FOXP2 mRNA and protein decline acutely within song-dedicated neurons during singing, indicating that its transcriptional targets are also behaviorally regulated. The identities of these targets in songbirds, and whether they differ across sex, development and/or behavioral conditions, are largely unknown. Results Here we used chromatin immunoprecipitation followed by sequencing (ChIP-Seq) to identify genomic sites bound by FOXP2 in male and female, juvenile and adult, and singing and non-singing birds. Our results suggest robust FOXP2 binding concentrated in putative promoter regions of genes. The number of genes likely to be bound by FOXP2 varied across conditions, suggesting specialized roles of the candidate targets related to sex, age, and behavioral state. We interrogated these binding targets both bioinformatically, with comparisons to previous studies, and biochemically, with immunohistochemistry using an antibody for a putative target gene. Gene ontology analyses revealed enrichment for human speech- and language-related functions in males only, consistent with the sexual dimorphism of song learning in this species. Fewer such targets were found in juveniles relative to adults, suggesting an expansion of this regulatory network with maturation. The fewest speech-related targets were found in the singing condition, consistent with the well-documented singing-driven down-regulation of FOXP2 in the songbird striatum. Conclusions Overall, these data provide an initial catalog of the regulatory landscape of FOXP2 in an avian vocal learner, offering dozens of target genes for future study and providing insight into the molecular underpinnings of vocal learning.

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'.

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.

Zebra finches undergo a gradual refinement of their vocalizations, transitioning from variable juvenile songs to the stereotyped song of adulthood. To investigate the neural mechanisms underlying song crystallization—a critical phase in this developmental process—we performed intracellular recordings in HVC (a premotor nucleus essential for song learning and production) of juvenile birds. We then compared these recordings to previously published electrophysiological data from adult birds. We found that HVC projection neurons in juvenile zebra finches during the song crystallization phase exhibited more variable spiking patterns compared to the precise bursting observed in adult HVC projection neurons. Additionally, subthreshold membrane potential fluctuations in juvenile neurons exhibited longer durations and larger amplitude excitatory postsynaptic potentials. These distinct temporal dynamics in HVC during song crystallization likely play a crucial role in the fine-tuning processes that shape the precise timing and structure of the mature zebra finch song.

Vocal production learning (VPL) is the capacity to learn to produce new vocalizations, which is a rare ability in the animal kingdom and thus far has only been identified in a handful of mammalian taxa and three groups of birds. Over the last few decades, approaches to the demonstration of VPL have varied among taxa, sound production systems and functions. These discrepancies strongly impede direct comparisons between studies. In the light of the growing number of experimental studies reporting VPL, the need for comparability is becoming more and more pressing. The comparative evaluation of VPL across studies would be facilitated by unified and generalized reporting standards, which would allow a better positioning of species on any proposed VPL continuum. In this paper, we specifically highlight five factors influencing the comparability of VPL assessments: (i) comparison to an acoustic baseline, (ii) comprehensive reporting of acoustic parameters, (iii) extended reporting of training conditions and durations, (iv) investigating VPL function via behavioural, perception-based experiments and (v) validation of findings on a neuronal level. These guidelines emphasize the importance of comparability between studies in order to unify the field of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.