Vocal Learning System Research Articles

Examining the capability for rhythmic synchronization and music production in vocal learning parrot species.

Vocal production learning and beat perception and synchronization (BPS) share some common characteristics, which makes the vocal learning and rhythmic synchronization hypothesis (VLH) a reasonable explanation for the evolution of the capability for rhythmic synchronization. However, even in vocal learners, it is rare to see non-human animals demonstrate BPS to human music. Therefore, the first objective of this article is to propose some possible reasons why we do not see BPS in budgerigars, an excellent vocal learning species, while presenting some of my own findings. The second objective of this article is to propose a seamless bridge to connect the capability for vocal learning and BPS in locomotion. For this purpose, I present my own findings, wherein cockatiels spontaneously sang in synchrony with a melody of human music. This behavior can be considered a vocal version of BPS. Therefore, it can establish a connection between these two capabilities. This article agrees with the possibility that some mechanisms other than the vocal learning system may enable BPS, contrary to the original idea of VLH. Nevertheless, it is still reasonable to connect the capability for vocal learning and that for BPS. At the very least, the capability for vocal learning may contribute to the evolution of BPS. From these arguments, this article also proposes a scenario which includes vocalizing in synchrony as a driving force for the evolution of BPS and the capability for music production.

Evolving the capacity for socially guided vocal learning in songbirds: a preliminary study.

Socially guided vocal learning, the ability to use contingent reactions from social partners to guide immature vocalizations to more mature forms, is thought to be a rare ability known to be used only by humans, marmosets and two unrelated songbird species (brown-headed cowbirds and zebra finches). However, this learning strategy has never been investigated in the vast majority of species that are known to modify their vocalizations over development. We propose a novel, preliminary evolutionary modelling approach that uses ecological, reproductive and developmental traits to predict which species may incorporate social influences as part of their vocal learning system. We demonstrate our model using data from 28 passerines. We found three highly predictive traits: temporal overlap between sensory (memorization) and sensorimotor (practice) phases of song learning, song used for mate attraction, and social gregariousness outside the breeding season. Species with these traits were distributed throughout the clade, suggesting that a trait-based approach may yield new insights into the evolution of learning strategies that cannot be gleaned from phylogenetic relatedness alone. Our model suggests several previously uninvestigated and unexpected species as likely socially guided vocal learners and offers new insight into the evolution and development of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

The role of sex chromosomes and sex hormones in vocal learning systems

Vocal learning is the ability to imitate and modify sounds through auditory experience, a rare trait found in only a few lineages of mammals and birds. It is a critical component of human spoken language, allowing us to verbally transmit speech repertoires and knowledge across generations. In many vocal learning species, the vocal learning trait is sexually dimorphic, where it is either limited to males or present in both sexes to different degrees. In humans, recent findings have revealed subtle sexual dimorphism in vocal learning/spoken language brain regions and some associated disorders. For songbirds, where the neural mechanisms of vocal learning have been well studied, vocal learning appears to have been present in both sexes at the origin of the lineage and was then independently lost in females of some subsequent lineages. This loss is associated with an interplay between sex chromosomes and sex steroid hormones. Even in species with little dimorphism, like humans, sex chromosomes and hormones still have some influence on learned vocalizations. Here we present a brief synthesis of these studies, in the context of sex determination broadly, and identify areas of needed investigation to further understand how sex chromosomes and sex steroid hormones help establish sexually dimorphic neural structures for vocal learning.

Estrogen and sex-dependent loss of the vocal learning system in female zebra finches

Sex hormones alter the organization of the brain during early development and coordinate various behaviors throughout life. In zebra finches, song learning is limited to males, with the associated song learning brain pathways only maturing in males and atrophying in females. While this atrophy can be prevented by treating females with exogenous estrogen during early post-hatch development, the requirement of estrogen during normal male song system development is uncertain. For the first time in songbirds, we administered exemestane, a potent third generation estrogen synthesis inhibitor, from the day of hatching until adulthood in order to reassess the role of estrogen in song circuit development. We examined the behavior, brain anatomy, and transcriptomes of individual song nuclei in these pharmacologically manipulated animals. We found that males with long-term exemestane treatment had diminished male-specific plumage and impaired song learning, but minimal effect on song nuclei sizes and their specialized transcriptome. Consistent with prior findings, females with long-term estrogen treatment retained a functional song system with song nuclei that had specialized gene expression similar, but not identical to males. We also observed that different song nuclei responded to estrogen manipulation differently, with Area X in the striatum being the most altered by estrogen modulation. These findings support the hypothesis that song learning is an ancestral trait in both sexes that was subsequently suppressed in females of some species and that estrogen has come to play a critical role in modulating this suppression as well as refinement of song learning.

Exploring the molecular basis of neuronal excitability in a vocal learner

BackgroundVocal learning, the ability to learn to produce vocalizations through imitation, relies on specialized brain circuitry known in songbirds as the song system. While the connectivity and various physiological properties of this system have been characterized, the molecular genetic basis of neuronal excitability in song nuclei remains understudied. We have focused our efforts on examining voltage-gated ion channels to gain insight into electrophysiological and functional features of vocal nuclei. A previous investigation of potassium channel genes in zebra finches (Taeniopygia guttata) revealed evolutionary modifications unique to songbirds, as well as transcriptional specializations in the song system [Lovell PV, Carleton JB, Mello CV. BMC Genomics 14:470 2013]. Here, we expand this approach to sodium, calcium, and chloride channels along with their modulatory subunits using comparative genomics and gene expression analysis encompassing microarrays and in situ hybridization.ResultsWe found 23 sodium, 38 calcium, and 33 chloride channel genes (HGNC-based classification) in the zebra finch genome, several of which were previously unannotated. We determined 15 genes are missing relative to mammals, including several genes (CLCAs, BEST2) linked to olfactory transduction. The majority of sodium and calcium but few chloride channels showed differential expression in the song system, among them SCN8A and CACNA1E in the direct motor pathway, and CACNG4 and RYR2 in the anterior forebrain pathway. In several cases, we noted a seemingly coordinated pattern across multiple nuclei (SCN1B, SCN3B, SCN4B, CACNB4) or sparse expression (SCN1A, CACNG5, CACNA1B).ConclusionThe gene families examined are highly conserved between avian and mammalian lineages. Several cases of differential expression likely support high-frequency and burst firing in specific song nuclei, whereas cases of sparse patterns of expression may contribute to the unique electrophysiological signatures of distinct cell populations. These observations lay the groundwork for manipulations to determine how ion channels contribute to the neuronal excitability properties of vocal learning systems.

Core and Shell Song Systems Unique to the Parrot Brain.

The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot “core” song system is similar to the song systems of songbirds and hummingbirds, whereas the “shell” song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.

Food rewards modulate the activity of song neurons in Bengalese finches

Vocal learning, a critical component of speech acquisition, is a rare trait in animals. Songbirds are a well-established animal model in vocal learning research; male birds acquire novel vocal patterns and have a well-developed 'song system' in the brain. Although this system is unique to songbirds, anatomical and physiological studies have reported similarities between the song system and the thalamo-cortico-basal ganglia circuit that is conserved among reptiles, birds, and mammals. Here, we focused on the similarity of the neural response between these two systems while animals were engaging in operant tasks. Neurons in the basal ganglia of vertebrates are activated in response to food rewards and reward predictions in behavioral tasks. A striatal nucleus in the avian song system, Area X, is necessary for vocal learning and is considered specialized for singing. We found that the spiking activity of singing-related Area X neurons was modulated by food rewards and reward signals in an operant task. As previous studies showed that Area X is not critical for general cognitive tasks, the role of Area X in general learning might be limited and vestigial. However, our results provide a new viewpoint to investigate the independence of the vocal learning system from neural systems involved in other cognitive tasks.

Sexually dimorphic perineuronal net expression in the songbird

Sexual dimorphism of song behavior and its underlying brain architecture characterizes the vocal learning system of many songbirds (Nottebohm and Arnold [1] and Ball and MacDougall-Shackleton [2]). Females do not sing and their neural song control system is reduced compared to males. However, females do learn to discriminate male song during a sensitive period (Clayton [3] and Nelson et al. [4]). We reasoned that any song nuclei that might store developmental social learning in female zebra finches would be marked by extracellular perineuronal nets (PNNs), which limit plasticity at the ends of critical periods (Hockfield et al. [5] and Hensch [6]), stabilize learning (Wang and Fawcett [7]), and demarcate all song nuclei in male finches (Balmer et al. [8]). PNN expression patterns in four brain areas were compared in males and females: the Lateral Magnocellular Nucleus (LMAN) and a basal ganglia region that contains Area X in males, which together constitute an anterior cortical-basal ganglia pathway necessary for male song plasticity, and HVC and the Robust Nucleus of the Arcopallium (RA), which together form a posterior pathway that is critical for song production in males. We found a dichotomy of PNN expression in the female song system: the anterior cortical-basal ganglia pathway was highly enriched for PNNs and indistinguishable from males, whereas the posterior pathway was essentially devoid of PNNs. These data indicate that social signaling in the female song system may undergo a true critical period, similar to sensory systems, and that limiting this critical period selectively involves the song cortical-basal ganglia pathway.

Molecular Mapping of Movement-Associated Areas in the Avian Brain: A Motor Theory for Vocal Learning Origin

Vocal learning is a critical behavioral substrate for spoken human language. It is a rare trait found in three distantly related groups of birds-songbirds, hummingbirds, and parrots. These avian groups have remarkably similar systems of cerebral vocal nuclei for the control of learned vocalizations that are not found in their more closely related vocal non-learning relatives. These findings led to the hypothesis that brain pathways for vocal learning in different groups evolved independently from a common ancestor but under pre-existing constraints. Here, we suggest one constraint, a pre-existing system for movement control. Using behavioral molecular mapping, we discovered that in songbirds, parrots, and hummingbirds, all cerebral vocal learning nuclei are adjacent to discrete brain areas active during limb and body movements. Similar to the relationships between vocal nuclei activation and singing, activation in the adjacent areas correlated with the amount of movement performed and was independent of auditory and visual input. These same movement-associated brain areas were also present in female songbirds that do not learn vocalizations and have atrophied cerebral vocal nuclei, and in ring doves that are vocal non-learners and do not have cerebral vocal nuclei. A compilation of previous neural tracing experiments in songbirds suggests that the movement-associated areas are connected in a network that is in parallel with the adjacent vocal learning system. This study is the first global mapping that we are aware for movement-associated areas of the avian cerebrum and it indicates that brain systems that control vocal learning in distantly related birds are directly adjacent to brain systems involved in movement control. Based upon these findings, we propose a motor theory for the origin of vocal learning, this being that the brain areas specialized for vocal learning in vocal learners evolved as a specialization of a pre-existing motor pathway that controls movement.

Neural systems for vocal learning in birds and humans: a synopsis

I present here a synopsis on a hypothesis that I derived on the similarities and differences of vocal learning systems in vocal learning birds for learned song and in humans for spoken language. This hypothesis states that vocal learning birds-songbirds, parrots, and hummingbirds-and humans have comparable specialized forebrain regions that are not found in their close vocal non-learning relatives. In vocal learning birds, these forebrain regions appear to be divided into two sub-pathways, a vocal motor pathway mainly used to produce learned vocalizations and a pallial-basal-ganglia-thalamic loop mainly used to learn and modify the vocalizations. I propose that humans have analogous forebrain pathways within and adjacent to the motor and pre-motor cortices, respectively, used to produce and learn speech. Recent advances have supported the existence of the seven cerebral vocal nuclei in the vocal learning birds and the proposed brain regions in humans. The results in birds suggest that the reason why the forebrain regions are similar across distantly related vocal learners is that the vocal pathways may have evolved out of a pre-existing motor pathway that predates the ancient split from the common ancestor of birds and mammals. Although this hypothesis will require the development of novel technologies to be fully tested, the existing evidence suggest that there are strong genetic constraints on how vocal learning neural systems can evolve.