Oscine Song Research Articles

Rudimentary substrates for vocal learning in a suboscine

Vocal learning has evolved in only a few groups of mammals and birds. The key neuroanatomical and behavioural links bridging vocal learners and non-learners are still unknown. Here we show that a non-vocal-learning suboscine, the eastern phoebe, expresses neural and behavioural substrates that are associated with vocal learning in closely related oscine songbirds. In phoebes, a specialized forebrain region in the intermediate arcopallium seems homologous to the oscine song nucleus RA (robust nucleus of arcopallium) by its neural connections, expression of glutamate receptors and singing-dependent immediate-early gene expression. Lesion of this RA-like region induces subtle but consistent song changes. Moreover, the unlearned phoebe song unexpectedly develops through a protracted ontogeny. These features provide the first evidence of forebrain vocal-motor control in suboscines, which has not been encountered in other avian non-vocal-learners, and offer a potential configuration of brain and behaviour from which vocal learning might have evolved.

Kiwis to pewees: the value of studying bird calls

Avian vocalizations are typically divided into two fundamental types: songs and calls. The dividing line between calls and songs is somewhat unclear, but researchers generally agree that songs are longer and more complex than calls, which tend to be brief and simple (Catchpole & Slater 2008). The literature on birdsong (particularly oscine passerine song) is extensive, encompassing the fields of behaviour, evolution, neuroscience, psychology and more (Slater 2003). Many fewer studies of avian vocalizations focus on the form and function of calls, but this is an area ripe for adding to our understanding of animal acoustic communication (Marler 2006). Researchers can learn much from analyses of avian calls for a number of reasons. First, calls are produced by all species. Many species of birds, particularly those in basal lineages, are not known to sing. Some nonpasserines do sing, but the majority of song research has been conducted on oscine passerine songbirds. Oscines are in part grouped together by their complex syringeal musculature and morphology that allows for the production of intricate song forms (Suthers & Zollinger 2006). However, it would be a mistake to assume that nonoscines, and even birds from basal lineages such as paleognath (ratites such as kiwis and ostriches), galliform and anseriform birds, do not exhibit complexity in the anatomy of their sound-producing structures or in their vocal repertoire. For example, ducks possess a range of fascinating syringeal morphologies (Livezey 1986, 1991); the relationship between the form of these structures and sound production remains to be studied. Basal birds can also produce a rich repertoire of vocalizations, as is seen in Wild Turkeys Meleagris gallopavo, which produce at least 28 different calls to help navigate their complex social world (Williams 1984). Both morphological and vocal complexity can hide undiscovered even in relatively well-studied species; in spite of decades of research into the vocal behavior of Greater Sage-grouse Centrocercus urophasianus, a ‘two-voiced’ system and a syringeal muscle found only in males were only recently described (Krakauer et al. 2009). Thus, while studies of song are necessarily taxonomically restricted, research into calls can take advantage of the rich diversity of morphology, ecology and behaviour found across all lineages of birds. Ornithologists are interested not only in how birds make sounds, but also why such a dizzying array of acoustic signals has arisen. Many hypotheses postulate evolutionary benefits associated with particular features of calls or songs. Inter-individual, inter-sexual and interpopulation differences in species with learned songs could result from the effects of learning. When the acoustic structure of an oscine song improves function, that outcome may be a result of cultural evolution. Calls, on the other hand, are generally thought to be innate, rather than learned (but this is not a universal rule, see Kroodsma & Baylis 1982, Zann 1985) (Catchpole & Slater 2008). Although they are innate, however, calls are not entirely fixed. The calls of many species show significant geographical and even inter-individual variation, as seen in the individual identity encoded in the harmonically rich calls of penguins (Aubin et al. 2000). Selection for communication functions has even led to adaptive variation within individuals. The calls of coucals, swans and tinamous vary with context or local environment, and the combination of vocal and visual displays in Red Junglefowl Gallus gallus has become a model system for understanding communication (Smith & Evans 2008, Geberzahn et al. 2009, Patel et al. 2010, Schuster et al. 2012). Thus, although calls are relatively fixed compared with songs, there is clearly individual variation and the potential for selection on these traits. When calls are unlearned, such selection would necessarily lead to biological evolution, allowing researchers to assess how vocal traits evolve in the absence of cultural influences. Finally, calls are particularly useful in studies of intersexual interactions because across avian species they are generally produced by both males and females (Catchpole & Slater 2008). Many studies of song-learning and song variation have been conducted in species where only the male sings. Although there is a growing interest in and recognition of female song (used in solo song or song duets), studies of song continue to be male-biased (Langmore 1998, Garamszegi et al. 2007). In contrast, studies of call form and function often focus on the calls of both sexes. By studying call form, researchers can gain insights into the power of natural selection in shaping vocal communication in both sexes. In an article published in this issue of Ibis, Digby et al. (2013) describe the calls of the Little Spotted Kiwi Apteryx owenii, providing an overview of call usage patterns and call structure. This article is one of only a *Corresponding author. Email: lauryn.benedict@unco.edu

Individual differences in the vocalizations of the buff-throated woodcreeper (Xiphorhynchus guttatus), a suboscine bird of neotropical forests

Unlike in temperate forests, bird communities in neo-tropical forests are largely composed of species of Tyranni, or suboscines, a suborder of passeriform birds that do not learn their songs. Thus, songs of suboscines are typically acoustically simple compared to the complex songs of Passeri, the oscine passeriforms. While a great deal is known about oscine song, few descriptions of the repertoires of tropical suboscines have been published, and relatively little is known about the use and function of song in suboscines. Additionally, whether suboscines can recognize individuals by voice alone has received little attention. One representative of these tropical suboscines is the buff-throated woodcreeper (Xiphorhynchus guttatus, Dendrocolaptinae), a bird commonly found in the forests of the tropical Americas. To investigate the possibility for individual variation in songs of this species, we recorded buff-throated woodcreepers at dawn and dusk in Amazonian Peru. From these recordings, we document two long-range song types, describe their acoustic parameters, and examine their occurrence at different times of day and across two seasons. Quantitative analysis of frequency, timing, and pattern of songs revealed that woodcreeper vocalizations varied significantly among individuals. A discriminant function analysis of song parameters successfully assigned a majority of songs to the correct individual. Despite their relatively simple structure, the vocalizations of buff-throated woodcreepers vary consistently among individuals but apparently not so distinctly as those of many oscines. Questions remain regarding whether the buffthroated woodcreeper can use these differences for individual recognition and how the two song types function in communication.

Conservation and expression of IQ‐domain‐containing calpacitin gene products (neuromodulin/GAP‐43, neurogranin/RC3) in the adult and developing oscine song control system

Songbirds are appreciated for the insights they provide into regulated neural plasticity. Here, we describe the comparative analysis and brain expression of two gene sequences encoding probable regulators of synaptic plasticity in songbirds: neuromodulin (GAP-43) and neurogranin (RC3). Both are members of the calpacitin family and share a distinctive conserved core domain that mediates interactions between calcium, calmodulin, and protein kinase C signaling pathways. Comparative sequence analysis is consistent with known phylogenetic relationships, with songbirds most closely related to chicken and progressively more distant from mammals and fish. The C-terminus of neurogranin is different in birds and mammals, and antibodies to the protein reveal high expression in adult zebra finches in cerebellar Purkinje cells, which has not been observed in other species. RNAs for both proteins are generally abundant in the telencephalon yet markedly reduced in certain nuclei of the song control system in adult canaries and zebra finches: neuromodulin RNA is very low in RA and HVC (relative to the surrounding pallial areas), whereas neurogranin RNA is conspicuously low in Area X (relative to surrounding striatum). In both cases, this selective downregulation develops in the zebra finch during the juvenile song learning period, 25-45 days after hatching. These results suggest molecular parallels to the robust stability of the adult avian song control circuit.

Enriched expression and developmental regulation of the middle‐weight neurofilament (NF‐m) gene in song control nuclei of the zebra finch

Songbirds evolved a complex set of dimorphic telencephalic nuclei that are essential for the learning and production of song. These nuclei, which together make up the oscine song control system, present several neurochemical properties that distinguish them from the rest of the telencephalon. Here we show that the expression of the gene encoding the middle-weight neurofilament (NF-M), an important component of the neuronal cytoskeleton and a useful tool for studying the cytarchitectonic organization of mammalian cortical areas, is highly enriched in large neurons within pallial song control nuclei (nucleus HVC, robustus nucleus of the arcopallium, and lateral magnocellular nucleus of the nidopallium) of male zebra finches (Taeniopygia guttata). We also show that this transcript is highly expressed in large neurons in the medulla, pons, midbrain, and thalamus. Moreover, we demonstrate that NF-M expression in song control nuclei changes during postembryonic development, peaking during an early phase of the song-learning period that coincides with the maturation of the song system. We did not observe changes in NF-M expression in auditory areas or in song control nuclei in the contexts of hearing song or singing, although these contexts result in marked induction of the transcription factor ZENK. This observation suggests that NF-M might not be under the regulatory control of ZENK in auditory areas or in song control nuclei. Overall, our data indicate that NF-M is a neurochemical marker for pallial song control nuclei and provide suggestive evidence of an involvement of NF-M in the development and/or maturation of the oscine song control system.

Calbindin‐positive neurons reveal a sexual dimorphism within the songbird analogue of the mammalian auditory cortex

The oscine song system, a set of interconnected brain nuclei involved in song production and learning, is one of the first and clearest examples of brain sexual dimorphism in a vertebrate, being typically well-developed in males, but not females. Here we present evidence for a sexual dimorphism in the caudomedial nidopallidum (NCM), an auditory area outside of the song system. NCM is thought to correspond to a portion of the auditory cortex of mammals and is involved in the perceptual processing of birdsong. We show that cells immunolabeled for the calcium-binding protein calbindin are primarily localized to caudal NCM and are almost twice as numerous in males as in females. We demonstrate that calbindin-positive cells constitute a subset of GABAergic cells in NCM, and show that the sex dimorphism in this cell population does not result from local gender differences in the overall density of neuronal or GABAergic cells. In addition, we demonstrate that calbindin-positive cells lack song-induced expression of the activity-dependent gene ZENK, and that song stimulation does not change the density or distribution of these cells in NCM. Finally, we show that the distribution of calbindin-positive cells in NCM is strikingly similar to the mRNA expression for the estrogen-generating enzyme aromatase. Together these results suggest that NCM is likely composed of neurochemically-distinct domains and presents a marked sex dimorphism in a specific subset of GABAergic neurons, which may confer sex-specific sensory processing capabilities to this auditory area. Our results also suggest that local sex steroid hormones may play a local role in auditory processing in the songbird telencephalon.

Peripheral Vocal Mechanisms in Birds: Are Songbirds Special?

This paper reviews recent advances regarding the peripheral mechanisms for song production by oscine songbirds and compares the vocal mechanisms of songbirds with those of certain non-oscines. The tracheobronchial syrinx of songbirds has several pairs of intrinsic muscles specialized for controlling particular aspects of sound production. The syringeal and vocal tract anatomy of non-oscines is much more diverse than that of songbirds and has fewer or no intrinsic syringeal muscles. Often the same extrinsic tracheal muscles control both the temporal and spectral properties of vocalizations. Although the vocalizations and vocal anatomy of these two groups are quite different, a number of motor patterns important in oscine song are also used by non-oscines. These include special respiratory techniques, such as minibreaths and pulsatile expiration, for sustained rapid vocalization, as well as the ability to simultaneously produce two acoustically unrelated 'voices'. However, the complex syringeal musculature of songbirds with laterally independent motor control of each side of the syrinx provides a more versatile vocal system in which the left and right sound sources can be coordinated in different ways, by specialized song control nuclei capable of vocal learning, to achieve diverse vocal effects.

A GABAergic, Strongly Inhibitory Projection to a Thalamic Nucleus in the Zebra Finch Song System

The anterior forebrain pathway (AFP) of the oscine song system is essential for song learning but not song production. Most cells recorded in this serially connected pathway show increased firing in response to song playback, suggesting largely excitatory connections among AFP nuclei. However, the neurons forming a key projection in this pathway, from area X to the medial nucleus of the dorsolateral thalamus (DLM), express glutamic acid decarboxylase in their somata and terminals, suggesting an inhibitory connection. To investigate the firing properties of DLM neurons and the functional influence of area X afferents in DLM, we made whole-cell recordings from DLM neurons in brain slices from adult male zebra finches. Most cells had intrinsic properties closely resembling those of mammalian thalamocortical cells, including a low-threshold Ca(2+) spike and time-dependent, hyperpolarization-activated inward rectification. Activation of afferents from area X evoked a strong, all-or-none IPSP whose amplitude and latency were unchanged by application of glutamate antagonists, consistent with a monosynaptic contact. The IPSP had a reversal potential near -70 mV and was blocked by the GABA(A) receptor antagonist bicuculline methiodide. Post-inhibitory rebound firing occurred in DLM neurons with a delay near 50 msec. Strong inhibition can combine with the intrinsic properties of DLM neurons to allow signaling on disinhibition. Our data are consistent with the hypothesis that the AFP corresponds to the mammalian corticobasal ganglia-thalamocortical loop. The similar functional properties of avian and mammalian thalamic neurons suggest conserved forebrain mechanisms of sensorimotor information processing across vertebrate taxa.

Descending auditory pathways in the adult male zebra finch (Taeniopygia Guttata)

Here, we examine the connectivity of two previously identified telencephalic stations of the auditory system of adult zebra finches, the neostriatal "shelf" that underlies the high vocal center (HVC) and the archistriatal "cup" adjacent to the robust nucleus of the archistriatum (RA). We used different kinds of neuroanatomical tracers to visualize the projections from the shelf to the HVC. In addition, we show that the shelf projects to the cup and that the cup projects to thalamic, midbrain, and pontine nuclei of the ascending auditory pathway. Our observations extend to songbirds anatomical features that are found in the auditory pathways of a nonoscine bird, the pigeon (Wild et al. [1993] J. Comp. Neurol. 337:32-62), and we suggest that the descending auditory projections found in mammals may also be a general property of the avian brain. Finally, we show that the oscine song control system is closely apposed to auditory pathways at many levels. Our observations may help in understanding the evolution and organization of networks for vocal communication and vocal learning in songbirds.

Acoustic analysis of the budgerigar vocal repertoire

Previous ethological studies of the budgerigar (Melopsittacus undulatus) have provided a functional description of the vocal repertoire [B. F. Brockway, Anim. Behav. 23, 294–324 (1964)]. The present study describes the acoustic structure of each of these complex vocalizations with an emphasis on the contact call. Acoustic features of each vocalization were measured from standard sonograms. Most of the vocalizations of the budgerigar are short, discrete calls varying in duration between 20 and 200 ms. A long, rambling courtship vocalization is also described which varies in duration from 10 s to 1 min. This vocalization is composed of many different elements and is performed primarily by males. This courtship vocalization may be functionally similar to the song of oscine song birds. The acoustic properties of these vocalizations are discussed in relation to the hearing capabilities of the budgerigar. [Work supported by NICHHD and NINCDS.]

Neuroanatomical Correlates of Hormone Sensitive Behaviors in Frogs and Birds

In this paper I review some aspects of neural and endocrine interactions in the control of reproductive behaviors of frogs and song birds. In Xenopus laevis , we have shown that castration will eliminate a male sex behavior, clasping, and that this behavior can be restored by the administration of exogenous testosterone or dihydrotestosterone but not by estradiol. This difference in hormone action is paralleled by differences in the locations of androgen and estrogen concentrating cells in the CNS of Xenopus . Certain brain regions contain autoradiographically demonstrable labelled cells only after the administration of tritiated testosterone; others only after estradiol injection. The possibility that label in a third group of nuclei, which contain radioactive steroid after either hormone, is due to metabolism of testosterone to estradiol is discussed. Studies in other anuran species have demonstrated that regions of hormone uptake are also involved in neural control of frog sex behavior. The song of oscine birds represents another hormone sensitive reproductive behavior whose neural control is probably inlluenced by the activity of hormone concentrating CNS cells. Some of the brain nuclei which comprise the efferent pathway for control of song in the canary have been shown to concentrate tritiated androgen in autoradiographic studies on song birds. The uptake of androgens by medullary motor neurons involved in the control of reproductively important vocalizations is common to anurans and oscine song birds. Whether this feature of hormone action on the CNS represents a special feature of the frog and bird brain or whether the phenomenon may also be present in other vertebrate groups awaits further investigation.