Disconnection of a basal ganglia circuit in juvenile songbirds attenuates the spectral differentiation of song syllables

Similar to language acquisition by human infants, juvenile male zebra finches (Taeniopygia guttata) imitate an adult (tutor) song by transitioning from repetitive production of one or two undifferentiated protosyllables to the sequential production of a larger and spectrally heterogeneous set of syllables. The primary motor region that controls learned song is driven by a confluence of input from two premotor pathways: a posterior pathway that encodes the adult song syllables and an anterior pathway that includes a basal ganglia (BG)‐thalamo‐cortical circuit. Similar to mammalian motor‐learning systems, the songbird BG circuit is thought to be necessary for shaping juvenile vocal behaviour (undifferentiated protosyllables) toward specific targets (the tutor's song syllables). Here, we tested the hypothesis that anterior pathway activity contributes to the process of protosyllable differentiation. Bilateral ablation of lateral magnocellular nucleus of the anterior nidopallium (LMAN) was used to disconnect BG circuitry at ages before protosyllable production and differentiation. Comparison to surgical controls revealed that protosyllables fail to differentiate in birds that received juvenile LMAN ablation—the adult songs of birds with >80% bilateral LMAN ablation consisted of only one or two syllables produced with the repetitive form and spectral structure that characterizes undifferentiated protosyllables in normal juveniles. Our findings support a role for BG circuitry in shaping juvenile vocal behaviour toward the acoustic structure of the tutor song and suggest that posterior pathway function remains in an immature “default” state when developmental interaction with the anterior pathway is reduced or eliminated. © 2013 Wiley Periodicals, Inc. Develop Neurobiol 74: 574–590, 2014     

Compromised neural selectivity for song in birds with impaired sensorimotor learning

Anterior forebrain (AF) neurons become selective for song as songbirds learn to produce a copy of a memorized tutor song. We report that development of selectivity is compromised when birds are prevented from matching their output to the tutor song. Finches with denervated vocal organs developed stable song, but it usually did not resemble the tutor song. In those birds, numerous neurons in Area X responded selectively to both tutor and bird's own song (BOS), indicating the importance of both in shaping AF responses. The degree of selectivity for BOS was less, however, than that of normal adults. In contrast, neurons in denervated birds that successfully mimicked tutor song exhibited normal adult selectivity for BOS. Thus, during sensorimotor learning, selectivity for complex stimuli may be influenced by how well motor output matches internal sensory models.     

Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production

Male zebra finches normally crystallize song at approximately 90 days and do not show vocal plasticity as adults. However, changes to adult song do occur after unilateral tracheosyringeal (ts) nerve injury, which denervates one side of the vocal organ. We examined the effect of placing bilateral lesions in LMAN (a nucleus required for song development but not for song maintenance in adults) upon the song plasticity that is induced by ts nerve injury in adults. The songs of birds that received bilateral lesions within LMAN followed by right ts nerve injury silenced, on average, 0.25 syllables, and added 0.125 syllables (for an average turnover of 0.375 syllables), and changed neither the frequency with which individual syllables occurred within songs nor the motif types they used most often. In contrast, the songs of birds that received sham lesions followed by ts nerve injury lost, on average, 1.625 syllables, silenced 0.125 syllables, and added 0.75 syllables, turning over an average of 2.5 syllables. They also significantly changed both the frequency with which individual syllables were included in songs and the motif variants used. Thus, song plasticity induced in adult zebra finches with crystallized songs requires the presence of LMAN, a nucleus which had been thought to play a role in vocal production only during song learning. Although the changes to adult songs induced by nerve transection are more limited than those that arise during song development, the same circuitry appears to underlie both types of plasticity.     

Novel motor gestures for phonation during inspiration enhance the acoustic complexity of birdsong.

Sound generation based on a pulmonary mechanism typically occurs during the expiratory phase of respiration. Phonation during inspiration has been postulated for the calls of some amphibians and for exceptional sounds in some human languages. No direct evidence exists for phonation during inspiration in birds, but such a mechanism has been proposed to explain very long uninterrupted songs. Here, we report the first physiological evidence for inspiratory sound production in the song of the zebra finch (Taeniopygia guttata). Motor gestures of the vocal and respiratory muscles leading to the production of inspiratory phonation differ from those of silent inspirations during song as well as from those leading to phonation during expiration. Inspiratory syllables have a high fundamental frequency, which makes them acoustically distinct from all other zebra finch song syllables. Furthermore, young zebra finches copy these inspiratory syllables from their tutor song, producing them during inspiration. This suggests that physical limitations confine the production of these sounds to the inspiratory phase in zebra finches. These findings directly demonstrate how novel respiratory-vocal coordination can enhance the acoustic structure of birdsong, and thus provide insight into the evolution of song complexity.     

Song development in the white-crowned sparrow: modification of learned song

Previous research has shown that laboratory-tutored white-crowned sparrows, Zonotrichia leucophrys nuttalli, can learn tape-recorded song only until they are about 50 days of age. However, they can learn either conspecific or allospecific song after they are 50 days of age when a live tutor is used. Because the live-tutored birds had not been exposed to song during the first 50 days of life, a question regarding the reasonableness of applying these results to the natural, field situation can be raised. In the experiments reported here, hand-raised nestling white-crowned sparrows between 10 and 50 days of age were tutored in the laboratory with one song, and were then placed with a live tutor singing a different dialect when they were over 50 days of age. Eight of 13 males, and none of 10 females, adopted the song of the second tutor. Birds were also captured in the field as fledglings, and were placed with a live tutor singing a song different from that of the natal area: three of seven males, and one of five females, adopted the song of the live tutor. Four birds that had been group-isolated (two males and two females) were exposed to a live tutor when they were 100 days old, and none acquired normal song; all sang isolate song. The results of these studies indicate that there is considerable plasticity in the song learning of whitecrowned sparrows, and that, for many individuals, song can be modified quite readily. The implications of these findings for the nature of the sensitive phase and for mechanisms of song learning are discussed.     

Song learning from playback in zebra finches: is there an effect of operant contingency?

Social interaction is often regarded as crucial for song copying in zebra finches, Taeniopygia guttata. Contingencies in the interaction between pupil and tutor might be essential for the song-copying process. The effect of contingency between a pupil's operant behaviour and tutor song has been studied previously, but with contradictory results. Our aim in this experiment was to provide a more rigorous test of the effect of operant contingent exposure to song playback in zebra finches. Eight experimental males were trained to expose themselves to tutor song by operant key pecking during their sensitive phase for song learning. Each bird had a yoked control, which heard the same tutor song at the same time. All birds were acoustically isolated. The results were surprising in two ways: (1) the control birds copied song to which they were passively exposed; and (2) the experimental birds did not copy more than the controls did. So, we found no effect of operant contingency on song learning. Furthermore, when tested as adults all but one male preferred the tutor song to an unfamiliar one. We conclude that zebra finches can copy playback song, and that social interaction is not crucial for song copying, although it might still be facilitating. Copyright 1999 The Association for the Study of Animal Behaviour.     

Song learning with audiovisual compound stimuli in zebra finches

We investigated the effects of audiovisual compound training on song learning in zebra finches, Taeniopygia guttata. In the first experiment, presentation of a stuffed adult zebra finch male was found to be reinforcing to zebra finch males in an operant task. In a separate experiment, zebra finch males were reared without their father from day 7 after hatching onwards. Between 35 and 76 days, they were placed in isolation and exposed to taped songs of a zebra finch male, according to a random schedule (20 presentations/h). For half of the birds, presentation of the song coincided with presentation of a stuffed zebra finch male. For the remaining birds, each presentation of the song was followed by presentation of a stuffed male. The birds were subsequently isolated until day 142, when their own songs were recorded and analysed. Birds in both groups shared significantly more song elements with their tutor songs than with an unfamiliar song. There was no significant difference in song learning between the groups. These results confirm that zebra finches can learn part of their songs from taped tutor songs. Furthermore, simultaneous presentation of the tutor song and a relevant, salient visual stimulus is not superior to sequential presentation. Copyright 1999 The Association for the Study of Animal Behaviour.     

Captive Rearing Experiments Confirm Song Development without Learning in a Tracheophone Suboscine Bird

The origin of vocal learning in animals has long been the subject of debate, but progress has been limited by uncertainty regarding the distribution of learning mechanisms across the tree of life, even for model systems such as birdsong. In particular, the importance of learning is well known in oscine songbirds, but disputed in suboscines. Members of this diverse group (∼1150 species) are generally assumed not to learn their songs, but empirical evidence is scarce, with previous studies restricted to the bronchophone (non-tracheophone) clade. Here, we conduct the first experimental study of song development in a tracheophone suboscine bird by rearing spotted antbird (Hylophylax naevioides) chicks in soundproofed aviaries. Individuals were raised either in silence with no tutor or exposed to standardized playback of a heterospecific tutor. All individuals surviving to maturity took a minimum of 79 days to produce a crystallized version of adult song, which in all cases was indistinguishable from wild song types of their own species. These first insights into song development in tracheophone suboscines suggest that adult songs are innate rather than learnt. Given that empirical evidence for song learning in suboscines is restricted to polygamous and lek-mating species, whereas tracheophone suboscines are mainly monogamous with long-term social bonds, our results are consistent with the view that sexual selection promotes song learning in birds.     

Factors limiting song acquisition in adult zebra finches

Song learning takes place in two separate or partially overlapping periods, a sensory phase in which a tutor song is memorized and a sensorimotor phase in which a copy of the model is produced. The stage of song development where song becomes stable and stereotyped is called crystallization. Adult birds usually do not learn new song in many species including the zebra finch. However, it is not known whether song crystallization as such or aging impedes adult learning. Exposure to loud noises prevents birds from developing and crystallizing their song, because they cannot control their voice by auditory feedback. Zebra finches even without previous experience of hearing or singing a song failed to learn a song model provided in adulthood. Thus, neither the absence of a tutor song nor the lack of song crystallization enables new song learning in adulthood, but age per se limits the ability or motivation to learn song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2009     

Song- and order-selective neurons develop in the songbird anterior forebrain during vocal learning

The anterior forebrain (AF) pathway of songbirds has an essential but poorly understood function during song learning, a process requiring auditory experience. Consistent with a role in processing auditory information, two nuclei of the AF, the lateral magnocellular nucleus of the anterior neostriatum (lMAN) and Area X (X), contain some of the most complex auditory neurons known. In adult zebra finches, these neurons are strongly selective for both spectral and temporal properties of song: They respond more robustly to the bird's own song (BOS) than to songs of conspecific individuals, and they respond less well to BOS if it is played in reverse. lMAN and X neurons of young finches early in the process of song learning (30–45 days of age) are also song responsive, but lack the song and order selectivity present in adult birds. By an intermediate stage of learning (60 days), when birds have experience of both tutor song and their own developing (plastic) song, AF neurons have significant song and order selectivity for both tutor song and BOS (in this case, plastic song). The degree of BOS selectivity is still less than that found in adults, however. In addition, neurons at 60 days are heterogenous in their preference for BOS versus tutor song: Most prefer BOS, some prefer tutor song, and others respond equally to both songs. The selectivity of adult AF auditory neurons therefore arises rapidly during development from neurons that are initially unselective. These neurons are one of the clearest examples of experience-dependent acquisition of complex stimulus selectivity. Moreover, the neural selectivity for both BOS and tutor song at 60 days raises the possibility that experience of both songs during learning contributes to the properties of individual AF neurons. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 694–709, 1997     

Song discrimination learning in zebra finches

Young male and female zebra finches, Taeniopygia guttata, were tested for their ability to discriminate between the song of their father or tutor and that of another male in two types of preference test, one with a male whose song was dissimilar to that of the father or tutor and one with a male who sang a similar song, on removal from the father, at 4 months and at 6 months of age. Birds that were isolated from their father at 25 days (group A) did not show a preference for their father's song whereas those isolated from the father at 35 days (groups B and C) learnt to prefer their father's song. In addition, group C, which were housed with tutor 1 from 35 to 70 days and with tutor 2 from 4 to 6 months of age, preferred their tutors' songs to those of other males. If one compares the strength of preference in the two types of test, group B showed a weaker preference for the father in tests with the father and a similar male. Further, group C showed a weaker preference in the test with tutor 1 versus a similar male. The possible influence of tutor, sibling and own song on the discrimination of the father's song is discussed, and the results are compared with those for song performance learning. Finally, the mother birds preferred their mate's song.     

Effects of housing condition and early corticosterone treatment on learned features of song in adult male zebra finches

Early developmental stress can have long-term physiological and behavioral effects on an animal. Developmental stress and early corticosterone (Cort) exposure affect song quality in many songbirds. Early housing condition can act as a stressor and affect the growth of nestlings and adult song, and improvements in housing condition can reverse adverse effects of early stress exposure in rodents. However, little is known about this effect in songbirds. Therefore, we took a novel approach to investigate if housing condition can modify the effects of early Cort exposure on adult song in male zebra finches. We manipulated early housing conditions to include breeding in large communal flight cages (FC; standard housing condition; with mixed-sex and mix-aged birds) versus individual breeding cages (IBC, one male–female pair with small, IBC-S, or large clutches, IBC-L) in post-hatch Cort treated male birds. We found that Cort treated birds from IBC-S have higher overall song learning scores (between tutor and pupil) than from FC but there is no difference between these groups in the No-Cort treated birds. When examining the effects of Cort within each housing condition, overall song learning scores decreased in Cort treated birds from flight cages but increased in birds from IBC-S compared to controls. Likewise, the total number of syllables and syllable types increased significantly in Cort treated birds from IBC-S, but decreased in FC-reared birds though this effect was not statistically significant. These findings suggest that the effects of early Cort treatment on learned features of song depend on housing condition.     

SONG DEVELOPMENT IN CHFFINCHES: WHAT IS LEARNT AND WHEN?

Male Chaffinches share no more songs with territorial neighbours than would be expected by chance, suggesting that some song learning occurs before young birds set up their territories. Hand-reared birds are capable of learning song both in their first spring and in the previous summer one young bird produced a good copy of a song which he had only heard as a nestling and fledgling eight months previously. While song learning involves accurate copying of individual elements, the variation in number in elements in a phrase and the temporal pattern of singing shown by hand-reared birds were similar to that of wild birds rather than being influenced by the tutor tapes.     

Altered auditory BOLD response to conspecific birdsong in zebra finches with stuttered syllables

How well a songbird learns a song appears to depend on the formation of a robust auditory template of its tutor's song. Using functional magnetic resonance neuroimaging we examine auditory responses in two groups of zebra finches that differ in the type of song they sing after being tutored by birds producing stuttering-like syllable repetitions in their songs. We find that birds that learn to produce the stuttered syntax show attenuated blood oxygenation level-dependent (BOLD) responses to tutor's song, and more pronounced responses to conspecific song primarily in the auditory area field L of the avian forebrain, when compared to birds that produce normal song. These findings are consistent with the presence of a sensory song template critical for song learning in auditory areas of the zebra finch forebrain. In addition, they suggest a relationship between an altered response related to familiarity and/or saliency of song stimuli and the production of variant songs with stuttered syllables.     

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

Learning-Related Neuronal Activation in the Zebra Finch Song System Nucleus HVC in Response to the Bird's Own Song

Like many other songbird species, male zebra finches learn their song from a tutor early in life. Song learning in birds has strong parallels with speech acquisition in human infants at both the behavioral and neural levels. Forebrain nuclei in the 'song system' are important for the sensorimotor acquisition and production of song, while caudomedial pallial brain regions outside the song system are thought to contain the neural substrate of tutor song memory. Here, we exposed three groups of adult zebra finch males to either tutor song, to their own song, or to novel conspecific song. Expression of the immediate early gene protein product Zenk was measured in the song system nuclei HVC, robust nucleus of the arcopallium (RA) and Area X. There were no significant differences in overall Zenk expression between the three groups. However, Zenk expression in the HVC was significantly positively correlated with the strength of song learning only in the group that was exposed to the bird's own song, not in the other two groups. These results suggest that the song system nucleus HVC may contain a neural representation of a memory of the bird's own song. Such a representation may be formed during juvenile song learning and guide the bird's vocal output.     

The Development of Geographic Song Preferences in Female Song Sparrows Melospiza melodia

Previous work suggests that early learning plays a role in auditory preferences of female songbirds. We explored whether early experience shapes preferences for local geographic song in female song sparrows ( Melospiza melodia ), a species that prefers local geographic song in adulthood. We hand-reared females from two locations 450 km apart and controlled song exposure early in life. To examine the effects of experience and inherited factors on geographic song preferences, we used a counterbalanced design. Females from each location were tutored with either natal song (recorded from their location of capture) or non-natal song (recorded from the other location) and their preferences for tutor vs. non-tutor song assessed in adulthood. We also examined song preferences in isolate females reared with no song experience. We found that tutored females preferred their tutor song over non-tutor song, regardless of their capture location. Furthermore, birds not exposed to song (isolates) had no geographic song preferences. Thus, song exposure early in life clearly plays an important role in adult female preferences for local song in this species.     

Vocal imitation in blindfolded zebra finches (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>) is facilitated in the presence of a non-singing conspecific female

Song acquisition in young male zebra finches, Taeniopygia guttata, is viewed as a learning process by imitation from a visible conspecific male acting as a song tutor. The role played by non-singing conspecific females in this process has been poorly documented. The influence of social contact on the song learning of blindfolded young males was investigated in both female-raised and pair-raised birds. Pupils with both eyes occluded from about 35 to 65 days post-hatch, the sensitive phase for song learning, copied significantly more from an adult male sharing their cage when tutored in the presence of a female sibling than in her absence. Interestingly, the effect was more pronounced in female-raised birds compared to pair-raised birds. I conclude that physical contact in the absence of visual cues is sufficient for song imitation to occur. The results demonstrate an instance of social stimulation by non-singing females in the song acquisition of male songbirds.     

Song Motor control organizes acoustic patterns on two levels in Bengalese finches (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

Based on statistical analyses of song sequences, Bengalese finch (Lonchura striata var. domestica) songs do not show unvarying motif repetition as has been found in zebra finches (Taeniopygia guttata). Instead, there are variations of partially stereotyped sequences of song syllables. Although these stereotyped sequences consist of multiple syllables, in most cases these syllables occur together. To examine whether such structures really exist as a vocal production unit, we subjected singing birds to a light flash and determined when the stimulus stopped the songs. When light interruptions were presented within the statistically stereotyped sequences, the subsequent syllables tended to be produced, whereas interruptions presented during the statistically variable sequences tended to cause instantaneous song termination. This suggests that the associations among the song syllables that compose the statistically stereotyped sequences are more order dependent than those for the statistically variable sequences, and the tolerances of syllable pairs to visual interruptions are consistent with the statistical song structures. Additionally, following interruptions, several types of song sequence variations were observed that had not been previously reported. These phenomena might be caused by various effects of the visual stimulus on the hierarchical motor control program.