Correlations between song acquisition, song production, and plasma levels of testosterone and estradiol in sparrows

Male birdsong is a sexually dimorphic behavior characterized by learned dialects. In a combined study of learning in relation to steroid levels in the plasma, changes in estradiol and testosterone levels were correlated with the timing of the sensitive period for song acquisition and with successive stages in song development. Male swamp sparrows were trained with a changing series of live singing tutors from 26 days to 1 year of age. Song acquisition was concentrated between 26 and 47 days of age (57%). By 85 days of age 71% of acquisition was completed; some occurred as late as 300 days. There were two major periods when testosterone levels were elevated. The first, from 30-80 days, encompassed most of the period of song acquisition. The second, from 260 to at least 360 days of age, coincided with song development. Estradiol levels were elevated from 18 to 170 days of age, encompassing almost all of the period of song acquisition. A marked estradiol peak between 40 and 50 days coincided with a trough in testosterone levels and a hiatus in song acquisition. The strong correlation between the second period of elevated testosterone and song motor development suggests a causal connection, with levels peaking in mid-development and declining during mature song production. Estradiol levels were elevated at the start of the study and remained so during early subsong production, from 30 to 165 days. They then fell to baseline, remaining there throughout the resumption of subsong and plastic song production at 250-326 days. Both estradiol and testosterone are candidates for possibly affecting song acquisition.     

Song development in the white-crowned sparrow: social factors and sex differences

Results of earlier studies indicated that hand-raised white-crowned sparrows exposed to taperecorded songs learned conspecific song between ages 10–50 days, but not before or after that age. These studies also indicated that allospecific songs were not learned. We describe song development in 41 male and 22 female hand-raised white-crowned sparrows. Thirty males and 15 females were exposed to a live adult singing male. It was found that most male students learned the song of their live tutor even though tutoring was begun at 50 days of age, an age by which young would have dispersed from the natal to the breeding area. Male students learned allospecific song as easily as they did conspecific song, even though conspecific song was present in the laboratory. Only three females copied any part of the song of either conspecific or allospecific live tutors. Six 50-day-old males and seven females were exposed to taperecorded song and none learned the tutor song. These results indicate that there are sex differences in song learning, and that, if live tutors are used, the sensitive phase for male song learning extends beyond 50 days of age. We conclude that social interaction can override any auditory gating mechanism that prevents inappropriate stimuli from influencing song learning centres.     

Song learning and social interaction in indigo buntings

Indigo buntings (Passerina cyanea) isolated as individuals from 60 days of age developed abnormal songs. Birds isolated in groups for 9 to 10 months and then individually isolated developed slightly more normal songs but lacked the adult song figures. Birds copied the songs of adult tutors with whom they interacted socially. Birds with two tutors copied the songs of tutors that they could see and join in supplanting behaviour, but not songs of tutors from which they were visually isolated. One song was transmitted culturally across three generations under experimental conditions. The importance of social factors in song development of yearling buntings explains the development of local groups of males that share songs or dialects with each other in the field.     

The Onset of Song Learning and Song Tutor Selection in Fledgling Zebra Finches

We investigated song development in the pre‐independent zebra finch (aged 15–35 d), a period when neural pathways for song learning and production are forming and social influences outside the family are limited. Expt 1 investigated the onset and the minimum duration of tutoring needed for song learning in fledglings. We found most begin to learn song from 25 d of age and need about 10 d contact with the father tutor to make accurate copies. This onset corresponds with major developments in the formation of the neural circuitry implicated in song acquisition. Subsong also begins on day 25 suggesting that the sensory and motor phases of song learning fully overlap in the zebra finch. Our findings support the hypothesis that the song circuitry is fully functional by 35 d of age and the sensitive phase for zebra finches extends therefore from about days 25–65. However, only the first 10 d of this period are necessary to learn a tutor's song with fair accuracy. Expt 2 investigated the role of the paternal bond, spatial proximity and mating status in a fledgling's choice of song tutor where the father was the sole parent. Young chose the father over single unrelated males (expt 2a) or unrelated males in company with their female partners (expt 2b). Given the close spatial proximity of both potential tutors to the fledglings it is probably the filial bond, established via paternal care that is the cause of this preference. Zebra finches sing the same song phrase in two contrasting contexts: female‐directed song during pre‐copulatory courtship and undirected song where no female or display is involved. In expt 3 we tested the song learning preference of pre‐independent young for two categories of non‐paternal tutors: those singing predominantly female‐directed song and those singing exclusively undirected song. There was a small, but significant, preference for fledgling zebra finches to copy songs from males that sang female‐directed song. This preference is consistent with the hypothesis that young males not only learn the acoustic features of their tutor's song but also the visual and dynamic movements that constitute the courtship display.     

Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches

Male zebra finches normally learn their song from adult models during a restricted period of juvenile development. If song models are not available then, juveniles develop an isolate song which can be modified in adulthood. In this report we investigate the features of juvenile experience that underly the timing of song learning. Juvenile males raised in soundproof chambers or in visual isolation from conspecifics developed stable isolate song. However, whereas visual isolate song notes were similar to those of colony-reared males, soundproof chamber isolates included many phonologically abnormal notes in their songs. Despite having stable isolate songs, both groups copied new notes from tutors presented to them in adulthood (2.7 notes per bird for soundproof chamber isolates, 4.4 notes per bird for visual isolates). Old notes were often modified or eliminated. We infer that social interactions with live tutors are normally important for closing the sensitive period for song learning. Lesions of a forebrain nucleus (IMAN) had previously been shown to disrupt juvenile song learning, but not maintenance of adult song for up to 5 weeks after surgery. In this study, colony-reared adult males given bilateral lesions of IMAN retained all their song notes for up to 4–7.5 months after lesioning. However, similar lesions blocked all song note acquisition in adulthood by both visual and soundproof chamber isolates. Other work has shown that intact hearing is necessary for the maintenance of adult zebra finch song. We infer that auditory pathways used for song maintenance and acquisition differ: IMAN is necessary for auditorily guided song acquisition—whether by juveniles or adults—but not for adult auditorily guided song maintenance. © 1993 John Wiley & Sons, Inc.     

Song learning and mate choice in estrildid finches raised by two species

Male zebra finches, Taeniopygia guttata, and Bengalese finches, Lonchura striata, were raised normally or cross-fostered to the other species until 35 days of age and then housed until 70 days old with two song tutors, one from each species. Males raised normally based their song on that of the conspecific tutor whereas cross-fostered males also learned from the other tutor, reflecting both own-species bias and a tendency to learn from the tutor whose song was similar to the father's. Males raised by one bird from each species learned from the father as well as the tutor(s) but were more likely to learn from the tutor whose song was similar to the father's if the father was a conspecific. Comparing these song learning results with those from male choice tests suggests there is no direct link between song learning and sexual imprinting.     

Addition of song-related neurons in swamp sparrows coincides with memorization, not production, of learned songs

During song learning in birds, neurons are added to some song nuclei and lost from others. Previous studies have been unable to distinguish whether these neural changes are uniquely associated with memorizing a song model (sensory acquisition) or vocal practice (sensorimotor learning). In this study we measured changes in neuron number within song nuclei of swamp sparrows, a species in which the two phases of song learning are nonoverlapping. Male swamp sparrows were collected as hatchlings and tape-tutored from approximately 22 to 62 days of age. Swamp sparrows memorize about 60% of their song material during this period, but do not begin practicing this learned material until approximately 275 days of age. Birds were sacrificed at 23, 41, 61, 71, 274, or 340 days of age. During sensory acquisition, neuron number increased drastically in both the caudal nucleus of the ventral hyperstriatum (HVc) and Area X. The period of sensorimotor learning was not associated with any further changes in neuron number within these regions. We were unable to detect any significant changes in neuron number within the magnocellular nucleus of the neostriatum or the robust nucleus of the archistriatum during either stage of song learning. These results raise the possibility that ongoing addition of HVc and Area X neurons may encourage, and thereby temporally restrict, song acquisition.     

Hatching late in the season requires flexibility in the timing of song learning

Most songbirds learn their songs from adult tutors, who can be their father or other male conspecifics. However, the variables that control song learning in a natural social context are largely unknown. We investigated whether the time of hatching of male domesticated canaries has an impact on their song development and on the neuroendocrine parameters of the song control system. Average age difference between early- and late-hatched males was 50 days with a maximum of 90 days. Song activity of adult tutor males decreased significantly during the breeding season. While early-hatched males were exposed to tutor songs for on average the first 99 days, late-hatched peers heard adult song only during the first 48 days of life. Remarkably, although hatching late in the season negatively affected body condition, no differences between both groups of males were found in song characteristics either in autumn or in the following spring. Similarly, hatching date had no effect on song nucleus size and circulating testosterone levels. Our data suggest that late-hatched males must have undergone accelerated song development. Furthermore, the limited tutor song exposure did not affect adult song organization and song performance.     

Song acquisition in photosensitive and photorefractory male European starlings

We tested the ability of 1-year-old European starlings (Sturnus vulgaris) to acquire songs while in different physiological states. Photorefractory males, with low testosterone levels, learned songs as completely and as accurately as photosensitive males in full reproductive condition. This indicates that song acquisition in 1-year-old males does not depend on high levels of androgens. The ability to learn songs during the nonbreeding season may reflect the high song output of potential tutors through most of the year, including the photorefractory period, and may facilitate increases in song repertoire size in adulthood.     

Statistical and Prosodic Cues for Song Segmentation Learning by Bengalese Finches (Lonchura striata var. domestica)

Juvenile songbirds learn their songs from adults. Birds do not simply learn songs verbatim but they sometimes learn parts of songs from multiple tutors and recombine these into one song sequence. How they segment a particular part and select that as a chunk and how these chunks are recombined are interesting questions to ask, because such segmentation and chunking is also considered to be a basic mechanism in human language acquisition. The song of the Bengalese finch has a complex syntax with variable note‐to‐note transition probabilities and could thus be suitable for the study of segmentation and chunking in birdsong. Thirty‐two male Bengalese finch chicks were reared in a large aviary where 11 adult tutors and 10 adult females were breeding freely. In this environment most male chicks learned songs from several tutors. The song note‐chunks that juveniles copied had higher transition probabilities and shorter silent intervals than did the boundaries of the chunks, suggesting that Bengalese finches segment songs using both statistical and prosodic cues. Thus, the Bengalese finch could prove to be an excellent model in which to study neural and behavioral mechanism for sound segmentation.     

Social influences during song development in the song sparrow: a laboratory experiment simulating field conditions

Oscine songbirds are exposed to many more songs than they keep for their final song repertoire and little is known about how a bird selects the particular song(s) to sing as an adult. We simulated in the laboratory the key variables of the natural song learning environment and examined the song selection process in nine hand-reared male song sparrows, Melospiza melodia, a species in which males sing 5-11 song types. During their second and third months (their presumed sensitive period), subjects were rotated equally among four live adult male tutors that had been neighbours in the field. Tutors were housed in individual aviary 'territories' in four corners of the roof of a building; subjects could see only one tutor at a time, but they could hear the others at a short distance. Later in their first year (months 5-12), half the subjects were again rotated among all four tutors and the other half were randomly stationed next to just one tutor. Results from this experiment confirm and extend the findings from our two previous field studies of song learning in this species. Young males in this experiment (1) learned whole song types, (2) learned songs from multiple tutors, (3) preferentially learned songs that were shared among their tutors, (4) learned songs that other young males in their group also chose, and (5) learned more songs from the tutor they were stationed next to during the later stage (stationary subjects). These last two results support the late influence hypothesis that interactions after a bird's sensitive period affect song repertoire development. Copyright 2000 The Association for the Study of Animal Behaviour.     

Partial muting leads to age‐dependent modification of motor patterns underlying crystallized zebra finch song

The crystallized structure of adult zebra finch (Taeniopygia guttata) song is modifiable if sensory feedback is altered during sound production. Such song plasticity has been studied by examining acoustic modifications to the motif; however, the underlying changes to the vocal motor patterns of these acoustic modifications have not been addressed. Adult birds in two age categories (young = 90–120 days or middle aged 150–250 days) that sang crystallized song were used in the experiment. Vocal motor patterns were monitored by recording respiratory air sac pressure before, during, and after song plasticity was induced by partial or complete reduction of phonation (i.e., “partial muting”). Birds were recorded until changes in air sac pressure patterns underlying the song structure were observed (up to 160 days). Young adult birds were more likely to insert shorter duration (<125 ms) expiratory pulses (EPs) into the motif than middle‐aged adults. These shorter duration EPs were produced with a unique pressure pattern relative to the intact song, and therefore appeared to be generated by novel motor gestures. Stuttering (atypical repetition of an EP) was observed when these novel EPs were inserted into the motif, regardless of age. The EP of the distance call, which is also a learned vocalization in zebra finches, showed a similar reduction in duration if EPs were also shortened in the song. The emergence of shorter duration EPs was not related to sound production, or nonspecific effects of the surgical procedure, which suggests an age‐dependent neural process for song plasticity. © 2004 Wiley Periodicals, Inc. J Neurobiol, 2004     

Song Learning in Song Sparrows: Relative Importance of Autumn vs. Spring Tutoring

We examined ‘late’ song learning in song sparrows (Melospiza melodia), i.e., song learning that occurs after the first few months, or classical sensitive period, of the natal summer. Fledgling juveniles were brought into the laboratory at 2–3 mo of age and exposed to computer‐simulated song tutors in three different time periods: late in the natal summer, the autumn, and the next spring. As expected, the birds’ final repertoires consisted mostly of songs heard in the field, but 30% of the birds’ songs were influenced by songs heard in the laboratory (selective retention) and another 8% were learned de novo in the laboratory. Parallel results were obtained for a second group of birds who received laboratory tutoring only in the spring. In fact, the results suggested that autumn tutoring may even be inhibitory. We conclude that the songs a young song sparrow hears in his first spring may be critical to his final repertoire development, indicating that the song learning process in song sparrows is longer and more flexible than previously supposed.     

Song Learning in Zebra Finches Exposed to a Series of Tutors during the Sensitive Phase

Young male zebra finches exposed to a series of adult males during their sensitive phase for song learning tended to learn from several of them, in contrast to those exposed to two or more tutors simultaneously. There is a tendency to learn more from later tutors, either because the memory of their elements over-writes that of earlier ones or because sensitivity is greater at this stage. No clear relation could be found between features of the song or behaviour of tutors and whether or not they were copied. In common with earlier studies, tutor song output, beyond a certain minimum was found to be unimportant.     

Does leg-ring colour affect song tutor choice in zebra finches?

Young male zebra finches, Taeniopygia guttata, reared by their mothers alone showed no preference between males with red and with light-green colour rings in their choice of song tutor. Behavioural observations showed that the tutee associated more with the adult from which it was subsequently found to have learnt. In a second experiment, birds reared by both parents wearing either light-blue or light-green colour rings and then given a choice of tutors wearing these ring combinations also showed no preference between them. These young males did, however, more often approach the tutor ringed as their parents had been. This may explain why they did not show more interest in the tutor whose song they learnt. The majority of the tutors were used twice, with the ring colour swapped before they were used the second time. There was a strong tendency for the same male to be copied by the two young birds exposed to him. This could not be attributed to a difference in song rate between the two tutors. Further work will be required to discover the basis of that individual's greater attractiveness. Copyright 1999 The Association for the Study of Animal Behaviour.     

Cultural Evolution of Puget Sound White-Crowned Sparrow Song Dialects

The songs of male Puget Sound white‐crowned sparrows currently form about 12 dialects along the Pacific Northwest coast. In his survey of 1970, Baptista (Condor 1977; 79: 356–370) defined six of the dialects based on the song's terminal trill because most males at each locality shared the simple syllables (SSs) in this trill. The complex syllables (CSs) in the song's introduction varied among males at a locality, and were often shared among localities. From 1997 to 2004 we revisited nine of the sites Baptista studied to determine whether the SSs and CSs had changed over the 30‐yr interval. Using Baptista's catalogs of SS and CS types as bases for comparison, we found that the relative proportions of CS types changed significantly more over time than did the proportions of SS types. These results suggest that SSs and CSs evolve independently. Observations were also made on the developmental mechanisms that either produce diversity or maintain uniformity in song phrases. In a survey of 670 field‐recorded songs, unique improvizations occurred significantly more often in CSs than in SSs. In a laboratory experiment using hand‐reared males and multiple song tutors, males were significantly more accurate in imitating SSs than CSs. In choosing their final song to keep from their overproduced repertoire, yearling males tended to retain the song type that matched the SSs in the song played back to them. We conclude by discussing how differences in the functions served by these two song phrases may have led to their different rates of cultural evolution.     

Assessing the Importance of Social Factors in Bird Song Learning: A Test Using Computer-Simulated Tutors

We used a mixed live/synthetic tutoring design to investigate whether the social factors of eavesdropping on adult singing interactions and/or direct interaction with a tutor would influence song learning in song sparrows ( Melospiza melodia ). Males were brought into the laboratory at 4–5 d-old, hand-raised and then tutored by two pairs of adult song sparrows in June and July From January through March of the next year, subjects received tutoring from computer simulations of two of the original live tutors. The first, non-interactive, model simulated one of the earlier tutors singing 'naturalistic' bouts of song with no interaction with the subject. The second, interactive, model simulated a different early tutor that behaved similarly to the non-interactive model, but synchronized its singing with the subject, and tried to match the subject's song. Subjects learned relatively more from their interactive late tutor and his early partner, and showed no tendency to learn more from their late than their early-only tutors. These results support the eavesdropping hypothesis, and also suggest that direct interaction with the tutor is a relevant social factor.     

Age-dependent effects of song exposure: song crystallization sets a boundary between fast and delayed vocal imitation

Song crystallization is a prominent developmental phase of oscine birds in which there is a transition from a production of plastic vocal material to a performance of elaborated song patterns that are typical for adult birds. Here we show that crystallization can be related to a marked change in memory properties involved in supplementary learning of song occurring during this phase. We studied nightingales, Luscinia megarhynchos, a species renowned for its large repertoire of song types. After a period of early tutoring as fledglings, hand-reared subjects (N=8) were exposed to a set of temporally distributed training experiences as juveniles and young adults. Analyses of the birds' singing yielded clear evidence for late song learning and also a striking phase-related shift in their memory properties. New songs heard shortly before crystallization (at an age of 40-42 weeks) were imitated within a few days and their structural and syntactical ‘quality’ seemed not to be inferior to imitations developed from songs heard earlier. In contrast, none of the songs experienced soon after song crystallization (at 45-47 weeks) appeared as imitations in the repertoires of the young adults (at 48-55 weeks). However, birds had clearly memorized these songs, as they produced imitations of them in their second spring. Our findings show that auditory song acquisition in nightingales extends well into the phase of vocal production. At the same time, however, the boundary between an immediate and a delayed form of vocal imitation suggests that song crystallization reflects a marked change in memory properties. That is, song crystallization seems to constrain the ability to develop motor programs for song patterns that are heard even though these are committed to memory. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

白腰文鸟发声行为的神经发育

本文研究了 5～ 15 0日龄雄性白腰文鸟 (Lonchurastriataswinhoei)不同年龄段的声谱变化以及这种变化的神经调制机制。结果如下 :(1)HVC、RA和AreaX三个发声核团的神经联系基本接近成年鸟的水平后 ,幼鸟才开始学习鸣叫 (约 45日龄 ) ;(2 )HVC、RA和AreaX达到成年核团体积时 (约 80日龄 ) ,幼鸟才具有成年雄鸟的鸣叫模式 ;(3)发声控制核团的发育与核团间的神经支配有关 ,而基本不受鸣唱行为的影响 ,HVC、RA和AreaX的最快增长时间段各不相同 ,三个核团随年龄增长而呈现体积增长的显著变化 (one wayANOVA ,P <0 0 5 ) ,但各核团在任意两个时间段的体积差异并不都显著。结果提示 :发声行为产生的时间和发展与发声控制核团的发育、核团间的神经联系有关 ,最终的体积发育程度受内在遗传力的作用 ,同时可能还受神经核团建立正常神经联系时间的影响     

Song Learning in Wild and Domesticated Strains of White‐Rumped Munia,Lonchura striata,Compared by Cross‐Fostering Procedures: Domestication Increases Song Variability by Decreasing Strain‐Specific Bias

Song diversity results from the interactions between natural selection, sexual selection, and individual learning. To understand song diversity, all three factors must be considered collectively, not separately. Bengalese Finches were domesticated about 250 yr ago. Their courtship songs have become different from their ancestor, the White‐rumped Munia. Bengalese Finches sing songs with complex note‐to‐note transition patterns and with acoustically diverse song notes while White‐rumped Munias sing songs with fixed note sequence and mostly broad band song notes. Bengalese Finches were selected for domestication based on their good parenting ability, not their songs, but this artificial selection has nonetheless affected their songs. To test whether divergence occurred not only in the song phenotypes but also in the genetic basis for predisposition of strain specific song learning, we conducted a cross‐fostering experiment between Bengalese Finches and White‐rumped Munias. In both strains, song learning was affected by rearing condition: the acoustical feature and transition patterns followed those of the foster fathers. However, the accuracy of song learning differed between the wild and the domesticated strains: sharing of song note between sons and tutors in Finches was not very accurate regardless of the tutor, while Munias were highly accurate in copying Munia songs but often omitted song elements from Finch fathers. These results suggest that White‐rumped Munias are strongly constrained to learn their own strain’s song, and that this constraint was relaxed in the Bengalese Finch by domestication.