Song repertoire development in male cowbirds (Molothrus ater): its relation to female assessment of song potency

Two studies were conducted to investigate the relation between the male cowbird's (Molothrus ater ater) development of a song repertoire and the female cowbird's assessment of song potency. Male development was assayed by vocal copying and female assessment by copulatory responsiveness to song playback. The results demonstrate that males do not copy most often the particular songs that females respond to most often. Whereas rank orderings of potency were highly correlated across two independent samples of playback females, male and female rank orderings were not significantly correlated. The data highlight the potential significance of social interactions between and across the sexes for repertoire development.     

Factors influencing song development in the white-crowned sparrow (Zonotrichia leucophrys)

Nestling white-crowned sparrows (Zonotrichia leucophrys nuttalli) were hand-reared in sound-isolation chambers under a variety of conditions. The songs of total isolates were compared with songs of birds tutored with song, and the number of inputs sufficient for a bird to produce a normal song was explored. The flexibility of the song learning system was investigated with a range of tape-recorded tutor songs: alien dialects, alien subspecies, alien species, alternating alien dialects, and an aberrant song. Adult songs were obtained for 40 males and 7 testosterone-injected females. All of the tutor songs could be learned. Also, some birds learned elements of an alien species' song. Birds tutored with two songs copied one or the other, were bilingual, or sang a hybrid of the two. No bird presented with fewer than 120 songs learned the tutor song; 2 birds tutored with 252 songs copied the tutor song. It is concluded that the song learning system is quite flexible, hat the results obtained with tape-tutors are very different from those with social tutors, and that there may be an interaction between total number of song inputs and the number presented on a single day. Some implications of these data for physiological mechanisms and the possible functional significance of the acquisition system are discussed.     

Song learning and cognitive ability are not consistently related in a songbird

Learned aspects of song have been hypothesized to signal cognitive ability in songbirds. We tested this hypothesis in hand-reared song sparrows (Melospiza melodia) that were tutored with playback of adult songs during the critical period for song learning. The songs developed by the 19 male subjects were compared to the model songs to produce two measures of song learning: the proportion of notes copied from models and the average spectrogram cross-correlation between copied notes and model notes. Song repertoire size, which reflects song complexity, was also measured. At 1 year of age, subjects were given a battery of five cognitive tests that measured speed of learning in the context of a novel foraging task, color association, color reversal, detour-reaching, and spatial learning. Bivariate correlations between the three song measures and the five cognitive measures revealed no significant associations. As in other studies of avian cognition, different cognitive measures were for the most part not correlated with each other, and this result remained true when 22 hand-reared female song sparrows were added to the analysis. General linear mixed models controlling for effects of neophobia and nest of origin indicated that all three song measures were associated with better performance on color reversal and spatial learning but were associated with worse performance on novel foraging and detour-reaching. Overall, the results do not support the hypothesis that learned aspects of song signal cognitive ability.     

Cross-fostering diminishes song discrimination in zebra finches (Taeniopygia guttata)

Song-production, -discrimination, and -preferences in oscine birds are dually influenced by species identity and the ontogenetic environment. The cross-fostering of a model species for recognition research, the zebra finch (Taeniopygia guttata) into heterospecific nests of the Bengalese finch (Lonchura striata vars. domestica) allows an exploration of the sensory limits of early development and the effects of species-specific acoustic cues upon song discrimination in adulthood. To quantify the song preferences of female and male normal-reared (control) and Bengalese finch fostered zebra finches, we recorded multiple behavioral measures, including spatial proximity, vocalization rates and response latency, during sequential song-playback choice-trials using both tutor species’ songs and the songs of two other ecologically relevant Australian species, the owl finch (Taeniopygia bichenovii) and the star finch (Neochmia ruficauda). Response strength was variable between the different measures, but no differences were detected within the specific behavioral responses towards the song playbacks of the two sexes. Control subjects strongly preferred their own species’ songs while Bengalese-fostered zebra finches exhibited reduced song discrimination between con-, tutor-, and heterospecific songs. Overall behavioral responsiveness was also modulated by social ontogeny. These results indicate a difference in the strength of preference for song that is dependent on the species identity of the rearing environment in oscine birds and illustrate the role of multiple behavioral measures and ecologically relevant stimulus species selection in behavioral research using zebra finches.     

Influence of social conditions in song sharing in the adult canary

In songbirds, experience of social and environmental cues during a discrete period after birth may dramatically influence song learning. In the canary, the ability to learn new songs is assumed to persist throughout life. The aim of the present study was to investigate whether social context could guide changes in adult song. Three groups of canaries were kept in different social and temporal conditions. Results showed that the multiple hierarchical levels of the canary song structure were affected by social environment: songs of males housed together for 2 years were more similar than those of males that spent the same time in individual cages in regard to acoustic parameters, syllable repertoire and repertoire of sequences of two-syllable types. However, social housing did not result in the emergence of a group-specific vocal signature within songs. In conclusion, these results suggested that under the influence of social factors, a copying process could allow adult canaries to adjust, at least in part, their songs to those of other individuals.     

Song syllable discrimination by song sparrows (Melospiza melodia)

A habituation test paradigm was used to examine the responses of free-living territorial adult male song sparrows (Melospiza melodia) to a range of synthetic songs. The three-phrased test songs differed from one another in having either conspecific or heterospecific (swamp sparrow, M. georgiana) syllables, or silence, in the second phrase. Subjects were exposed to repeated presentations of one song type until their approach distance to a loudspeaker increased. In one experiment, birds were habituated with a song consisting of three phrases of song sparrow syllables and then tested for generalization to either novel song sparrow syllables in the second phrase, swamp sparrow syllables, or silence. Birds discriminated between song sparrow syllables on two response measures, and between song sparrow and swamp sparrow syllables on one measure. In a second experiment, after habituation to a song with swamp sparrow syllables in the second phrase, birds did not generalize to novel song sparrow syllables, but they did generalize to novel swamp sparrow syllables. Thus song sparrows make finer distinctions among conspecific syllable variants than with alien syllables. The results further suggest that subtle species-specific differences in note structure within syllables are discriminated by song sparrows and potentially provide an adequate basis for individual recognition by song.     

Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches (Taeniopygia guttata)

Zebra finches communicate via several distinct vocalizations, of which song is the most studied. Behavioral observations indicate that adults are able to discriminate among the songs of different conspecific individuals. In the wild, zebra finches live in structured but mobile colonies, and encounter new individuals on a frequent basis. Thus it seems plausible that adult finches might have the capacity to recognize and remember new songs they encounter on a single day, but this has never been directly tested. Here we devised a simple observational assay to determine whether adult male zebra finches show recognition of a song they have heard repeatedly from taped playbacks, over a single three hour period the day before. We quantified the rate of production of six discrete behaviors (short calls, contact calls, singing, short hops, long hops, and beak swipes) made by adult male zebra finches as they listened to the playbacks. At the onset of song playback, all birds suspended these behaviors and sat silently-occasionally moving their heads. Then, after a measurable period ("response latency"), the birds resumed these activities. We observed that the response latency was long (approximately 10 min) when birds were hearing a particular song for the first time. The response latency was much shorter (approximately 1-2 min) when the birds had heard the same song the day before. Thus, functional song memories must result from as little as 3 h of passive song-exposure. These results suggest that ongoing song learning may play a natural role in the daily life of adult zebra finches, and provide a behavioral reference point for studies of molecular and physiological plasticity in the adult auditory system.     

Song sequence discrimination in the black-capped chickadee (Parus atricapillus)

Captive black-capped chickadees (Parus atricapillus) were presented with normal and altered versions of their species-specific "fee bee" song, to determine how note type, number, and sequence affect recognition. The number of perch changes and vocalizations (analyzed separately) given in response to playback did not differ reliably as a function of song type, whereas latency to first vocalization after playback did. In an initial experiment using two-note songs, birds vocalized sooner to songs beginning with fee than with bee and to fee bee than to fee fee. In a second experiment, birds were presented with shortened (single note), normal, and lengthened (three note) songs each consisting of a single-note type (either fee or bee). Habituation slowed responding to altered songs but not to fee bee over three test sessions. Results from the first session suggest that chickadees distinguished single fees and three-note songs from normal song, single fees from single bees, and two-note songs from three-note songs. Results from the third session suggested that chickadees distinguished normal song from any of the altered songs. The internal representation of conspecific song in the chickadee thus distinguishes between fee and bee notes, contains information about note order, and is sensitive to note number. The pattern of responses is consistent with a model of recognition based on note-by-note integration of individual decisions about song structure.     

Timbre control in zebra finch (Taeniopygia guttata) song syllables

Zebra finch (Taeniopygia guttata) song syllables often include harmonically related frequency components. These harmonics may be suppressed, and this differential emphasis varies between the syllables in a song and between individual birds' songs. These patterns of harmonic suppression are timbre. Individual syllables' patterns of harmonic suppression are constant with adult males' songs. Young males that imitate the songs of older males also imitate their patterns of harmonic suppression. Syringeal denervation distorts these patterns, which suggests that they are produced through active control of the vocal organ. The selective suppression and emphasis of some harmonics creates a great number of possible timbre variants for any one syllable. These add signal diversity to the limited array of frequency modulations and range of fundamental frequencies found in zebra finch song. Analyses of bird song that disregard timbre may overlook a feature that is important in vocal communication.     

Social metrics of song learning

Five metrics of song learning are described for brown-headed cowbirds (Molothrus ater). The intent of these metrics is to capture not only the behavior of the song learner but the social context in which song learning occurs. Playback procedures, observations of mating, and acoustic and functional assessment of song content are combined to yield measures of song potency, functional validity, social dynamics, vocal flexibility, and social reactivity. Taken as a whole, the results revealed by these metrics indicate that males learn to be effective singers by attending to the social consequences of their behavior.     

Song perception during the sensitive period of song learning in zebra finches (Taeniopygia guttata)

The sensitive period is a special time for auditory learning in songbirds. However, little is known about perception and discrimination of song during this period of development. The authors used a go/no-go operant task to compare discrimination of conspecific song from reversed song in juvenile and adult zebra finches (Taeniopygia guttata), and to test for possible developmental changes in perception of syllable structure and syllable syntax. In Experiment 1, there were no age or sex differences in the ability to learn the discrimination, and the birds discriminated the forward from reversed song primarily on the basis of local syllable structure. Similar results were found in Experiment 2 with juvenile birds reared in isolation from song. Experiment 3 found that juvenile zebra finches could discriminate songs on the basis of syllable order alone, although this discrimination was more difficult than one based on syllable structure. The results reveal well-developed song discrimination and song perception in juvenile zebra finches, even in birds with little experience with song.     

Syllable chunking in zebra finch (Taeniopygia guttata) song.

We examined how 61 young zebra finch (Taeniopygia guttata) males copied song from 5 adult tutors. Zebra finch song consists of a string of 5-15 distinct syllables, and these syllables were copied as chunks, or strings of consecutive syllables (modal length = 3). The silent interval between 2 syllables was copied as part of the syllable after the silence. Copied chunks had boundaries that fell at consistent locations within the tutor's song, marked by a relatively long intersyllable silent period, a transition between call-like and noncall-like syllables, and a tendency for the tutor male to stop his song short. Young males also tended to break their songs off at the boundaries of the chunks they had copied. Chunks appear to be an intermediate level of hierarchy in song organization and to have both perceptual (syllables were learned as part of a chunk) and motor (song delivery was broken almost exclusively at chunk boundaries) aspects.     

Age-based discrimination of rival males in western bluebirds

Adaptive social behavior frequently involves discriminating between classes of individuals such as relatives versus non-relatives, older versus younger individuals, or individuals of different status. In the absence of spatial cues, this discrimination may be based on signals that correlate with fitness-related traits (e.g., older or high-status males may sing higher performance songs) or with identity, for example, when receivers distinguish and classify signalers based on their unique signal structure. Here, we examine vocal age-based discrimination in western bluebirds (Sialia mexicana), a North American songbird in which older males have a significant advantage in obtaining extra-pair fertilizations, and therefore pose a significantly higher threat to paternity than younger males. We asked whether western bluebird males showed a higher response to playback of songs of older males compared to younger males relative to their own age. We prepared song stimuli by removing three potential signals of age that have been identified as important in other species: (1) note consistency (which was achieved by playing a single instance of each note repeatedly), (2) note repertoire size, and (3) singing rate (the latter two were equalized across conditions). Even in the absence of these potential signals of age, young males responded more strongly to playback of older males’ songs than to young males’ songs, suggesting that they are able to discriminate between age classes relative to the threat they pose. Further research is required to determine whether this discrimination is based on individual recognition or signal features that are correlated with age.     

Left-side dominance for song discrimination in Bengalese finches (Lonchura striata var. domestica)

Male Bengalese finches are left-side dominant for the motor control of song in the sensorimotor nucleus (the high vocal center, or HVc) of the telencephalon. We examined whether perceptual discrimination of songs might also be lateralized in this species. Twelve male Bengalese finches were trained by operant conditioning to discriminate between a Bengalese finch song and a zebra finch song. Before training, the left HVc was lesioned in four birds and the right HVc was lesioned in four other birds. The remaining four birds were used as controls without surgery. Birds with a left HVc lesion required significantly more time to learn to discriminate between the two songs than did birds with a right HVc lesion or intact control birds. These results suggest that the left HVc is not only dominant for the motor control of song, but also for the perceptual discrimination of song. Accepted after revision: 11 September 2001 Electronic Publication     

Direct social contacts override auditory information in the song-learning process in starlings (Sturnus vulgaris)

Social influence on song acquisition was studied in 3 groups of young European starlings raised under different social conditions but with the same auditory experience of adult song. Attentional focusing on preferred partners appears the most likely explanation for differences found in song acquisition in relation to experience, sex, and song categories. Thus, pair-isolated birds learned from each other and not from broadcast live songs, females did not learn from the adult male tutors, and sharing occurred more between socially associated peers. On the contrary, single-isolated birds clearly copied the adult songs that may have been the only source of attention stimulation. Therefore, social preference appears as both a motor for song learning and a potential obstacle for acquisition from nonpreferred partners, including adults.     

Multiple levels of representation of song by European starlings (Sturnus vulgaris): open-ended categorization of starling song types and differential forgetting of song categories and exemplars

Four European starlings (Sturnus vulgaris) were trained to discriminate among conspecific and heterospecific song segments in a go/no-go operant task. In Experiment 1, the starlings discriminated among novel starling and heterospecific songs, indicating an open-ended category of conspecific song types. The starlings also showed excellent memory for reinforced conspecific songs and discriminated among subordinate categories of conspecific song. In Experiment 2, the starlings were presented with the song segments from Experiment 1 after an 8-month delay period. The starlings retained the discrimination between conspecific and heterospecific songs but not among conspecific songs. The starlings also retained memory for individual singers over the 8-month delay. Starlings categorize song at the level of species, and at subordinate categories of song types, and may have superior long-term retention of song categories relative to song exemplars.     

Experience with songs in adulthood reduces song-induced gene expression in songbird auditory forebrain

Male songbirds learn to produce song within a limited phase early in life; however they continue to learn to recognize songs in adulthood. Studies looking at Zenk activation after exposure to songs learned early in life for song production and songs learned in adulthood show opposite patterns of activation, suggesting distinct neural mechanisms may be involved in these two forms of learning. In this study, we look at IEG Zenk activation in auditory regions NCM and CMM of song sparrows (Melospiza melodia) to see whether recent exposure to song in adulthood leads to greater or decreased Zenk activation upon hearing that song versus a novel song. We found significantly lower activation in birds exposed to previously heard songs versus novel songs in vNCM but not dNCM, though further analysis suggest an overall trend in NCM. We found no significant difference in the amount of activation to previously heard songs vs. novel songs in CMM. These results support previous findings suggesting that activation is reduced to learned stimuli; we discuss possible implications of these findings in relation to song production learning early in life and song recognition learning in adulthood.     

Amplitude modulation of sexy phrases is salient for song attractiveness in female canaries (Serinus canaria)

Song discrimination and recognition in songbird species have usually been studied by measuring responses to song playbacks. In female canaries, Serinus canaria, copulation solicitation displays (CSDs) are used as an index of female preferences, which are related to song recognition. Despite the fact that many studies underline the role of song syntax in this species, we observed that short segments of songs (a few seconds long) are enough for females to discriminate between conspecific and heterospecific songs, whereas such a short duration is not sufficient to identify the syntax rules. This suggests that other cues are salient for song recognition. In this experiment, we investigated the influence of amplitude modulation (AM) on the responses (CSDs) of female canaries to song playbacks. We used two groups of females: (1) raised in acoustic isolation and (2) raised in normal conditions. When adult, we tested their preferences for sexy phrases with different AMs. We broadcast three types of stimuli: (1) songs with natural canary AM, (2) songs with AM removed, or (3) song with wren Troglodytes troglodytes AM. Results indicate that female canaries prefer and have predispositions for a song type with the natural canary AM. Thus, this acoustic parameter is a salient cue for song attractiveness.     

Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus

In our search for relations between vocal learning and neuron structure in the song control nuclei of songbird forebrains, we tested whether differential experience that leads to differences in adult song repertoire would affect dendritic spine density in HVc (also called high vocal center) and RA (robustus archistriatalis). We tape-tutored juvenile Eastern marsh wrens (Cistothorus palustris) with either 5 or 45 song types. As adults, the small repertoire group had learned mostly 5 or 6 song types, and the large repertoire group had learned 36 to 47. Wrens that learned the large song repertoires had a greater dendritic spine density for the most spiny neurons present in HVc (mean difference, 36%), but not in RA. Recent physiological evidence describes HVc as a premotor area coding syllables, motifs, and higher-order song patterns, and our data now clearly reveal that differences in the size of the song repertoire that is experienced lead to differences both in song learning and in the density of dendritic spines in HVc. In the forebrain song nuclei of these songbirds, as in some other vertebrate systems, differences in learning and performance are associated with differences in synaptic anatomy specifically in the region that organizes the learned pattern.