Auditory temporal pattern learning by songbirds using maximal stimulus diversity and minimal repetition

The sequential patterning of complex acoustic elements is a salient feature of bird song and other forms of vocal communication. For European starlings (Sturnus vulgaris), a songbird species, individual vocal recognition is improved when the temporal organization of song components (called motifs) follows the normal patterns of each singer. This sensitivity to natural motif sequences may underlie observations that starlings can also learn more complex, unnatural motif patterns. Alternatively, it has been proposed that the apparent acquisition of abstract motif patterning rules instead reflects idiosyncrasies of the training conditions used in prior experiments. That is, that motif patterns are learned not by recognizing differences in temporal structures between patterns, but by identifying serendipitous features (e.g., acoustical cues) in the small sets of training and testing stimuli used. Here, we investigate this possibility, by asking whether starlings can learn to discriminate between two arbitrary motif patterns, when unique examples of each pattern are presented on every trial. Our results demonstrate that abstract motif patterning rules can be acquired from trial-unique stimuli and suggest that such training leads to better pattern generalization compared with training with much smaller stimulus subsets.     

Stimulus-dependent flexibility in non-human auditory pitch processing

Songbirds and humans share many parallels in vocal learning and auditory sequence processing. However, the two groups differ notably in their abilities to recognize acoustic sequences shifted in absolute pitch (pitch height). Whereas humans maintain accurate recognition of words or melodies over large pitch height changes, songbirds are comparatively much poorer at recognizing pitch-shifted tone sequences. This apparent disparity may reflect fundamental differences in the neural mechanisms underlying the representation of sound in songbirds. Alternatively, because non-human studies have used sine-tone stimuli almost exclusively, tolerance to pitch height changes in the context of natural signals may be underestimated. Here, we show that European starlings, a species of songbird, can maintain accurate recognition of the songs of other starlings when the pitch of those songs is shifted by as much as ±40%. We observed accurate recognition even for songs pitch-shifted well outside the range of frequencies used during training, and even though much smaller pitch shifts in conspecific songs are easily detected. With similar training using human piano melodies, recognition of the pitch-shifted melodies is very limited. These results demonstrate that non-human pitch processing is more flexible than previously thought and that the flexibility in pitch processing strategy is stimulus dependent.     

Working memory for patterned sequences of auditory objects in a songbird

The capacity to remember sequences is critical to many behaviors, such as navigation and communication. Adult humans readily recall the serial order of auditory items, and this ability is commonly understood to support, in part, the speech processing for language comprehension. Theories of short-term serial recall posit either use of absolute (hierarchically structured) or relative (associatively structured) position information. To date, neither of these classes of theories has been tested in a comparative auditory model. European starlings, a species of songbird, use temporally structured acoustic signals to communicate, and thus have the potential to serve as a model system for auditory working memory. Here, we explore the strategies that starlings use to detect the serial order of ecologically valid acoustic communication signals and the limits on their capacities to do so. Using a two-alternative choice operant procedure, we demonstrate that starlings can attend to the serial ordering of at least four song elements (motifs) and can use this information to classify differently ordered sequences of motifs. Removing absolute position cues from sequences while leaving relative position cues intact, causes recognition to fail. We then show that starlings can, however, recognize motif-sequences using only relative position cues, but only under rigid circumstances. The data are consistent with a strong learning bias against relative position information, and suggest that recognition of structured vocal signals in this species is inherently hierarchical.     

Integration of melody and text in memory for songs

Two experiments examined whether the memory representation for songs consists of independent or integrated components (melody and text). Subjects heard a serial presentation of excerpts from largely unfamiliar folksongs, followed by a recognition test. The test required subjects to recognize songs, melodies, or texts and consisted of five types of items: (a) exact songs heard in the presentation; (b) new songs; (c) old tunes with new words; (d) new tunes with old words; and (e) old tunes with old words of a different song from the same presentation (‘mismatch songs’). Experiment 1 supported the integration hypothesis: Subjects' recognition of components was higher in exact songs (a) than in songs with familiar but mismatched components (e). Melody recognition, in particular, was near chance unless the original words were present. Experiment 2 showed that this integration of melody and text occurred also across different performance renditions of a song and that it could not be eliminated by voluntary attention to the melody.     

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.     

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.     

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.     

成年雄性斑胸草雀高级发声中枢鸣声控制的右侧优势

鸣禽是研究语言功能的动物模型。鸣禽端脑的高级发声中枢(high vocal center, HVC)与人类布洛卡氏区具有功能同源性。利用电损毁与声谱分析相结合的方法, 对成年雄性斑胸草雀两侧HVC分别进行电损毁, 观察HVC控制鸣声的侧别差异。结果表明, 损毁左侧HVC对长鸣和鸣曲的频域和声强特征均无显著性影响。损毁右侧HVC导致长鸣的振幅、调频、幅度调制显著减小(p < 0.05), 鸣曲的振幅、平均频率、峰频率显著减小(p < 0.05)。损毁双侧HVC后均引起鸣曲时域特征的改变, 暗示鸣曲时域特征的编码需要两侧半球鸣唱系统的整合。HVC在控制鸣声频域和声强特征上具有右侧优势, 但对鸣曲时域特征的控制需要两侧HVC的共同参与。     

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.     

Song copying by humpback whales: themes and variations

Male humpback whales (Megaptera novaeangliae) produce long, structured sequences of sound underwater, commonly called songs. Humpbacks progressively modify their songs over time in ways that suggest that individuals are copying song elements that they hear being used by other singers. Little is known about the factors that determine how whales learn from their auditory experiences. Song learning in birds is better understood and appears to be constrained by stable core attributes such as species-specific sound repertoires and song syntax. To clarify whether similar constraints exist for song learning by humpbacks, we analyzed changes over 14 years in the sounds used by humpback whales singing in Hawaiian waters. We found that although the properties of individual sounds within songs are quite variable over time, the overall distribution of certain acoustic features within the repertoire appears to be stable. In particular, our findings suggest that species-specific constraints on temporal features of song sounds determine song form, whereas spectral variability allows whales to flexibly adapt song elements.Electronic Supplementary Material Supplementary material is available for this article at .     

Perception of warble song in budgerigars (Melopsittacus undulatus): evidence for special processing

The long, rambling warble song of male budgerigars is composed of a large number of acoustically complex elements uttered in streams lasting minutes a time and accompanied by various courtship behaviors. Warble song has no obvious sequential structure or patterned repetition of elements, raising questions as to which aspects of it are perceptually salient, whether budgerigars can detect changes in natural warble streams, and to what extent these capabilities are species-specific. Using operant conditioning and a psychophysical paradigm, we examined the sensitivity of budgerigars, canaries, and zebra finches to changes in long (>6?min) natural warble sequences of a male budgerigar. All three species could detect a single insertion of pure tones, zebra finch song syllables, budgerigar contact calls, or warble elements from another budgerigar’s warble. In each case, budgerigars were more sensitive to these changes than were canaries or finches. When warble elements from the ongoing warble stream were used as targets and inserted, out of order, into the natural warble stream so that the only cue available was the violation of the natural ordering of warble elements, only budgerigars performed above chance. When the experiment was repeated with all the ongoing warble stream elements presented in random order, the performance of budgerigars fell to chance. These results show species-specific advantages in budgerigars for detecting acoustic changes in natural warble sequences and indicate at least a limited sensitivity to sequential rules governing the structure of their species-specific warble songs.     

Changes in stereotyped central motor patterns controlling vocalization are induced by peripheral nerve injury.

Adult male zebra finches (Taeniopygia guttata), as closed-ended learners, normally crystallize their songs at 90 days of age, and the song remains fixed throughout life (Price, 1979). We show that injuring the tracheosyringeal nerve(s) (each of which innervates the ipsilateral half of the syrinx, the avian vocal organ) results in a short-term deficit in the syllables forming adult male song; this deficit disappears after ts nerve regeneration. However, when adult males were followed for a period of several weeks after unilateral tracheosyringeal nerve injury, long-term changes occurred in the temporal patterning of song. Syllables were deleted, remaining portions of the song were linked, and new syllables were added. Syllables with call-like morphology were less likely to be deleted from and more likely to be added to the song. Deletions were most often contiguous chunks of syllables. Changes in the temporal patterning of song occurred during specific periods following nerve injury, were completed within 100 days after nerve transection, and were not dependent upon regeneration of the ts nerve. The resulting newly formed song patterns were stable, remaining unchanged up to 1 year later. The ability of adult male zebra finches to make specific types of changes to crystallized song indicates that some form of vocal plasticity remains even after song learning is completed, though this plasticity may be restricted to a subset of song characteristics. The limitations on the types of changes that are possible may reflect how song is centrally organized.     

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.     

Name that tune: Identifying popular recordings from brief excerpts

We tested listeners’ ability to identify brief excerpts from popular recordings. Listeners were required to match 200- or 100-msec excerpts with the song titles and artists. Performance was well above chance levels for 200-msec excerpts and poorer but still better than chance for 100-msec excerpts. Performance fell to chance levels when dynamic (time-varying) information was disrupted by playing the 100-msec excerpts backward and when high-frequency information was omitted from the 100-msec excerpts; performance was unaffected by the removal of low-frequency information. In sum, successful identification required the presence of dynamic, high-frequency spectral information.     

From central pattern generator to sensory template in the evolution of birdsong

Central nervous networks, be they a part of the human brain or a group of neurons in a snail, may be designed to produce distinct patterns of movement. Central pattern generators can account for the development and production of normal vocal signals without auditory feedback in non-songbirds. Songbirds need auditory feedback to develop and maintain the normal song of their species. The prerequisite for the use of auditory feedback for the control of song is a set of acoustic criteria or a template to which voice must match. The template method perhaps evolved to free birds from fixed central pattern generators, resulting in the evolution of diverse and complex songs among oscine songbirds. The evolution of human speech may have followed a similar course.     

Temporal Induction of Missing Birdsong Segments in European Starlings

Four European starlings (Sturnus vulgaris) discriminated a 300-ms segment of starling song from a 300-ms segment of budgerigar song in three contexts in a two-choice key-peck operant discrimination task. In the starling-song context, on each trial, one of the song segments was presented in the context of starling song; in the budgerigar-song context, the segments were presented in the context of budgerigar song. In the no-song context, the song segments were presented outside of a song context. On occasional unreinforced probe trials, the song segments were replaced by either white noise or silence. On noise trials in the two song contexts, but not on silent trials in the song contexts or noise trials in the no-song context, the starlings were significantly more likely to respond to the key associated with the starling song segment than to the key associated with the budgerigar song segment. This effect was especially pronounced in the starling-song context. The results indicate that noise induces perceptual restoration of missing birdsong segments in songbirds.     

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     

Effect of acoustic cue modifications on evoked vocal response to calls in zebra finches (Taeniopygia guttata)

Besides their song, which is usually a functionally well-defined communication signal with an elaborate acoustic structure, songbirds also produce a variety of shorter vocalizations named calls. While a considerable amount of work has focused on information coding in songs, little is known about how calls' acoustic structure supports communication processes. Because male and female zebra finches use calls during most of their interactions and answer to conspecific calls without visual contact, we aimed at identifying which calls' acoustic cues are necessary to elicit a vocal response. Using synthetic zebra finch calls, we examined evoked vocal response of male and female zebra finches to modified versions of the distance calls. Our results show that the vocal response of zebra finches to female calls requires the full harmonic structure of the call, whereas the frequency downsweep of male calls is necessary to evoke a vocal response. It is likely that both female and male calls require matching a similar frequency bandwidth to trigger a response in conspecific individuals.     

Song recognition in zebra finches: Are there sensitive periods for song memorization?

Male zebra finches learn to sing songs that they hear between 25 and 65 days of age, the sensitive period for song learning. In this experiment, male and female zebra finches were exposed to zebra finch songs either before (n = 9) or during (n = 4) the sensitive period. Following song exposure, recognition memory for the songs was assessed with an operant discrimination between familiar and novel songs. Zebra finches that were exposed to songs between 22 and 30 days of age discriminated between familiar and novel songs; zebra finches exposed to songs from 9 to 17 days of age did not. Failure to memorize songs heard prior to the sensitive period may contribute to the exclusion of those songs from the repertoire of songbirds.     

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.