Auditory scene analysis in estrildid finches (Taeniopygia guttata and Lonchura striata domestica): a species advantage for detection of conspecific song

Operant-conditioning techniques were used to investigate the ability of zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) to detect a zebra finch or a Bengalese finch target song intermixed with other birdsongs. Sixteen birds were trained to respond to the presence of a particular target song, either of their own species (n = 8) or of another species (n = 8). The birds were able to learn a discrimination between song mixtures that contained a target song and song mixtures that did not, and they were able to maintain their response to the target song when it was mixed with novel songs. Zebra finches, but not Bengalese finches, learned the discrimination with a conspecific target more quickly and were worse at detecting a Bengalese finch in the presence of a conspecific song. The results indicate that selective attention to birdsongs within an auditory scene is related to their biological relevance.     

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     

Perceptual chunking in the self-produced songs of Bengalese finches (Lonchura striata var. domestica)

Like humans, songbirds, including Bengalese finches, have hierarchical structures in their vocalizations. When humans perceive a sentence, processing occurs in phrase units, not words. In this study, we investigated whether songbirds also perceive their songs by chunks (clusters of song notes) rather than single song notes. We trained male Bengalese finches to react to a short noise in a Go/NoGo task. We then superimposed the noise onto recordings of their own songs and examined whether the reaction time was affected by the location of the short noise, that is, whether the noise was placed between chunks or in the middle of a chunk. The subjects’ reaction times to the noise in the middle of a chunk were significantly longer than those to the noise placed between chunks. This result was not observed, however, when the songs were played in reverse. We thus concluded that Bengalese finches perceive their songs by chunks rather than single notes.     

Sexual communication and domestication may give rise to the signal complexity necessary for the emergence of language: An indication from songbird studies

For language to be a vehicle of thought, protolanguage must develop a degree of complexity that allows for the syntactic manipulation of symbol sequences. Thus, before language emerged, a process in which signals became complex must have occurred. Here, we submit a scenario describing the process in which courtship songs gained in complexity during the course of domestication of Bengalese finches. By comparing domesticated Bengalese finches with their wild strain, white-rumped munias, we found that female preferences for complex songs were coupled with domesticated relaxed environments to give rise to song complexity. Furthermore, we found that the outcomes of domestication in Bengalese finches include decreased psychological and physiological stress reactions, decreased aggressiveness, and changed plumage colors. These characteristics are consistent with “domestication syndrome,” originally proposed for mammals but now possibly applicable to birds. Our finding that domestication was a cause of signal complexity might be helpful in considering the process of signal evolution in human language.     

Significance of visual cues in choice behavior in the female zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis><Emphasis Type="Italic">castanotis</Emphasis>)

Female zebra finches show a preference for male zebra finches over heterospecific males based solely on the auditory cues of males, such as songs. The present study was designed to investigate whether females show a similar preference for male zebra finches based solely on visual cues. Using a Y-maze apparatus, social preference of female zebra finches was studied between male zebra finches and male Bengalese finches in three experiments. In experiment 1, where female zebra finches could see and hear live male zebra finches and male Bengalese finches, the females preferred to associate with the male zebra finches. In experiment 2, using a sound-attenuated experimental apparatus, subjects could see, but not hear, male zebra finches and male Bengalese finches. The subjects did not show a significant preference for associating with zebra finches. In experiment 3, as in experiment 2, females could see live male zebra finches and male Bengalese finches in the sound-attenuated chambers. However, in experiment 3, the subjects also heard prerecorded auditory cues (i.e., songs and calls) of male zebra finches, which were presented simultaneously in both arms of the maze. Although the females could not use the auditory cues to identify the location of the male zebra finches, they preferred to associate with the male zebra finches rather than the male Bengalese finches. These results suggest that visual cues alone were effective in initiating choice behaviors by females and that auditory cues facilitate such visually based choice behaviors. Electronic Publication     

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.     

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.     

Does zebra finch (Taeniopygia guttata) preference for the (familiar) father's song generalize to the songs of unfamiliar brothers?

Several studies have demonstrated that zebra finches (Taeniopygia guttata) prefer their fathers' songs over unfamiliar songs. Songs of tutors (i.e., fathers) and tutees (i.e., sons) resemble each other as a result of cultural transmission. Subjects (N = 18) with a previously established preference for the father's song could choose between the song of an unfamiliar brother or a random unfamiliar song in an operant task. Most subjects showed a significant preference for either category of song, but overall, the songs of unfamiliar brothers were not preferred, although they were more similar to the father's song than were the unfamiliar songs. This suggests that subjects did not generalize their learned preference for a song of a particular tutor to the songs of his tutees.     

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.     

Blockade of NMDA Receptors in the Anterior Forebrain Impairs Sensory Acquisition in the Zebra Finch (Poephila guttata)

Juvenile zebra finches (Poephila guttata) learn song in two stages: during sensory acquisition, they memorize the song of an adult tutor, and during sensorimotor learning, they alter their vocalizations to match the stored song model. Like many other forms of neural plasticity and memory formation, vocal learning in zebra finches is impaired by pharmacological blockade of NMDA receptors, but the relevant NMDA receptors have not yet been localized. During song development, one neural region that has been implicated specifically in song learning, the lMAN, exhibits an increased density of NMDA receptors as well as decreased binding affinity for the NMDA antagonist MK-801. To test the hypothesis that sensory acquisition requires activation of NMDA receptors in or near the lMAN we infused the NMDA receptor antagonist amino-5-phosphonopentanoic acid (AP5; 2.5 μg in 0.1 μl) directly into the anterior forebrain. Birds receiving AP5 infusions prior to each of 10 tutoring sessions copied significantly less of their tutor's song than did sham-operated birds, saline-infused birds, birds that received AP5 infusions on nontutoring days, or birds that received AP5 infusions into the cerebellum. Furthermore, infusions of AP5 in the anterior forebrain did not impair young birds’ ability to discriminate zebra finch from canary song. These findings are consistent with the hypothesis that NMDA receptor activation in the anterior forebrain is necessary for the memorization of song material during avian vocal learning. This is also the first report that song-related regions of the anterior forebrain contribute to sensory acquisition specifically.     

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.     

Relative salience of syllable structure and syllable order in zebra finch song

There is a rich history of behavioral and neurobiological research focused on the ‘syntax’ of birdsong as a model for human language and complex auditory perception. Zebra finches are one of the most widely studied songbird species in this area of investigation. As they produce song syllables in a fixed sequence, it is reasonable to assume that adult zebra finches are also sensitive to the order of syllables within their song; however, results from electrophysiological and behavioral studies provide somewhat mixed evidence on exactly how sensitive zebra finches are to syllable order as compared, say, to syllable structure. Here, we investigate how well adult zebra finches can discriminate changes in syllable order relative to changes in syllable structure in their natural song motifs. In addition, we identify a possible role for experience in enhancing sensitivity to syllable order. We found that both male and female adult zebra finches are surprisingly poor at discriminating changes to the order of syllables within their species-specific song motifs, but are extraordinarily good at discriminating changes to syllable structure (i.e., reversals) in specific syllables. Direct experience or familiarity with a song, either using the bird’s own song (BOS) or the song of a flock mate as the test stimulus, improved both male and female zebra finches’ sensitivity to syllable order. However, even with experience, birds remained much more sensitive to structural changes in syllables. These results help to clarify some of the ambiguities from the literature on the discriminability of changes in syllable order in zebra finches, provide potential insight on the ethological significance of zebra finch song features, and suggest new avenues of investigation in using zebra finches as animal models for sequential sound processing.     

Sexual dimorphism of auditory activity in the zebra finch song system

While the tracheosyringeal motor neurons of anesthetized male zebra finches fire in response to acoustic stimuli, the same motor neurons in females show no such response. Females masculinized by estradiol implants on Days 1 or 2 after hatching may develop auditory responses in their tracheosyringeal motor neurons; the presence of the response is directly related to the degree of masculinization of the estradiol-treated females' telencephalic song centers. In male zebra finches, neurons in HVc (Hyperstriatum Ventrale pars caudalis) respond to sound, and the HVc is necessary for the tracheosyringeal auditory response. Multiunit auditory activity was demonstrated in the HVc of female zebra finches. A single 20-microA pulse delivered to the male HVc elicits a large volley in the tracheosyringeal nerve; microstimulating the female HVc does not evoke a response in the motor nerve. This failure of both auditory and HVc stimulation to elicit a response in the female tracheosyringeal nerve is attributed to the lack of a functional HVc-nucleus Robustus Archistriatalis projection in females. If, as has been suggested, the tracheosyringeal auditory response may be important for the processing of song, female zebra finches might not process song in the same manner as do males.     

Experimental determination of a unit of song production in the zebra finch (Taeniopygia guttata)

Zebra finch (Taeniopygia guttata) song is composed of syllables delivered in a set order. Little is known about the program that controls this temporal delivery. A decision to sing or not to sing may or may not affect the entire song. Song, once commenced, may continue or may halt. If song is halted, stops may occur only at certain points. Seven zebra finches were presented with short bursts of strobe light while engaged in song. The variables of interest were whether the birds stopped and where they stopped. The results can be summarized as follows: Ongoing zebra finch song can be interrupted, interruptions occur at discrete locations in song, and the locations almost always fall between song syllables. These results reveal a functional representation of song production and place constraints on possible neural mechanisms that underlie song production in zebra finches and probably other oscine species. The results also raise hypotheses about the elements of song perception and memory.     

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.     

Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch

Area X, a large sexually dimorphic nucleus in the avian ventral forebrain, is part of a highly discrete system of interconnected nuclei that have been implicated in either song learning or adult song production. Previously, this nucleus has been included in the song system because of its substantial connections with other vocal control nuclei, and because its volume is positively correlated with the capacity for song. In order to directly assess the role of Area X in song behavior, this nucleus was bilaterally lesioned in both juvenile and adult zebra finches, using ibotenic acid. We report here that lesioning Area X disrupts normal song development in juvenile birds, but does not affect the production of stereotyped song by adult birds. Although juvenile-lesioned birds were consistently judged as being in earlier stages of vocal development than age-matched controls, they continued to produce normal song-like vocalizations. Thus, unlike the lateral magnocellular nucleus of the anterior neostriatum, another avian forebrain nucleus implicated in song learning, Area X does not seem to be necessary for sustaining production of juvenile song. Rather, the behavioral results suggest Area X is important for either the acquisition of a song model or the improvement of song through vocal practice.     

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.     

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.     

Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches.

Although songbirds rely on auditory input for normal song development, many species eventually attain adult song patterns that are thought to be maintained without reference to auditory feedback. In such species, it is believed that a central motor program for song is established when the stereotyped adult song pattern is achieved. However, we report here that in the Australian zebra finch, stereotyped song patterns gradually change in adult males following bilateral cochlear removal. By 16 weeks after surgery, deaf birds accurately reproduced only 36% of the song syllables produced prior to surgery. Moreover, on average, the phonology of over 50% of the syllables produced by deaf birds was either only slightly similar or unlike the phonology of any syllable produced prior to surgery. In contrast, control birds accurately retained over 90% of their syllables over a comparable time period and less than 5% of their syllables was unmatched or only slightly similar in phonology to previously recorded syllables. In many of the deafened birds, changes in song patterns were not evident until 6-8 weeks after surgery. These data indicate that continued auditory input is necessary to maintain the patterns of neural organization supporting learned song in zebra finches and raise questions concerning the neural sites and cellular mechanisms that mediate this feedback control.