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.     

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.     

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.     

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 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.     

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.     

Timbre discrimination in zebra finch (Taeniopygia guttata) song syllables

Zebra finch (Taeniopygia guttata) songs include syllables of a fundamental frequency and harmonics. Individual harmonics in 1 syllable can be more or less emphasized. The functional role of this variability is unknown. These experiments provide evidence of how the phenomenon is perceived. We trained 12 male and female zebra finches on a go-no-go operant procedure to discriminate between 2 song syllables that varied only in the absence of the 2nd or 5th harmonic. Training involved many thousands of trials. Both sexes used the presence or absence of the 2nd harmonic as the sole discriminative cue. Females had more difficulty learning to perform the task when the presence of the 2nd harmonic was the go stimulus, which indicates that their use of the information was biased by stimulus-response contingencies. The results are discussed in terms of a broad strategy to understand how animals perceive sounds used in communication.     

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.     

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.     

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.     

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.     

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.     

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.     

Stuttering and syllable stress

Eighteen adult stutterers read two lists each of 16 bisyllabic words. In one list, stress appeared on the first syllable; in the second, the “same” words carried second syllable stress. There proved to be no significant difference in proportion between stressed and unstressed syllables associated with stuttering. This investigation appears to dispute the proposition that stressed syllables provide the focal points of stuttering (Wingate, 1976).     

Effects of syllable frequency in speech production

In the speech production model proposed by [Levelt, W. J. M., Roelofs, A., Meyer, A. S. (1999). A theory of lexical access in speech production. Behavioral and Brain Sciences, 22, pp. 1-75.], syllables play a crucial role at the interface of phonological and phonetic encoding. At this interface, abstract phonological syllables are translated into phonetic syllables. It is assumed that this translation process is mediated by a so-called Mental Syllabary. Rather than constructing the motor programs for each syllable on-line, the mental syllabary is hypothesized to provide pre-compiled gestural scores for the articulators. In order to find evidence for such a repository, we investigated syllable-frequency effects: If the mental syllabary consists of retrievable representations corresponding to syllables, then the retrieval process should be sensitive to frequency differences. In a series of experiments using a symbol-position association learning task, we tested whether high-frequency syllables are retrieved and produced faster compared to low-frequency syllables. We found significant syllable frequency effects with monosyllabic pseudo-words and disyllabic pseudo-words in which the first syllable bore the frequency manipulation; no effect was found when the frequency manipulation was on the second syllable. The implications of these results for the theory of word form encoding at the interface of phonological and phonetic encoding; especially with respect to the access mechanisms to the mental syllabary in the speech production model by (Levelt et al.) are discussed.     

Dissociation between extension of the sensitive period for avian vocal learning and dendritic spine loss in the song nucleus lMAN

Several instances of early learning coincide with significant rearrangements of neural connections in regions contributing to these behaviors. In fact developmentally restricted learning may be constrained temporally by the opportunity for experience to selectively maintain appropriate synapses amidst the elimination of exuberant connections. Consistent with this notion, during the normal sensitive period for vocal learning in zebra finches (Taenopygia guttata), there is a decline in the density of dendritic spines within a region essential for song development, the lateral magnocellular nucleus of the anterior nidopallium (lMAN). Moreover, in birds isolated from conspecific song shortly after hatching, both the closure of the sensitive period for vocal learning and the pruning of spines from lMAN neurons is delayed. Here, we employed a more subtle form of deprivation to delay the close of the sensitive period for song learning, and found that late song learning occurred without obvious alterations in the pruning of dendritic spines on lMAN neurons. At posthatch day (PHD) 65 (beyond the end of the normal sensitive period for song memorization in zebra finches), birds isolated from song beginning on PHD30 did not differ from normally reared birds in measures of dendritic spine density on Golgi-Cox stained lMAN neurons. Moreover, tutor exposure from PHD65 to 90 did not increase spine elimination in these isolates (who memorized new song material) relative to controls (who did not). Thus, we conclude that the extent of normally occurring lMAN spine loss is not sufficient to account for the timing of the sensitive period for zebra finch song learning.     

声调在汉语音节感知中的作用

探讨超音段(如声调)与音段信息的共同作用机制, 对口语词汇识别研究具有重要的理论意义。有研究探讨了声调在口语词汇语义通达阶段的作用, 但在相对早期的音节感知阶段, 声调与声母、韵母的共同作用机制还缺乏系统的认识。本研究采用oddball实验范式, 通过两个行为实验考察了声调在汉语音节感知中的作用。实验1发现检测声调和声母变化的时间没有差异, 均比检测韵母变化的时间长, 表明在汉语音节感知中对声调的敏感性不及韵母。实验2发现声母和韵母的组合并没有明显优于对韵母的觉察, 但声调与声母或韵母的同时变化都促进了被试对偏差刺激的觉察, 表明声调通过与声母、韵母的结合来共同影响汉语音节的感知加工。研究结果在认知行为层面为声调在音节感知中的作用机制提供了直接的实验证据, 为进一步探讨超音段与音段信息共同作用的认知神经机制提供了基础。     

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.     

Social learning of food types in zebra finches (<Emphasis Type="Italic">Taenopygia guttata</Emphasis>) is directed by demonstrator sex and feeding activity

In this study we examined how social learning of feeding preferences by zebra finches was affected by the identity of different demonstrators. We presented adult zebra finches with two demonstrators, one male and one female, that exhibited different food choices, and we recorded their subsequent preference when given a choice between the two food types. Previously it was found that young zebra finches' patterns of social learning are affected by the sex of the individual demonstrating a feeding behaviour. This result could be explained by the lack of exposure these animals had to the opposite sex, or by their mating status. Therefore, we investigated the social learning preferences of adult mated zebra finches. We found the same pattern of directed social learning of a different type of feeding behaviour (food colour): female zebra finches preferred the colour of food eaten by male demonstrators, whereas male zebra finches showed little evidence of any preference for the colour of food eaten by female demonstrators. Furthermore, we found that female observers' preferences were biased by demonstrators' relative feeding activity: the female demonstrator was only ever preferred if it ate less than its male counterpart. Electronic Publication