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.     

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。     

Perceptual organization of acoustic stimuli by budgerigars (Melopsittacus undulatus): II. Vocal signals

Operant conditioning and multidimensional scaling procedures were used to study auditory perception of complex sounds in the budgerigar. In a same-different discrimination task, budgerigars learned to discriminate among natural vocal signals. Multidimensional scaling procedures were used to arrange these complex acoustic stimuli in a two-dimensional space reflecting perceptual organization. Results show that budgerigars group vocal stimuli according to functional and acoustical categories. Studies with only contact calls show that birds also make within-category discriminations. The acoustic cues in contact calls most salient to budgerigars appear to be quite complex. There is a suggestion that the sex of the signaler may also be encoded in these calls. The results from budgerigars were compared with the results from humans tested on some of the same sets of complex sounds.     

Acoustic and perceptual categories of vocal elements in the warble song of budgerigars (Melopsittacus undulatus)

The warble songs of budgerigars (Melopsittacus undulatus) are composed of a number of complex, variable acoustic elements that are sung by male birds in intimate courtship contexts for periods lasting up to several minutes. If these variable acoustic elements can be assigned to distinct acoustic-perceptual categories, it provides the opportunity to explore whether birds are perceptually sensitive to the proportion or sequential combination of warble elements belonging to different categories. By the inspection of spectrograms and by listening to recordings, humans assigned the acoustic elements in budgerigar warble from several birds to eight broad, overlapping categories. A neural-network program was developed and trained on these warble elements to simulate human categorization. The classification reliability between human raters and between human raters and the neural network classifier was better than 80% both within and across birds. Using operant conditioning and a psychophysical task, budgerigars were tested on large sets of these elements from different acoustic categories and different individuals. The birds consistently showed high discriminability for pairs of warble elements drawn from between acoustic categories and low discriminability for pairs drawn from within acoustic categories. With warble elements reliably assigned to different acoustic categories by humans and birds, it affords the opportunity to ask questions about the ordering of elements in natural warble streams and the perceptual significance of this ordering.     

Differential vocalization in budgerigars: towards an experimental analysis of naming.

In Experiment 1, 3 budgerigars (Melopsittacus undulatus) were trained with food reinforcement to make low- or high-frequency calls in response to different color stimuli, C1 and C2 (a color-naming task), using a gradual response-differentiation procedure and an automatic call-recognition system. Thus, a call within a certain frequency band was reinforced in the presence of C1 ("C1 call"), and a call within a different band was reinforced in the presence of C2 ("C2 call"). In Experiment 2, all 3 budgerigars were trained in a form-to-color matching-to-sample task, alternating trial by trial with either the color-naming task (2 birds) or an identity color matching-to-sample task (1 bird). Sample stimuli for the new matching-to-sample task were forms (F1 or F2) and comparisons were the same two colors (C1 and C2). Given Sample F1 or F2, birds had to make a call to produce Comparison Pair C1 and C2. With F1 as the sample, a peck on C1 was reinforced; with F2 as the sample, a peck on C2 was reinforced. Although no particular call was specified in the presence of F1 and F2, 2 birds made the C1 call in the presence of F1 and the C2 call in the presence of F2. In Experiment 3, the bird that failed to match form and color calls in Experiment 2 and another bird were first trained in a color-to-form matching-to-sample task: C1 to F3 and C2 to F4. In this task, to produce the comparison pair of forms, a high call (or low for the other bird) was required in the presence of C1, and a low call (or high) was required in the presence of C2. Both birds were then trained with an identity matching-to-sample task in which sample and comparison stimuli were the same two forms, F3 and F4. Trials on the identity task alternated with the color-to-form trials. Although no particular call was required in the presence of Samples F3 and F4, both birds came to make the C1 call in the presence of F3 and the C2 call in the presence of F4. Our technique promises to be useful for the study of emergent vocal relations in budgerigars and other animals.     

Effects of deafening on the development of nestling and juvenile vocalizations in budgerigars (Melopsittacus undulatus).

The effects of complete and partial cochlear extirpation at ages 9-11 days posthatch were assessed in 5 nestling budgerigars (Melopsittacus undulatus) to determine if auditory feedback is necessary for the production of nestling vocalizations. Although early deafening had no effect on the production of food-begging calls produced during the first 2 weeks posthatch, deafening did disrupt the expected transition from these early calls to the longer and more complex frequency-modulated, patterned food-begging calls normally appearing 3-4 weeks posthatch. All birds sustaining either complete or partial cochlear extirpation failed to develop stereotyped contact calls around the time of fledging at 5 weeks. These results are consistent with previous research showing that deafened nestlings do not develop normal contact calls (R. J. Dooling, B. F. Gephart, P. H. Price, C. McHale, & S. E. Brauth, 1987) and also indicate that a form of sensorimotor learning is involved in the production of mature, patterned food-begging calls in budgerigars.     

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.     

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.     

A method for studying stimulus class dynamics using budgerigars and vocal responding

We describe a methodology for examining stimulus class dynamics in budgerigars. Three budgerigars served as subjects. Four call types were trained as operant responses to four discriminative stimuli. The birds were over‐trained in this discrimination, and then run through two conditions. In Condition 1 the birds were trained to peck two of the four stimuli when these two stimuli appeared in two novel locations, while continuing to vocalize to all four stimuli when they occurred in the original training location. An analysis of vocal errors showed that the two stimuli assigned to the peck response were more likely to become confused with one another. In Condition 2 the birds experienced symbolic matching‐to‐sample training. Vocal discrimination trials were run concurrently with this training. The observed vocal‐response errors suggest that during a matching‐to‐sample task, sample stimuli became temporarily confused with one another. The results, although primarily intended to illustrate the utility of our method, support the hypothesis that stimuli assigned a common response become more similar, or equivalent, to one another.     

Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus)

Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species' vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.     

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.     

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.     

Generalizing prosodic patterns by a non-vocal learning mammal

Prosody, a salient aspect of speech that includes rhythm and intonation, has been shown to help infants acquire some aspects of syntax. Recent studies have shown that birds of two vocal learning species are able to categorize human speech stimuli based on prosody. In the current study, we found that the non-vocal learning rat could also discriminate human speech stimuli based on prosody. Not only that, but rats were able to generalize to novel stimuli they had not been trained with, which suggests that they had not simply memorized the properties of individual stimuli, but learned a prosodic rule. When tested with stimuli with either one or three out of the four prosodic cues removed, the rats did poorly, suggesting that all cues were necessary for the rats to solve the task. This result is in contrast to results with humans and budgerigars, both of which had previously been studied using the same paradigm. Humans and budgerigars both learned the task and generalized to novel items, but were also able to solve the task with some of the cues removed. In conclusion, rats appear to have some of the perceptual abilities necessary to generalize prosodic patterns, in a similar though not identical way to the vocal learning species that have been studied.     

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.     

Acoustic interactions in broods of nestling birds (Tachycineta bicolor)

Studies of acoustic interactions in animal groups, such as chorusing insects, anurans, and birds, have been invaluable in showing how cooperation and competition shape signal structure and use. The begging calls of nestling birds are ideal for such studies, because they function both as a cooperative signals of the brood's needs and as competitive signals for parental allocation within the brood. Nonetheless, studies of acoustic interactions among nestlings are rare. Here we review our work on acoustic interactions in nestling tree swallows (Tachycineta bicolor), especially how calls are used in competition for parental feedings. Nestlings attracted parental attention and responded to acoustic interference mainly by increasing call output. However, nestlings also gave more similar calls when they called together and decreased their call bandwidth when exposed to elevated noise. We suggest that these competitive uses of calls might intensify the cooperative brood signal, affecting both parental provisioning and vocal development. Given their tremendous variation across species, begging calls offer promising opportunities for developmental and comparative studies of acoustic signaling.     

The origins of vocal learning: New sounds, new circuits, new cells

We do not know how vocal learning came to be, but it is such a salient trait in human evolution that many have tried to imagine it. In primates this is difficult because we are the only species known to possess this skill. Songbirds provide a richer and independent set of data. I use comparative data and ask broad questions: How does vocal learning emerge during ontogeny? In what contexts? What are its benefits? How did it evolve from unlearned vocal signals? How was brain anatomy altered to enable vocal learning? What is the relation of vocal learning to adult neurogenesis? No one has described yet a circuit or set of circuits that can master vocal learning, but this knowledge may soon be within reach. Moreover, as we uncover how birds encode their learned song, we may also come closer to understanding how we encode our thoughts.     

Vocal and manual response latencies to bilateral and unilateral tachistoscopic letter displays

Bilateral rows of eight letters and unilateral rows of four letters were presented in randomized sequences for 100 ms. Subjects were required to recall all letters in a trial (Experiment I); recall letters from one hemifield cued at exposure (Experiment II); recognize a single letter, making a vocal response (Experiment III); recognize a single letter, making a manual response (Experiment IV). In Experiments I, II and III, identification errors were fewer and vocal response latencies were faster for RVF stimuli, except in the bilateral condition on Experiment I; in Experiment IV manual response latencies were the same, for left and right, bilateral and unilateral conditions. Collectively, the results could not be satisfactorily accounted for by any one hypothesis: report-order, trace-scanning, or cerebral dominance. The relative contribution of each process to the laterality effect was discussed.     

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.     

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.     

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.