Hearing and vocalizations in a small songbird, the red-cheeked cordon bleu (Uraeginthus bengalus) (L).

The auditory sensitivity of a small songbird, the red-cheeked cordon bleu, was measured using the standard methods of animal psychophysics. Hearing in cordon bleus is similar to other small passerines with best hearing in the frequency region from 2 to 4 kHz and sensitivity declining at the rate of about 10 dB/octave below 2 kHz and about 35 dB/octave as frequency increases from 4 to 9 kHz. While critical ratios are similar to other songbirds, the long-term average power spectrum of cordon bleu song falls above the frequency of best hearing in this species.

Constraints on vocal production learning in budgerigars (Melopsittacus undulates).

Budgerigars (Melopsittacus undulatus) are small Australian parrots with a well-documented, learned vocal repertoire and a high degree of vocal production learning. These birds live in large, social flocks and they vocally interact with each other in a dynamic, reciprocal manner. We assume that budgerigars must process and integrate a wide variety of sensory stimuli when selecting appropriate vocal responses to conspecifics during vocal interactions, but the relative contributions of these different stimuli to that process are next to impossible to tease apart in a natural context. Here we show that budgerigars, under operant control, can learn to respond to specific stimuli with a specific vocal response. Budgerigars were trained to produce contact calls to a combination of auditory and visual cues. Birds learned to produce specific contact calls to stimuli that differed either in location (visual or auditory) or quality (visual). Interestingly, the birds could not learn to associate different vocal responses with different auditory stimuli coming from the same location. Surprisingly, this was so even when the auditory stimuli and the responses were the same (i.e., the bird's own contact call). These results show that even in a highly controlled operant context, acoustic cues alone were not sufficient to support vocal production learning in budgerigars. From a different perspective, these results highlight the significant role that social interaction likely plays in vocal production learning so elegantly shown by Irene Pepperberg's work in parrots.

How canaries listen to their song: Species-specific shape of auditory perception.

The melodic, rolling songs of canaries have entertained humans for centuries and have been studied for decades by researchers interested in vocal learning, but relatively little is known about how the birds listen to their songs. Here, it is investigated how discriminable the general acoustic features of conspecific songs are to canaries, and their discrimination abilities are compared with a small parrot species, the budgerigar. Past experiments have shown that female canaries are more sexually responsive to a particular song element-the "special" syllables-and consistent with those observations, it was found that special syllables are perceptually distinctive for canaries. It is also shown that canaries discriminate the subtle differences among syllables and phrases using spectral, envelope, and temporal fine structure cues. Yet, while canaries can hear these fine details of the acoustic structure of their song, the evidence overall suggests that they listen at a more global, phrase by phrase level, rather than an analytic, syllable by syllable level, except when attending to some features of special syllables. These results depict the species-specific shape of auditory perception in canaries and lay the groundwork for future studies examining how song perception changes seasonally and according to hormonal state.

Strain differences in hearing in song canaries.

Belgian Waterslager song canaries, bred for hundreds of years for a low-pitched song, have also acquired an inherited high-frequency hearing loss associated with hair cell abnormalities. Here, auditory thresholds measured using auditory brainstem responses and psychophysical methods in three different strains of canaries are compared: Belgian Waterslagers, American Singers, and Borders. Border canaries have not been bred for song characteristics while American Singer canaries have been bred for song only since the 1930s. Results show that American Singer canaries also have elevated high frequency thresholds that are similar to those of the Belgian Waterslager, while Border canaries have normal thresholds. These results strengthen the case that song canary breeders in selecting for song characteristics may have inadvertently selected for hearing abnormalities.

Auditory-vocal coupling in the naked mole-rat, a mammal with poor auditory thresholds.

Naked mole-rats are extremely social and extremely vocal rodents, displaying a wide range of functionally distinct call types and vocalizing almost continuously. Their vocalizations are low frequency, and a behavioral audiogram has shown that naked mole-rats, like other subterranean mammals, hear only low frequencies. Hence, the frequency range of their hearing and vocalizations appears to be well matched. However, even at low frequencies, naked mole-rats show very poor auditory thresholds, suggesting vocal communication may be effective only over short distances. However, in a tunnel environment where low frequency sounds propagate well and background noise is low, it may be that vocalizations travel considerable distances at suprathreshold intensities. Here, we confirmed hearing sensitivity using the auditory brainstem response; we characterized signature and alarm calls in intensity and frequency domains and we measured the effects of propagation through tubes with the diameter of naked mole-rat tunnels. Signature calls-used for intimate communication-could travel 3-8 m at suprathreshold intensities, and alarm calls (lower frequency and higher intensity), could travel up to 15 m. Despite this species' poor hearing sensitivity, the naked mole-rat displays a functional, coupled auditory-vocal communication system-a hallmark principle of acoustic communication systems across taxa.

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.

Masking Experiments in Humans and Birds Using Anthropogenic Noises.

This study investigated the masking of pure tones by anthropogenic noises in humans and birds. Bird experiments were conducted in the laboratory using operant conditioning and psychophysical procedures but with anthropogenic noises rather than white noise. Humans were tested using equivalent psychophysical procedures in the field with ambient background noise. Results show that for both humans and birds published critical ratios can be used to predict the masking thresholds for pure tones by these complex noises. Thus, the species' critical ratio can be used to estimate the effect of anthropogenic environmental noises on the perception of communication and other biologically relevant sounds.

Auditory brainstem responses and auditory thresholds in woodpeckers.

Auditory sensitivity in three species of woodpeckers was estimated using the auditory brainstem response (ABR), a measure of the summed electrical activity of auditory neurons. For all species, the ABR waveform showed at least two, and sometimes three prominent peaks occurring within 10 ms of stimulus onset. Also ABR peak amplitude increased and latency decreased as a function of increasing sound pressure levels. Results showed no significant differences in overall auditory abilities between the three species of woodpeckers. The average ABR audiogram showed that woodpeckers have lowest thresholds between 1.5 and 5.7 kHz. The shape of the average woodpecker ABR audiogram was similar to the shape of the ABR-measured audiograms of other small birds at most frequencies, but at the highest frequency data suggest that woodpecker thresholds may be lower than those of domesticated birds, while similar to those of wild birds.

Sound order discrimination in two species of birds-Taeniopygia guttata and Melopsittacus undulatus.

Recent psychophysical experiments have shown that zebra finches (Taeniopygia guttata-a songbird) are surprisingly insensitive to syllable sequence changes in their species-specific motifs while budgerigars (Melopsittacus undulatus-a psittacine) do much better when tested on exactly the same sounds. This is unexpected since zebra finch males learn the order of syllables in their songs when young and sing the same song throughout adulthood. Here we probe the limits of this species difference by testing birds on an order change involving just two syllables, hereafter called bi-syllable phrases. Results show budgerigars still perform better than zebra finches on an order change involving just two syllables. An analysis of response latencies shows that both species respond to an order change in a bi-syllable motif at the onset of the first syllable rather than listening to the entire sequence before responding. Additional tests with one syllable omitted or doubled, or with white noise bursts substituted for syllables, indicate that the first syllable in the sequence has a dominant effect on subsequent discrimination of changes in a bi-syllable pattern. These results are surprising in that zebra finch males sing their full motif syllable sequence with a high degree of stereotypy throughout life, suggesting that this consistency in production may not rely on perceptual mechanisms for processing syllable order in adulthood. Budgerigars, on the other hand, are quite sensitive to bi-syllable order changes, an ability that may be related to useful information being encoded in the sequence of syllables in their natural song. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

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.

Hearing in birds: what changes from air to water.

We reviewed what is known about hearing in birds, including the effects of anthropogenic noise, to speculate on the nature of underwater hearing in diving birds. Taking into consideration changes inhuman hearing underwater, the effects of changes in middle ear pressure on hearing in humans, and the protective effects against acoustic overexposure in birds from changes in middle ear pressure, we suggest that if similar patterns hold for diving birds, they may not hear well underwater. Moreover,the frequency of best hearing sensitivity may shift to frequencies below 2 and 4 kHz. Trapped air may allow the middle ear cavity of birds to function much as the swim bladder functions in fish.Diving birds present important auditory and environmental issues. To resolve these issues properly requires comparative anatomical investigations of the middle and inner ears of diving birds.More importantly, behavioral measures of hearing in diving birds must be conducted both in air and in water. Finally, behavioral studies of these animals in their natural habitats are required to deter-mine whether they use sound underwater for communication, foraging, predator avoidance, or other behaviors.

Relative salience of envelope and fine structure cues in zebra finch song.

Zebra finches produce a learned song that is rich in harmonic structure and highly stereotyped. More is generally known about how birds learn and produce this song than how they perceive it. Here, zebra finches were trained with operant techniques to discriminate changes in natural and synthetic song motifs. Results show that zebra finches are quite insensitive to changes to the overall envelope of the motif since they were unable to discriminate more than a doubling in inter-syllable interval durations. By contrast, they were quite sensitive to changes in individual syllables. A series of tests with synthetic song syllables, including some made of frozen noise and Schroeder harmonic complexes, showed that birds used a suite of acoustic cues in normal listening but they could also distinguish among syllables simply on the basis of the temporal fine structure in the waveform. Thus, while syllable perception is maintained by multiple redundant cues, temporal fine structure features alone are sufficient for syllable discrimination and may be more important for communication than previously thought.

Learned vocalizations in budgerigars (Melopsittacus undulatus): the relationship between contact calls and warble song.

The budgerigar (Melopsittacus undulatus) has an extraordinarily complex, learned, vocal repertoire consisting of both the long rambling warble song of males and a number of short calls produced by both sexes. In warble, the most common elements (>30%) bear a strong resemblance to the highly frequency-modulated, learned contact calls that the birds produce as single utterances. However, aside from this apparent similarity, little else is known about the relationship between contact calls and warble call elements. Here, both types of calls were recorded from four male budgerigars. Signal analysis and psychophysical testing procedures showed that the acoustic features of these two vocalizations were acoustically different and perceived as distinctive vocalizations by birds. This suggests that warble call elements are not simple insertions of contact calls but are most likely different acoustic elements, created de novo, and used solely in warble. Results show that, like contact calls, warble call elements contain information about signaler identity. The fact that contact calls and warble call elements are acoustically and perceptually distinct suggests that they probably represent two phonological systems in the budgerigar vocal repertoire, both of which arise by production learning.

Masked auditory thresholds in three species of birds, as measured by the auditory brainstem response (L).

Auditory brainstem responses (ABRs) were recorded in adult budgerigars, canaries, and zebra finches in quiet and in three levels of white noise for tone stimuli between 1 and 4 kHz. Similar to behavioral results, masked ABR thresholds increased linearly with increasing noise levels. When the three species are considered together, ABR-derived CRs were higher than behavioral CRs by 18-23 dB between 2 and 4 kHz and by about 30 dB at 1 kHz. This study clarifies the utility of using ABRs for estimating masked auditory thresholds in natural environmental noises in species that cannot be tested behaviorally.

Discrimination of natural acoustic variation in vocal signals.

Studies of acoustic communication often focus on the categories and units of vocalizations, but subtle variation also occurs in how these signals are uttered. In human speech, it is not only phonemes and words that carry information but also the timbre, intonation, and stress of how speech sounds are delivered (often referred to as "paralinguistic content"). In non-human animals, variation across utterances of vocal signals also carries behaviorally relevant information across taxa. However, the discriminability of these cues has been rarely tested in a psychophysical paradigm. Here, we focus on acoustic communication in the zebra finch (Taeniopygia guttata), a songbird species in which the male produces a single stereotyped motif repeatedly in song bouts. These motif renditions, like the song repetitions of many birds, sound very similar to the casual human listener. In this study, we show that zebra finches can easily discriminate between the renditions, even at the level of single song syllables, much as humans can discriminate renditions of speech sounds. These results support the notion that sensitivity to fine acoustic details may be a primary channel of information in zebra finch song, as well as a shared, foundational property of vocal communication systems across species.

The auditory brainstem response in two lizard species.

Although lizards have highly sensitive ears, it is difficult to condition them to sound, making standard psychophysical assays of hearing sensitivity impractical. This paper describes non-invasive measurements of the auditory brainstem response (ABR) in both Tokay geckos (Gekko gecko; nocturnal animals, known for their loud vocalizations) and the green anole (Anolis carolinensis, diurnal, non-vocal animals). Hearing sensitivity was measured in 5 geckos and 7 anoles. The lizards were sedated with isoflurane, and ABRs were measured at levels of 1 and 3% isoflurane. The typical ABR waveform in response to click stimulation showed one prominent and several smaller peaks occurring within 10 ms of the stimulus onset. ABRs to brief tone bursts revealed that geckos and anoles were most sensitive between 1.6-2 kHz and had similar hearing sensitivity up to about 5 kHz (thresholds typically 20-50 dB SPL). Above 5 kHz, however, anoles were more than 20 dB more sensitive than geckos and showed a wider range of sensitivity (1-7 kHz). Generally, thresholds from ABR audiograms were comparable to those of small birds. Best hearing sensitivity, however, extended over a larger frequency range in lizards than in most bird species.

Familiarity enhances moment-to-moment behavioral coordination in zebra finch (Taeniopygia guttata) dyads.

An individual's ability to respond to and align with the behavior of others is a fundamental component of social behavior. Zebra finches form lifelong monogamous pair bonds; however, zebra finches are also gregarious and can form strong social bonds with same-sex conspecifics. Here, we quantified behavior during brief 10-min reunions for males and females in five types of social conditions: monogamously bonded opposite-sex partners, familiar same-sex, familiar opposite-sex, novel same-sex, and novel opposite-sex dyads. We analyzed these interactions in three ways. First, we quantified overall activity levels (call and movement rates) for each individual. Second, we measured how coordinated calls and movements were by calculating (a) the percent difference in activity rates as an estimate of how similar calling and movement activity were between individuals within a dyad, and (b) the sliding correlation coefficients for time-stamped calls and movements for each dyad. Finally, we described multimodal behavioral profiles of coordination using principal component analyses. Overall, females were more active than males. For both females and males, activity levels as well as the coordination of calls and movements were significantly affected by social condition. In general, monogamous partners, female familiar same-sex dyads and familiar opposite-sex dyads were the most coordinated. This effect of familiarity shows that moment-to-moment behavioral coordination can be influenced by prior social experiences. Quantifying patterns of coordination or social synchrony may prove valuable for understanding the effects of social experience on brain and behavior. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Sound sequences in birdsong: how much do birds really care?

The complex and melodic nature of many birds' songs has raised interest in potential parallels between avian vocal sequences and human speech. The similarities between birdsong and speech in production and learning are well established, but surprisingly little is known about how birds perceive song sequences. One popular laboratory songbird, the zebra finch (Taeniopygia guttata), has recently attracted attention as an avian model for human speech, in part because the male learns to produce the individual elements in its song motif in a fixed sequence. But psychoacoustic evidence shows that adult zebra finches are relatively insensitive to the sequential features of song syllables. Instead, zebra finches and other birds seem to be exquisitely sensitive to the acoustic details of individual syllables to a degree that is beyond human hearing capacity. Based on these findings, we present a finite-state model of zebra finch perception of song syllable sequences and discuss the rich informational capacity of their vocal system. Furthermore, we highlight the abilities of budgerigars (Melopsittacus undulatus), a parrot species, to hear sequential features better than zebra finches and suggest that neurophysiological investigations comparing these species could prove fruitful for uncovering neural mechanisms for auditory sequence perception in human speech. This article is part of the theme issue 'What can animal communication teach us about human language?'

Monogamy in a Moment: How do Brief Social Interactions Change Over Time in Pair-Bonded Zebra Finches (Taeniopygia guttata)?

Research on monogamy has largely focused on marked behaviors that are unique to pair bonded partners. However, these marked behaviors represent only a subset of the pair-directed behaviors that partners engage in; the influence of pair bonding on mundane or subtle social interactions among partners remains largely unknown. In this study, we describe the changes that occur during brief social reunions (or greets) over the course of pair bonding in zebra finches. We quantified pair-directed behavior during 5-min reunions from three stages of pair bonding: initial pairing (between 4 and 72 h), early pairing (1-2 weeks), and late pairing (>1 month). These social interactions were operationalized in multiple ways. First, we quantified the overall activity levels (call and movement rates) for both the male and female. Overall, females were more active than males, but for both males and females calling activity was highest at initial pairing. We quantified behavioral coordination between partners in two ways: (1) similarity in call and movement rates between partners and (2) temporal synchrony of calls and movements between partners (via sliding correlation coefficients of time-stamped calls and movements). Overall, there were no effects of pairing stage on behavioral coordination. Finally, we used principal component analyses to disentangle behavioral coordination from the activity levels of the male and female. These results contribute to a growing line of evidence that male and female zebra finches differentially contribute to social dynamics and highlight the influence of pair bonding on the development of social dynamics. Furthermore, our preliminary analyses raise the hypothesis that behavioral coordination during the earliest phases of pairing is modulated by the extent and nature of prior experience. Overall, while behavioral coordination is clearly important for many salient interactions such as duetting, courtship displays, and biparental care, the significance of mundane social interactions for monogamous partnerships remains largely unknown.

The effect of altered auditory feedback on control of vocal production in budgerigars (Melopsittacus undulatus).

Budgerigars learn their vocalizations by reference to auditory information and they retain the ability to learn new vocalizations throughout life. Auditory feedback of these vocalizations was manipulated in three experiments by training birds to produce vocalizations while wearing small earphones. Experiments 1 and 2 examined the effect of background noise level (Lombard effect) and the effect of manipulating feedback level from self-produced vocalizations (Fletcher effect), respectively. Results show that birds exhibit both a Lombard effect and a Fletcher effect. Further analysis showed that changes in vocal intensity were accompanied by changes in call fundamental frequency and duration. Experiment 3 tested the effect of delaying or altering auditory feedback during vocal production. Results showed subsequent production of incomplete and distorted calls in both feedback conditions. These distortions included changes in the peak fundamental frequency, amplitude, duration, and spectrotemporal structure of calls. Delayed auditory feedback was most disruptive to subsequent calls when the delay was 25 ms. Longer delays resulted in fewer errors.