Whether the sequential structure of bird song has perceptual significance has long been an interest of animal behaviorists. The long, rambling warble song of male budgerigars is acoustically complex and composed of a number of distinct elements uttered in streams lasting several minutes, usually accompanied by various courtship behaviors, such as head bobbing and beak touching. Recent work has shown that warble song may have a sequential structure, or patterned repetition of elements. This raises questions as to whether budgerigars can detect changes in natural warble streams and to what extent these capabilities are specific to conspecific song. Here, this study examined the perception of long bouts of warble song from male budgerigars. Using operant conditioning and a psychophysical procedure, the study probed the limits of the birds' ability to detect various changes in new and familiar sequences of warble elements. The study shows that budgerigars can detect sequence changes in short unfamiliar sequences of warble and in much longer segments of familiar warble sequences.

Mate choice is a critical decision-making process, having lasting impacts on an individual’s time, energy, and reproductive success. Across songbirds, females are generally assumed to prefer higher song rates, greater complexity, and higher quality performances; however, there is growing evidence implicating syllable level details in songbird communication. Here, we build on our previous psychoacoustic results to ask whether female zebra finches use the kinds of syllable level details that they are capable of hearing. Female zebra finches produce calls during male songs as a component of courtship. These calls can be leveraged to explore how females assess and interact with male songs. To test whether syllable level details are behaviorally relevant in a courtship context, we quantified female call responses to manipulated songs in four experiments. First, we validated that our playback procedure elicited robust calling responses from females (Exp 1). Next, we found that females decreased calling to songs where syllables were spectro-temporally reversed (REVERSAL), but did not respond differently if the syllable order was manipulated (SHUFFLED). Females also modulated their calling when experimental songs were composed of natural rendition-to-rendition variation in song syllables (RENDITION) relative to songs consisting of a single repeated rendition (FIXED) (Exp 2). Furthermore, we found that females decreased calling responses even when only a portion of syllables were spectro-temporally reversed (Exp 4). Across these experiments, we also report the striking extent to which females habituated to a male’s song (Exps 3 and 4). To maximize female responses, we tried adjusting the paradigm in Exps 3 and 4 to increase female calling. However, our adjustments had minimal effects, consistent with the notion that females rapidly decreased calling in response to a given males’ stimuli. Altogether, our results contribute to growing evidence that syllable level details in birdsong are behaviorally relevant, and, perhaps more importantly, demonstrate that birds’ enhanced ability to discriminate acoustic fine structure as shown in psychophysical tests plays a role in communication.

Over hundreds of years, breeders have selectively bred different strains of canaries for plumage and song characteristics. One strain, the Belgian Waterslager canary, has been bred for loud, low frequency song and coincidently has been found to have a high-frequency hearing loss due to damaged and missing hair cells in the basilar papilla. Here, we investigated the possible genetic basis for this hearing loss in the Belgian Waterslager canary by conducting whole-genome Illumina (San Diego, CA) sequencing in three canary strains. We identified a total of 16 Belgian Waterslager male-specific "high-impact" single nucleotide polymorphisms (SNP) variants with three mutations occurring within genes previously identified in mammalian hair cell abnormalities and hearing loss disorders: pericentriolar material 1 (PCM1), p21 (RAC1) activated kinase 3 (PAK3)-like, and protein tyrosine phosphatase receptor type K (PTPRK). Interestingly, we also identified three male-specific "high-impact" SNP variants in one of our control strains: the American Singer canary. One of these mutations occurs within genes previously associated with hearing loss in mammals. Since songbirds rely on hearing to develop a normal vocal repertoire, investigating the role of these genes in hearing loss at the molecular level may provide a valuable animal model for examining the relationship between hearing loss and vocal development in humans.

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.

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).

The 40-year-old discovery that birds regenerate hair cells in the inner ear after damage has yet to lead to treatments for hearing loss in humans, but there are other unique ways in which birds contribute to understanding the mechanisms and consequences of hearing loss. Like humans, many birds learn their vocalizations by reference to auditory information. Deafened as adults, birds experience a degradation in vocal output. Budgerigars trained to match a specific call lose precision in call production with temporary hair cell loss but regain that vocal precision with even a partial return of hearing. Canaries bred for low-pitched songs over hundreds of years inherit hair cell abnormalities, deficits in complex sound perception, and genetic mutations corresponding to mutations underlying human hair cell abnormalities. Treatment with aminoglycosides in these birds, which causes hair cell loss followed by regeneration and recovery of hearing, leads to improved hearing in birds with these hair cell abnormalities but not in those with normal hair cells suggesting that inducing supporting cell division leads to hearing recovery. Taken together, these and other findings suggest that birds should continue to be a fertile animal model for investigating hearing loss and recovery well into the future. [Work supported by NIH.]

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.

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.

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?'

Canaries have been selectively bred for specific song characteristics (song canaries) or for morphology or plumage (type canaries) for centuries. Type canaries (e.g., Border and Gloster strains) retain song characteristics that are quite similar to those of wild canaries. By contrast, song canaries (e.g., Belgian Waterslager and Roller strains) have been selected for song types pleasing to the human ear, resulting in songs that, in most cases, are less complex, lower-pitched, and narrower in a frequency range than songs from wild canaries. We now suspect that song selection in the Belgian Waterslager song canary has either directly or indirectly resulted in high-frequency hearing loss associated with hair cell abnormalities. Here, we compare hearing in the Belgian Waterslager and several other type and song canaries including the American Singer Canary. Though bred only since the 1930s, American Singer canaries may also have a high-frequency hearing loss that looks very similar to that of the Belgian Waterslager and may involve similar pathologies. Illumina whole-genome sequencing has preliminarily identified a number of high-impact SnpEff variants in Belgian Waterslager and American Singer Canaries, some of which are related to deafness genes in mammals.

Zebrafish are a popular vertebrate animal model for biomedical research including investigations of the auditory system. Responses to acoustic stimulation have been a challenge to carefully measure in zebrafish. Here, the authors have developed a procedure for measuring hearing sensitivity in adult zebrafish using an appetitive automated Go/No Go task. In this task, a trial is initiated when a fish passes through an observing gate. In a sound trial, the fish is reinforced by an automated food delivery system when it enters the reinforcement compartment. If the fish enters the reinforcement compartment during a no-sound trial, a timeout is implemented. Zebrafish successfully learned this task in a median of about ten days of daily training. Zebrafish were most sensitive at a frequency of 800 Hz, which corresponds well with sensitivity reported from physiological methods. As far as the authors know, the present study is the first to provide hearing thresholds for zebrafish using a conventional combination of operant conditioning and psychophysical procedures. This could open the door to other kinds of tests using acoustic stimuli as are commonly conducted in many other laboratory animals.

SynopsisResearch 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.

Combined, we have known Peter Narins for well over 120 years. We take great pleasure in honoring an “old” and greatly valued colleague and friend. We start by pointing out that none of us have done research with Peter, but that each off us knows, admires, and greatly values his work. For over 40 years, Peter's interdisciplinary blend of acoustics, psychophysics, physiology, and anatomy, often conducted in exotic places, has held us all in awe. Moreover, one of the most important part of Peter's work is that its impact extends far beyond amphibians. His work has helped us think about the bioacoustics of birds and fishes, and about the evolution of vertebrate hearing. His work has also stimulated research questions and how we understand research results for non-amphibian species. And, most importantly, it is not only the three of us who have benefitted from Peter's work – his contributions permeate all of animal bioacoustics and will do so for decades. Our talk will focus on how Peter's work has, and continues, to contribute to our own research, and that of many others. [Funded by three old guys.]

Breeders have bred canaries either for specific song characteristics (song canaries) or morphology/plumage (type canaries) for centuries. Type canaries (e.g., Border and Gloster strains) retain song characteristics that are typically quite similar to those of wild canaries. By contrast, song canaries (e.g., Belgian Waterslager and Roller strains) have been selected for song types pleasing to the human ear, resulting in songs that, in most cases, are less complex, lower pitched, and narrower in a frequency range than songs from wild canaries. We now suspect that song selection in the Belgian Waterslager song canary has either directly or indirectly resulted in high-frequency hearing loss associated with hair cell abnormalities. Here, we compare hearing in the Belgian Waterslager and several other type and song canaries including the American Singer Canary. Though bred only since the 1930s, American Singer canaries also have a high-frequency hearing loss that looks very similar to that of the Belgian Waterslager and may have similar pathologies. Illumina whole genome sequencing has preliminarily identified a number of high-impact SnpEff variants in Belgian Waterslager and American Singer Canaries, some of which are related to deafness genes in mammals.

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).

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.

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.