Publications by authors named "Robert J Dooling"

51 Publications

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

Integr Org Biol 2020 26;2(1):obaa034. Epub 2020 Dec 26.

Department of Psychology, University of Maryland, College Park, MD, USA.

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.
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http://dx.doi.org/10.1093/iob/obaa034DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7810576PMC
December 2020

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

Learn Behav 2021 03 2;49(1):150-158. Epub 2021 Mar 2.

Department of Psychology, University of Maryland, College Park, MD, 20742, USA.

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.
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http://dx.doi.org/10.3758/s13420-021-00465-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7979668PMC
March 2021

Discrimination of natural acoustic variation in vocal signals.

Sci Rep 2021 Jan 13;11(1):916. Epub 2021 Jan 13.

Department of Psychology, University of Maryland, Biology-Psychology Bldg., 4094 Campus Dr., College Park, MD, 20742, USA.

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.
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http://dx.doi.org/10.1038/s41598-020-79641-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7807010PMC
January 2021

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

Philos Trans R Soc Lond B Biol Sci 2020 01 18;375(1789):20190044. Epub 2019 Nov 18.

Psychology Department, University of Maryland, 4094 Campus Drive, College Park, MD 20742, USA.

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 (), 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 (), 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?'
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http://dx.doi.org/10.1098/rstb.2019.0044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6895548PMC
January 2020

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

J Comp Psychol 2020 05 24;134(2):135-148. Epub 2019 Oct 24.

Department of Psychology.

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).
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http://dx.doi.org/10.1037/com0000201DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7180088PMC
May 2020

Strain differences in hearing in song canaries.

J Acoust Soc Am 2019 07;146(1):EL71

Psychology Department, University of Maryland College Park, 4094 Campus Drive, College Park, Maryland 20742,

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.
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http://dx.doi.org/10.1121/1.5117168DOI Listing
July 2019

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

J Acoust Soc Am 2019 01;145(1):562

Psychology Department, University of Maryland, 4094 Campus Drive, College Park, Maryland 20742, USA.

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.
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http://dx.doi.org/10.1121/1.5087692DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6910023PMC
January 2019

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

J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2018 11 19;204(11):905-914. Epub 2018 Sep 19.

Department of Biological Sciences, University of Illinois, Chicago, IL, USA.

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.
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http://dx.doi.org/10.1007/s00359-018-1287-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6208660PMC
November 2018

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

Anim Cogn 2018 Jul 15;21(4):467-480. Epub 2018 May 15.

Psychology Department, University of Maryland, Biology-Psychology Bldg., 4094 Campus Dr., College Park, MD, 20742, USA.

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.
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http://dx.doi.org/10.1007/s10071-018-1182-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6438364PMC
July 2018

Acoustic fine structure may encode biologically relevant information for zebra finches.

Sci Rep 2018 04 18;8(1):6212. Epub 2018 Apr 18.

Department of Psychology, University of Maryland, College Park, USA.

The ability to discriminate changes in the fine structure of complex sounds is well developed in birds. However, the precise limit of this discrimination ability and how it is used in the context of natural communication remains unclear. Here we describe natural variability in acoustic fine structure of male and female zebra finch calls. Results from psychoacoustic experiments demonstrate that zebra finches are able to discriminate extremely small differences in fine structure, which are on the order of the variation in acoustic fine structure that is present in their vocal signals. Results from signal analysis methods also suggest that acoustic fine structure may carry information that distinguishes between biologically relevant categories including sex, call type and individual identity. Combined, our results are consistent with the hypothesis that zebra finches can encode biologically relevant information within the fine structure of their calls. This study provides a foundation for our understanding of how acoustic fine structure may be involved in animal communication.
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http://dx.doi.org/10.1038/s41598-018-24307-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5906677PMC
April 2018

Do we hear what birds hear in birdsong?

Anim Behav 2017 Feb 18;124:283-289. Epub 2016 Nov 18.

Department of Psychology, University of Maryland, College Park, MD, U.S.A.

Peter Marler's fascination with richness of birdsong included the notion that birds attended to some acoustic features of birdsong, likely in the time domain, which were inaccessible to human listeners. While a considerable amount is known about hearing and vocal communication in birds, how exactly birds perceive their auditory world still remains somewhat of a mystery. For sure, field and laboratory studies suggest that birds hear the spectral, gross temporal features (i.e. envelope) and perhaps syntax of birdsong much like we do. However, there is also ample anecdotal evidence that birds are consistently more sensitive than humans to at least some aspects of their song. Here we review several psychophysical studies supporting Marler's intuitions that birds have both an exquisite sensitivity to temporal fine structure and may be able to focus their auditory attention on critical acoustic details of their vocalizations. Zebra finches, , particularly, seem to be extremely sensitive to temporal fine structure in both synthetic stimuli and natural vocalizations. This finding, together with recent research highlighting the complexity of zebra finch vocalizations across contexts, raises interesting questions about what information zebra finches may be communicating in temporal fine structure. Together these findings show there is an acoustic richness in bird vocalizations that is available to birds but likely out of reach for human listeners. Depending on the universality of these findings, it raises questions about how we approach the study of birdsong and whether potentially significant information is routinely being encoded in the temporal fine structure of avian vocal signals.
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http://dx.doi.org/10.1016/j.anbehav.2016.10.012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5884127PMC
February 2017

Masking Experiments in Humans and Birds Using Anthropogenic Noises.

Adv Exp Med Biol 2016 ;875:239-43

Department of Psychology, University of Maryland, College Park, MD, 20742, USA.

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.
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http://dx.doi.org/10.1007/978-1-4939-2981-8_28DOI Listing
June 2016

Effect of auditory stimuli on conditioned vocal behavior of budgerigars.

Behav Processes 2016 Jan 17;122:87-9. Epub 2015 Nov 17.

Department of Psychology, University of Maryland, College Park, MD 20742, United States.

The budgerigar (Melopsittacus undulatus) is a highly social species and serves as an excellent model of vocal learning and production. This species can be trained to vocalize as a conditioned response using an operant conditioning paradigm. In addition, the birds can be trained to produce different vocalizations in response to different visual signals. Budgerigars may be fairly unique in the capability for vocal production under operant control. Whether acoustic features of the bird's natural social milieu can influence this conditioned vocal output is uncertain. The present study asked whether conditioned vocal behavior in budgerigars can be influenced by hearing vocalizations of other birds. The results show that birds vocalizing under operant control produced louder calls in the presence of vocalizations from other birds, than in pure tones or in quiet. The acoustic variation of the conditioned vocalization also increased when it is in the context of hearing other . These results reveal a functional connection between the vocal production under operant control and the perceptual mechanisms subserving vocal production in the budgerigars' natural social milieu.
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http://dx.doi.org/10.1016/j.beproc.2015.11.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4696898PMC
January 2016

Effects of noise on fishes: what we can learn from humans and birds.

Integr Zool 2015 Jan;10(1):29-37

Department of Psychology, University of Maryland, College Park, Maryland, USA.

In this paper we describe the masking of pure tones in humans and birds by manmade noises and show that similar ideas can be applied when considering the potential effects of noise on fishes, as well as other aquatic vertebrates. Results from many studies on humans and birds, both in the field and in the laboratory, show that published critical ratios can be used to predict the masked thresholds for pure tones when maskers consist of complex manmade and natural noises. We argue from these data that a single, simple measure, the species critical ratio, can be used to estimate the effect of manmade environmental noises on the perception of communication and other biologically relevant sounds. We also reason that if this principle holds for species as diverse as humans and birds, it probably also applies for all other vertebrates, including fishes.
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http://dx.doi.org/10.1111/1749-4877.12094DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4497558PMC
January 2015

Auditory brainstem responses and auditory thresholds in woodpeckers.

J Acoust Soc Am 2013 Jan;133(1):337-42

Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, Maryland 21250, USA.

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.
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http://dx.doi.org/10.1121/1.4770255DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3548892PMC
January 2013

Return of function after hair cell regeneration.

Hear Res 2013 Mar 29;297:113-20. Epub 2012 Nov 29.

Department of Communication Sciences and Disorders, James Madison University, 701 Carrier Drive, MSC 4304, Harrisonburg, VA 22807, USA.

The ultimate goal of hair cell regeneration is to restore functional hearing. Because birds begin perceiving and producing song early in life, they provide a propitious model for studying not only whether regeneration of lost hair cells can return auditory sensitivity but also whether this regenerated periphery can restore complex auditory perception and production. They are the only animal where hair cell regeneration occurs naturally after hair cell loss and where the ability to correctly perceive and produce complex acoustic signals is critical to procreation and survival. The purpose of this review article is to survey the most recent literature on behavioral measures of auditory functional return in adult birds after hair cell regeneration. The first portion of the review summarizes the effect of ototoxic drug induced hair cell loss and regeneration on hearing loss and recovery for pure tones. The second portion reviews studies of complex, species-specific vocalization discrimination and recognition after hair cell regeneration. Finally, we discuss the relevance of temporary hearing loss and recovery through hair cell regeneration on complex call and song production. Hearing sensitivity is restored, except for the highest frequencies, after hair cell regeneration in birds, but there are enduring changes to complex auditory perception. These changes do not appear to provide any obstacle to future auditory or vocal learning. This article is part of a Special Issue entitled "Inner Ear Development and Regeneration".
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http://dx.doi.org/10.1016/j.heares.2012.11.019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3593961PMC
March 2013

Perception of warble song in budgerigars (Melopsittacus undulatus): evidence for special processing.

Anim Cogn 2012 Nov 14;15(6):1151-9. Epub 2012 Aug 14.

Department of Psychology, University of Maryland, College Park 20742, USA.

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.
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http://dx.doi.org/10.1007/s10071-012-0539-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3474876PMC
November 2012

Hearing in birds: what changes from air to water.

Adv Exp Med Biol 2012 ;730:77-82

University of Maryland, College Park, College Park, MD 20742, USA.

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.
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http://dx.doi.org/10.1007/978-1-4419-7311-5_17DOI Listing
April 2012

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

J Comp Psychol 2011 Nov;125(4):420-30

Department of Psychology and Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA.

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.
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http://dx.doi.org/10.1037/a0024396DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4497543PMC
November 2011

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

J Acoust Soc Am 2011 Jun;129(6):3445-8

Department of Psychology, University of Maryland, College Park, Maryland 20742, USA.

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.
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http://dx.doi.org/10.1121/1.3578452DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3135144PMC
June 2011

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

J Acoust Soc Am 2011 May;129(5):3373-83

Neuroscience and Cognitive Science Program, University of Maryland, College Park, Maryland 20742, USA.

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.
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http://dx.doi.org/10.1121/1.3560121DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3108398PMC
May 2011

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

J Acoust Soc Am 2011 Apr;129(4):2289-97

Department of Psychology, University of Maryland, College Park, Maryland 20742, USA.

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.
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http://dx.doi.org/10.1121/1.3557035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3087398PMC
April 2011

The auditory brainstem response in two lizard species.

J Acoust Soc Am 2010 Aug;128(2):787-94

Department of Psychology, University of Maryland, College Park, Maryland 20742, USA.

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.
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http://dx.doi.org/10.1121/1.3458813DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2933256PMC
August 2010

Electrophysiological and morphological development of the inner ear in Belgian Waterslager canaries.

Hear Res 2010 Oct 16;269(1-2):56-69. Epub 2010 Jul 16.

Department of Psychology, University of Maryland, College Park, MD 20742, USA.

Belgian Waterslager (BW) canaries have an inherited hearing loss due to missing and abnormal hair cells, but it is unclear whether the loss is congenital or developmental. We used auditory brainstem responses and scanning electron microscopy to describe the development of auditory sensitivity and hair cell abnormalities in BW and non-BW canaries. In both strains, adult ABR thresholds were higher than behavioral thresholds, but BW canaries exhibited higher thresholds than non-BW canaries across all frequencies. Immediately post-hatch, ABR thresholds and hair cell numbers were similar in both strains. Two weeks later, thresholds were significantly higher in BW canaries, and hair cell number progressively decreased as the birds aged. These data show that in BW canaries: the peripheral auditory system is functionally similar to non-BW canary from hatch to 2 weeks, ABR thresholds improve during this developmental period, actually becoming better than those of adults, but then worsen as the bird continues to age. Hair cell number and appearance is similar to non-BW canaries at hatch but progressively declines after 30 days of age. These data show that the hearing loss characteristic of BW canaries is, at least in part, developmental and is established by the time song learning begins.
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http://dx.doi.org/10.1016/j.heares.2010.07.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2934893PMC
October 2010

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

J Acoust Soc Am 2009 Aug;126(2):911-9

Department of Psychology, University of Maryland, College Park, MD 20742, USA.

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.
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http://dx.doi.org/10.1121/1.3158928DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2730712PMC
August 2009

Discrimination of auditory gratings in birds.

Hear Res 2009 Oct 7;256(1-2):11-20. Epub 2009 May 7.

Department of Psychology, University of Maryland - College Park, Biology-Psychology Building, College Park, MD 20742, USA.

Auditory gratings (also called auditory ripples) are a family of complex, broadband sounds with sinusoidally modulated logarithmic amplitudes and a drifting spectral envelope. These stimuli have been studied both physiologically in mammals and psychophysically in humans. Auditory gratings share spectro-temporal properties with many natural sounds, including species-specific vocalizations and the formant transitions of human speech. We successfully trained zebra finches and budgerigars, using operant conditioning methods, to discriminate between flat-spectrum broadband noise and noises with ripple spectra of different densities that moved up or down in frequency at various rates. Results show that discrimination thresholds (minimum modulation depth) increased as a function of increasing grating periodicity and density across all species. Results also show that discrimination in the two species of birds was better at those grating periodicities and densities that are prominent in their species-specific vocalizations. Budgerigars were generally more sensitive than both zebra finches and humans. Both bird species showed greater sensitivity to descending auditory gratings, which mirrors the main direction in their vocalizations. Humans, on the other hand, showed no directional preference even though speech is somewhat downward directional. Overall, our results are suggestive of both common strategies in the processing of complex sounds between birds and mammals and specialized, species-specific variations on that processing in birds.
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http://dx.doi.org/10.1016/j.heares.2009.04.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4497563PMC
October 2009

Presence of aromatase and estrogen receptor alpha in the inner ear of zebra finches.

Hear Res 2009 Jun 3;252(1-2):49-55. Epub 2009 May 3.

Department of Psychology, University of Maryland, College Park, MD 20742, USA.

Sex differences in song behavior and in the neural system controlling song in songbirds are well documented but relatively little is known about sex differences in hearing. We recently demonstrated the existence of sex differences in auditory brainstem responses in a songbird species, the zebra finch (Taeniopygia guttata). Many sex differences are regulated by sex steroid hormone action either during ontogeny or in adulthood. As a first step to test the possible implication of sex steroids in the control of sex differences in the zebra finch auditory system, we evaluated via immunocytochemistry whether estrogens are produced and act in the zebra finch inner ear. Specifically we examined the distribution of aromatase, the enzyme converting testosterone into an estrogen, and of estrogen receptors of the alpha subtype (ERalpha) in adult zebra finch inner ears. The anatomy of the basilar papillae was visualized by fluorescein-phalloidin, which delineated the actin structure of hair cells and supporting cells at their apical surface. Whole mount preparations of basilar papillae stained by immunocytochemistry revealed in both males and females an abundant aromatase distribution in the cytoplasm of hair cells, while ERalpha was identified in the nuclei of hair cells and of underlying supporting cells. Double-labeled preparations confirmed the extensive co-localization of aromatase and ERalpha in the vast majority of the hair cells. These results are consistent with studies on non-avian species, suggesting a role for estrogens in auditory function. These findings are also consistent with the notion that estrogens may contribute to a sex difference in hearing. To our knowledge, this is the first demonstration of the presence of aromatase and of the co-localization of aromatase and ERalpha in the sensory epithelium of the inner ear in any animal model.
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http://dx.doi.org/10.1016/j.heares.2009.04.012DOI Listing
June 2009

Psychophysical evidence of damaged active processing mechanisms in Belgian Waterslager Canaries.

J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2009 Feb 12;195(2):193-202. Epub 2008 Dec 12.

Department of Psychology, University of Maryland, College Park, MD, 20742, USA.

Belgian Waterslager canaries (BWC), bred for a distinct low-pitched song, have an inherited high-frequency hearing loss associated with hair cell abnormalities. Hair cells near the abneural edge of the papilla, which receive primarily efferent innervation in normal birds, are among the most severely affected. These cells are thought to support nonlinear active processing in the avian ear, though the mechanisms are poorly understood. Here we present psychophysical evidence that suggests degraded active processing in BWC compared to normal-hearing non-BWC. Critical ratios, psychophysical masking patterns and phase effects on masking by harmonic complexes were measured in BWC and non-BWC using operant conditioning procedures. Critical ratios were much larger in BWC than in non-BWC at high frequencies. Psychophysical tuning curves derived from the masking patterns for BWC were broadened at high frequencies. BWC also showed severely reduced phase effects on masking by harmonic complexes compared to non-BWC. As has been hypothesized previously for hearing-impaired humans, these results are consistent with a loss of active processing mechanisms in BWC.
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http://dx.doi.org/10.1007/s00359-008-0398-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2884960PMC
February 2009

WDR1 presence in the songbird basilar papilla.

Hear Res 2008 Jun 15;240(1-2):102-11. Epub 2008 Apr 15.

Department of Biology, University of Maryland, Biology Psychology Building, College Park, MD 20742-0001, USA.

WD40 repeat 1 protein (WDR1) was first reported in the acoustically injured chicken inner ear, and bioinformatics revealed that WDR1 has numerous WD40 repeats, important for protein-protein interactions. It has significant homology to actin interacting protein 1 (Aip1) in several lower species such as yeast, roundworm, fruitfly and frog. Several studies have shown that Aip1 binds cofilin/actin depolymerizing factor, and that these interactions are pivotal for actin disassembly via actin filament severing and actin monomer capping. However, the role of WDR1 in auditory function has yet to be determined. WDR1 is typically restricted to hair cells of the normal avian basilar papilla, but is redistributed towards supporting cells after acoustic overstimulation, suggesting that WDR1 may be involved in inner ear response to noise stress. One aim of the present study was to resolve the question as to whether stress factors, other than intense sound, could induce changes in WDR1 presence in the affected avian inner ear. Several techniques were used to assess WDR1 presence in the inner ears of songbird strains, including Belgian Waterslager (BW) canary, an avian strain with degenerative hearing loss thought to have a genetic basis. Reverse transcription, followed by polymerase chain reactions with WDR1-specific primers, confirmed WDR1 presence in the basilar papillae of adult BW, non-BW canaries, and zebra finches. Confocal microscopy examinations, following immunocytochemistry with anti-WDR1 antibody, localized WDR1 to the hair cell cytoplasm along the avian sensory epithelium. In addition, little, if any, staining by anti-WDR1 antibody was observed among supporting cells in the chicken or songbird ear. The present observations confirm and extend the early findings of WDR1 localization in hair cells, but not in supporting cells, in the normal avian basilar papilla. However, unlike supporting cells in the acoustically damaged chicken basilar papilla, the inner ear of the BW canary showed little, if any, WDR1 up-regulation in supporting cells. This may be due to the fact that the BW canary already has established hearing loss and/or to the possibility that the mechanism(s) involved in BW hearing loss may not be related to WDR1.
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http://dx.doi.org/10.1016/j.heares.2008.03.008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4497556PMC
June 2008

Vocal learning in Budgerigars (Melopsittacus undulatus): effects of an acoustic reference on vocal matching.

J Acoust Soc Am 2008 Mar;123(3):1729-36

Department of Psychology, University of Maryland, College Park, Maryland 20742, USA.

Budgerigars were trained to produce specific vocalizations (calls) using operant conditioning and food reinforcement. The bird's call was compared to a digital representation of the call stored in a computer to determine a match. Once birds were responding at a high level of precision, we measured the effect of several manipulations upon the accuracy and the intensity of call production. Also, by differentially reinforcing other aspects of vocal behavior, budgerigars were trained to produce a call that matched another bird's contact call and to alter the latency of their vocal response. Both the accuracy of vocal matching and the intensity level of vocal production increased significantly when the bird could hear the template immediately before each trial. Moreover, manipulating the delay between the presentation of an acoustic reference and the onset of vocal production did not significantly affect either vocal intensity or matching accuracy. Interestingly, the vocalizations learned and reinforced in these operant experiments were only occasionally used in more natural communicative situations, such as when birds called back and forth to one another in their home cages.
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http://dx.doi.org/10.1121/1.2835440DOI Listing
March 2008