Bird speech perception and vocal production: a comparison with humans

Research into speech perception by nonhuman animals can be crucially informative in assessing whether specific perceptual phenomena in humans have evolved to decode speech, or reflect more general traits. Birds share with humans not only the capacity to use complex vocalizations for communication but also many characteristics of its underlying developmental and mechanistic processes; thus, birds are a particularly interesting group for comparative study. This review first discusses commonalities between birds and humans in perception of speech sounds. Several psychoacoustic studies have shown striking parallels in seemingly speech-specific perceptual phenomena, such as categorical perception of voice-onset-time variation, categorization of consonants that lack phonetic invariance, and compensation for coarticulation. Such findings are often regarded as evidence for the idea that the objects of human speech perception are auditory or acoustic events rather than articulations. Next, I highlight recent research on the production side of avian communication that has revealed the existence of vocal tract filtering and articulation in bird species-specific vocalization, which has traditionally been considered a hallmark of human speech production. Together, findings in birds show that many of characteristics of human speech perception are not uniquely human but also that a comparative approach to the question of what are the objects of perception--articulatory or auditory events--requires careful consideration of species-specific vocal production mechanisms.     

FoxP2 in song-learning birds and vocal-learning mammals

FoxP2 is the first identified gene that is specifically involved in speech and language development in humans. Population genetic studies of FoxP2 revealed a selective sweep in recent human history associated with two amino acid substitutions in exon 7. Avian song learning and human language acquisition share many behavioral and neurological similarities. To determine whether FoxP2 plays a similar role in song-learning birds, we sequenced exon 7 of FoxP2 in multiple song-learning and nonlearning birds. We show extreme conservation of FoxP2 sequences in birds, including unusually low rates of synonymous substitutions. However, no amino acid substitutions are shared between the song-learning birds and humans. Furthermore, sequences from vocal-learning whales, dolphins, and bats do not share the human-unique substitutions. While FoxP2 appears to be under strong functional constraints in mammals and birds, we find no evidence for its role during the evolution of vocal learning in nonhuman animals as in humans.     

Vocal-tract filtering by lingual articulation in a parrot

Human speech and bird vocalization are complex communicative behaviors with notable similarities in development and underlying mechanisms. However, there is an important difference between humans and birds in the way vocal complexity is generally produced. Human speech originates from independent modulatory actions of a sound source, e.g., the vibrating vocal folds, and an acoustic filter, formed by the resonances of the vocal tract (formants). Modulation in bird vocalization, in contrast, is thought to originate predominantly from the sound source, whereas the role of the resonance filter is only subsidiary in emphasizing the complex time-frequency patterns of the source (e.g., but see ). However, it has been suggested that, analogous to human speech production, tongue movements observed in parrot vocalizations modulate formant characteristics independently from the vocal source. As yet, direct evidence of such a causal relationship is lacking. In five Monk parakeets, Myiopsitta monachus, we replaced the vocal source, the syrinx, with a small speaker that generated a broad-band sound, and we measured the effects of tongue placement on the sound emitted from the beak. The results show that tongue movements cause significant frequency changes in two formants and cause amplitude changes in all four formants present between 0.5 and 10 kHz. We suggest that lingual articulation may thus in part explain the well-known ability of parrots to mimic human speech, and, even more intriguingly, may also underlie a speech-like formant system in natural parrot vocalizations.     

Prosody Discrimination by Songbirds (Padda oryzivora)

In human verbal communication, not only lexical information, but also paralinguistic information plays an important role in transmitting the speakers’ mental state. Paralinguistic information is conveyed mainly through acoustic features like pitch, rhythm, tempo and so on. These acoustic features are generally known as prosody. It is known that some species of birds can discriminate certain aspects of human speech. However, there have not been any studies on the discrimination of prosody in human language which convey different paralinguistic meanings by birds. In the present study, we have shown that the Java sparrow (Padda oryzivora) can discriminate different prosodic patterns of Japanese sentences. These birds could generalize prosodic discrimination to novel sentences, but could not generalize sentence discrimination to those with novel prosody. Moreover, unlike Japanese speakers, Java sparrows used the first part of the utterance as the discrimination cue.     

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

Speech spectrum's correlation with speakers' Eysenck personality traits

The current study explored the correlation between speakers' Eysenck personality traits and speech spectrum parameters. Forty-six subjects completed the Eysenck Personality Questionnaire. They were instructed to verbally answer the questions shown on a computer screen and their responses were recorded by the computer. Spectrum parameters of /sh/ and /i/ were analyzed by Praat voice software. Formant frequencies of the consonant /sh/ in lying responses were significantly lower than that in truthful responses, whereas no difference existed on the vowel /i/ speech spectrum. The second formant bandwidth of the consonant /sh/ speech spectrum was significantly correlated with the personality traits of Psychoticism, Extraversion, and Neuroticism, and the correlation differed between truthful and lying responses, whereas the first formant frequency of the vowel /i/ speech spectrum was negatively correlated with Neuroticism in both response types. The results suggest that personality characteristics may be conveyed through the human voice, although the extent to which these effects are due to physiological differences in the organs associated with speech or to a general Pygmalion effect is yet unknown.     

Species interactions and habitat associations of birds inhabiting urban areas of Sydney,Australia

Abstract The absence of small birds from many suburban areas may be due to adverse garden characteristics, interspecific aggression or human behaviour such as supplementary food provisioning that encourages predators. We investigated the relationship between these factors and the presence of seven small bird species in Sydney through a community‐based survey. The survey was conducted by participants over a 7‐day period between 7 am and 10 am in November and early December 2000. Three dominant species, the noisy miner (Manorina melanocephala), pied currawong (Strepera graculina) and common myna (Acridotheres tristis) were each present in over 59% of gardens. Each small bird species was present in less than 40% of gardens. All small birds were negatively associated with noisy miners, but only the silvereye (Zosterops lateralis) was negatively associated with pied currawongs. None of the species of small birds was negatively associated with common mynas. Four species of small birds were associated with at least one habitat variable, notably the proportion of native vegetation. Although more birds were recorded in gardens in which meat was provided, there were significantly fewer small birds in these gardens. There were also more birds recorded in gardens where seed was provided, with red‐browed finches (Neochmia temporalis) positively associated with seed provisioning in most regions of Sydney. The presence of dogs and cats was not related to the total abundance of birds overall or small birds in gardens. While garden characteristics may influence the presence of small birds to some degree, the presence of noisy miners, a species that are thought to aggressively exclude other species from their territories, is likely to be an important influence on these species in suburban areas. Furthermore, supplementary feeding by people is likely to negatively influence some small birds. The presence of carnivorous pets does not seem to influence the presence of small birds at the scale of the individual garden.     

Are large frugivorous birds better seed dispersers than medium‐ and small‐sized ones? Effect of body mass on seed dispersal effectiveness

Frugivorous birds vary in seed dispersal effectiveness (SDE) depending on their body mass. It has been suggested that large birds are more effective dispersers than small ones because they consume a large number of fruits, disperse seeds of distinct sizes, and transport seeds over long distances. Yet, few studies have evaluated the impact of body mass on SDE of birds. In this study, we compiled one database for the quantity (i.e., frequency of visits to plants and number of seeds removed per visit) and quality (i.e., germination of seeds after gut passage and gut retention time of seeds) of seed dispersal by frugivorous birds to evaluate the impact of body mass on SDE. In addition, we compiled data on plant characteristics such as life‐form, fruit type, number of seeds per fruit, and size of seed to evaluate their influence on the quantity and quality of seed dispersal. Data were analyzed with linear mixed effects models and quantile regressions to evaluate the relationship between body mass of birds and quantity, quality, and SDE, in addition to the influence of plant characteristics on SDE. The body mass of birds was negatively related to the frequency of visits to plants. Furthermore, it was positively related to the number of seeds removed per visit, although negatively related to seed size. The life‐form of plants was the only factor explaining the germination of seeds after gut passage. Yet, the body mass of birds was positively related to the gut retention time of seeds. Small and medium birds have a relatively higher SDE than large birds. These results differ from the assertion that large birds are more effective dispersers of plants. Small and medium birds are also effective dispersers of plants that should be preserved and protected from the impact of human activities.     

Stimulus Familiarity Affects Perceptual Restoration in the European Starling (Sturnus vulgaris)

Background

Humans can easily restore a speech signal that is temporally masked by an interfering sound (e.g., a cough masking parts of a word in a conversation), and listeners have the illusion that the speech continues through the interfering sound. This perceptual restoration for human speech is affected by prior experience. Here we provide evidence for perceptual restoration in complex vocalizations of a songbird that are acquired by vocal learning in a similar way as humans learn their language.

Methodology/Principal Findings

European starlings were trained in a same/different paradigm to report salient differences between successive sounds. The birds'' response latency for discriminating between a stimulus pair is an indicator for the salience of the difference, and these latencies can be used to evaluate perceptual distances using multi-dimensional scaling. For familiar motifs the birds showed a large perceptual distance if discriminating between song motifs that were muted for brief time periods and complete motifs. If the muted periods were filled with noise, the perceptual distance was reduced. For unfamiliar motifs no such difference was observed.

Conclusions/Significance

The results suggest that starlings are able to perceptually restore partly masked sounds and, similarly to humans, rely on prior experience. They may be a suitable model to study the mechanism underlying experience-dependent perceptual restoration.     

On human speech,syntax, and language

The evolution of human speech and syntax, which appear to be the defining characteristics of modern human beings, is discussed. Speech depends on the morphology of the mouth, tongue, and larynx which yield the human «vocal tract», and neural mechanisms that facilitate the perception of speech and make possible the control of the articulatory gestures that underly speech. The neural mechanisms that underly human syntax may have derived by means of the Darwinian process of preadaption from the structures of the brain that first evolved to facilitate speech motor control. Recent data consistent with this theory are presented; deficits in the comprehension of syntax of normal aged people are correlated with a slowdown in speech rate.     

Perception of Vocal Tract Resonances by Whooping Cranes Grus americana

Although formants (vocal tract resonances) can often be observed in avian vocalizations, and several bird species have been shown to perceive formants in human speech sounds, no studies have examined formant perception in birds' own species-specific calls. We used playbacks of computer-synthesized crane calls in a modified habituation—dishabituation paradigm to test for formant perception in whooping cranes ( Grus americana ). After habituating birds to recordings of natural contact calls, we played a synthesized replica of one of the habituating stimuli as a control to ensure that the synthesizer worked adequately; birds dishabituated in only one of 13 cases. Then, we played the same call with its formant frequencies shifted. The birds dishabituated to the formant-shifted calls in 10 out of 12 playbacks. These data suggest that cranes perceive and attend to changes in formant frequencies in their own species-specific vocalizations, and are consistent with the hypothesis that formants can provide acoustic cues to individuality and body size.     

Species differences in the identification of acoustic stimuli by birds

The perceptual organization of auditory stimuli can reveal a great deal about how the brain naturally groups events. The current study uses identification techniques to investigate the abilities of two species of birds in identifying zebra finch song as well as synthetically generated speech stimuli. Budgerigars (Melopsittacus undulatus) and zebra finches (Taeniopygia guttata) were trained to differentially peck keys in response to the presentation of various complex stimuli. Although there were no clear differences in performance during the training paradigm between the two species, budgerigars were far more adept at learning to identify both sets of complex stimuli than were zebra finches, requiring far less trials to reach criterion. The non-singing but vocally plastic budgerigars vastly outperformed zebra finches at identifying both zebra finch song and synthetically designed human speech despite known similarities in auditory sensitivities between the two species and seemingly equivalent learning capacity. The flexibility that budgerigars seem to have at identifying various stimuli is highlighted by their enhanced performance in these tasks. These results are discussed in the context of what is known about both general and specialized processes which may contribute to any differences or similarities in performance.     

Localized brain activation related to the strength of auditory learning in a parrot

Parrots and songbirds learn their vocalizations from a conspecific tutor, much like human infants acquire spoken language. Parrots can learn human words and it has been suggested that they can use them to communicate with humans. The caudomedial pallium in the parrot brain is homologous with that of songbirds, and analogous to the human auditory association cortex, involved in speech processing. Here we investigated neuronal activation, measured as expression of the protein product of the immediate early gene ZENK, in relation to auditory learning in the budgerigar (Melopsittacus undulatus), a parrot. Budgerigar males successfully learned to discriminate two Japanese words spoken by another male conspecific. Re-exposure to the two discriminanda led to increased neuronal activation in the caudomedial pallium, but not in the hippocampus, compared to untrained birds that were exposed to the same words, or were not exposed to words. Neuronal activation in the caudomedial pallium of the experimental birds was correlated significantly and positively with the percentage of correct responses in the discrimination task. These results suggest that in a parrot, the caudomedial pallium is involved in auditory learning. Thus, in parrots, songbirds and humans, analogous brain regions may contain the neural substrate for auditory learning and memory.     

Low-Arousal Speech Noise Improves Performance in N-Back Task: An ERP Study

The relationship between noise and human performance is a crucial topic in ergonomic research. However, the brain dynamics of the emotional arousal effects of background noises are still unclear. The current study employed meaningless speech noises in the n-back working memory task to explore the changes of event-related potentials (ERPs) elicited by the noises with low arousal level vs. high arousal level. We found that the memory performance in low arousal condition were improved compared with the silent and the high arousal conditions; participants responded more quickly and had larger P2 and P3 amplitudes in low arousal condition while the performance and ERP components showed no significant difference between high arousal and silent conditions. These findings suggested that the emotional arousal dimension of background noises had a significant influence on human working memory performance, and that this effect was independent of the acoustic characteristics of noises (e.g., intensity) and the meaning of speech materials. The current findings improve our understanding of background noise effects on human performance and lay the ground for the investigation of patients with attention deficits.     

Birds at a Southern California beach: seasonality, habitat use and disturbance by human activity

Use of a Santa Barbara beach by people and birds varied in both time and space. There were 100 birds, 18 people and 2 dogs per kilometer. Bird density varied primarily with the season and tide while human activity varied most between weekend and weekday. Bird distributions along the beach were determined mainly by habitat type (particularly a lagoon and exposed rocky intertidal areas) For crows and western gulls, there was some evidence that access to urban refuse increased abundance. Interactions between birds and people often caused birds to move or fly away, particularly when people were within 20 m. During a short observation period, 10% of humans and 39% of dogs disturbed birds. More than 70% of birds flew when disturbed. Bird species varied in the frequency that they were disturbed, partially because a few bird species foraged on the upper beach where contact with people was less frequent. Most disturbances occurred low on the beach. Although disturbances caused birds to move away from humans, most displacement was short enough that variation in human activity did not alter large-scale patterns of beach use by the birds. Birds were less reactive to humans (but not dogs) when beach activity was low.     

Movement Coordination during Conversation

Behavioral coordination and synchrony contribute to a common biological mechanism that maintains communication, cooperation and bonding within many social species, such as primates and birds. Similarly, human language and social systems may also be attuned to coordination to facilitate communication and the formation of relationships. Gross similarities in movement patterns and convergence in the acoustic properties of speech have already been demonstrated between interacting individuals. In the present studies, we investigated how coordinated movements contribute to observers’ perception of affiliation (friends vs. strangers) between two conversing individuals. We used novel computational methods to quantify motor coordination and demonstrated that individuals familiar with each other coordinated their movements more frequently. Observers used coordination to judge affiliation between conversing pairs but only when the perceptual stimuli were restricted to head and face regions. These results suggest that observed movement coordination in humans might contribute to perceptual decisions based on availability of information to perceivers.     

The Evolution of Language: A Comparative Review

For many years the evolution of language has been seen as a disreputable topic, mired in fanciful “just so stories” about language origins. However, in the last decade a new synthesis of modern linguistics, cognitive neuroscience and neo-Darwinian evolutionary theory has begun to make important contributions to our understanding of the biology and evolution of language. I review some of this recent progress, focusing on the value of the comparative method, which uses data from animal species to draw inferences about language evolution. Discussing speech first, I show how data concerning a wide variety of species, from monkeys to birds, can increase our understanding of the anatomical and neural mechanisms underlying human spoken language, and how bird and whale song provide insights into the ultimate evolutionary function of language. I discuss the “descended larynx” of humans, a peculiar adaptation for speech that has received much attention in the past, which despite earlier claims is not uniquely human. Then I will turn to the neural mechanisms underlying spoken language, pointing out the difficulties animals apparently experience in perceiving hierarchical structure in sounds, and stressing the importance of vocal imitation in the evolution of a spoken language. Turning to ultimate function, I suggest that communication among kin (especially between parents and offspring) played a crucial but neglected role in driving language evolution. Finally, I briefly discuss phylogeny, discussing hypotheses that offer plausible routes to human language from a non-linguistic chimp-like ancestor. I conclude that comparative data from living animals will be key to developing a richer, more interdisciplinary understanding of our most distinctively human trait: language.     

Differences in measures of boldness even when underlying behavioral syndromes are present in two populations of the song sparrow (<Emphasis Type="Italic">Melospiza melodia</Emphasis>)

One commonly studied behavioral syndrome is the correlation between aggression and boldness. Studies in song sparrows (M. melodia) have found greater aggression and boldness in urban populations and a correlation between aggression and boldness in rural populations, but not within urban populations. In previous studies, boldness was measured as flight initiation distance (FID), which may reflect habituation by urban birds to human presence. In this study, we measured boldness using playbacks of heterospecific alarm calls and investigated whether higher boldness is a general trait of urban birds and whether the same pattern of correlations between aggression and boldness would be seen. We conducted trials involving FID, alarm call playbacks and conspecific song playbacks on 25 birds from both an urban and a rural site. The results showed that urban birds were bolder, as measured by FID and response to alarm calls. Boldness and aggression were correlated in rural birds with each method of measuring boldness but were correlated in urban birds only when using alarm call playbacks. Our results suggest that a behavioral syndrome exists in both urban and rural populations but that urban birds are able to decrease their response to human disturbance.     

Superfast vocal muscles control song production in songbirds

Birdsong is a widely used model for vocal learning and human speech, which exhibits high temporal and acoustic diversity. Rapid acoustic modulations are thought to arise from the vocal organ, the syrinx, by passive interactions between the two independent sound generators or intrinsic nonlinear dynamics of sound generating structures. Additionally, direct neuromuscular control could produce such rapid and precisely timed acoustic features if syringeal muscles exhibit rare superfast muscle contractile kinetics. However, no direct evidence exists that avian vocal muscles can produce modulations at such high rates. Here, we show that 1) syringeal muscles are active in phase with sound modulations during song over 200 Hz, 2) direct stimulation of the muscles in situ produces sound modulations at the frequency observed during singing, and that 3) syringeal muscles produce mechanical work at the required frequencies and up to 250 Hz in vitro. The twitch kinematics of these so-called superfast muscles are the fastest measured in any vertebrate muscle. Superfast vocal muscles enable birds to directly control the generation of many observed rapid acoustic changes and to actuate the millisecond precision of neural activity into precise temporal vocal control. Furthermore, birds now join the list of vertebrate classes in which superfast muscle kinetics evolved independently for acoustic communication.