Perceptual organization of acoustic stimuli by budgerigars (Melopsittacus undulatus): III. Contact calls

We trained budgerigars by operant conditioning to discriminate among a set of contact calls in a same-different task and analyzed response latencies from this task by using multidimensional-scaling (MDS) and cluster-analysis procedures. Humans listened to the same calls and indicated the similarity between pairs of calls by a direct rating procedure. An MDS program (sindscal) was used to arrange these complex acoustic stimuli in multidimensional space reflecting perceptual organization. Multiple regression techniques were used to identify the acoustic characteristics of contact calls that were correlated with the perceptual dimensions obtained from MDS. A number of spectral characteristics (e.g., peak frequency, rate of frequency modulation, and concentration of spectral energy) emerged as important for both budgerigars and humans, but the relative salience of these cues differed for the two species. Additional tests with two groups of budgerigars--cagemates and noncagemates--showed that experience with calls can change the salience of various acoustic characteristics used for perceptual organization and individual recognition.     

Speech perception by budgerigars (Melopsittacus undulatus): spoken vowels

Discrimination of natural, sustained vowels was studied in 5 budgerigars. The birds were trained using operant conditioning procedures on a same-different task, which was structured so that response latencies would provide a measure of stimulus similarity. These response latencies were used to construct similarity matrices, which were then analyzed by multidimensional scaling (MDS) procedures. MDS produced spatial maps of these speech sounds where perceptual similarity was represented by spatial proximity. The results of the three experiments suggest that budgerigars perceive natural, spoken vowels according to phonetic categories, find the acoustic differences among different talkers less salient than the acoustic differences among vowel categories, and use formant frequencies in making these complex discriminations.     

Perceptual organization of acoustic stimuli by budgerigars (Melopsittacus undulatus): I. Pure tones

A new combination of operant conditioning and psychophysical scaling procedures was used to study auditory perception in a small bird. In a same-different discrimination task, budgerigars learned to discriminate among pure tones that varied along one or more acoustic dimensions. Response latencies were used to generate a matrix of interstimulus similarities. Multidimensional scaling procedures were used to arrange these acoustic stimuli in a multidimensional space that supposedly reflects the bird's perceptual organization. For tones that varied in intensity, duration, and frequency simultaneously, budgerigars were much more sensitive to frequency changes. From a set of tones that varied only in intensity, it was possible to calculate the growth of loudness with intensity for the budgerigar. For tones that varied only in frequency, budgerigars showed evidence of an "acoustic fovea" for frequency change in the spectral region of 2-4 kHz. Budgerigars and humans also differed in their perceptual grouping of tone sequences that rise, fall, or remain constant in pitch. Surprisingly, budgerigars were much less responsive to pitch contour than were humans.     

Speech perception by budgerigars(Melopsittacus undulatus): The voiced-voiceless distinction

Discrimination of synthetic speech sounds from the bilabial, alveolar,and velar voice onset time (VOT) series was studied in 5 budgerigars. The birds were trained, using operant conditioning procedures, to detect changes in a repeating background of sound consisting of a synthetic speech token. Response latencies for detection were measured and were used to construct similarity matrices. Multidimensional scaling procedures were then used to produce spatial maps of these speech sounds, in which perceptual similarity was represented by spatial proximity. The results of these experiments suggest that budgerigars discriminate among synthetic speech sounds from these three VOT continua, especially between those from the bilabial and alveolar series, in a categorical fashion.     

The discrimination of temporal fine structure in call-like harmonic sounds by birds

Thresholds for discriminating changes in the temporal fine structure of call-like, harmonic sounds were measured in zebra finches (Taeniopygia guttata) and budgerigars (Melopsittacus undulatus). Birds could detect changes in periods as short as 1.225 ms at near 100% accuracy even when spectral and envelope cues were identical, as in time-reversed stimuli. Humans performed poorly on such stimuli, paralleling results from previous studies. Bird thresholds were in the range of those reported in neurophysiological studies of the songbird high vocal center (HVC) to temporally modified conspecific songs. Taken together, these results show that birds can hear differences in temporal fine structure in their natural vocalizations that go beyond human capabilities, but whether these abilities have communicative relevance remains to be seen.     

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

The long, rambling warble song of male budgerigars is composed of a large number of acoustically complex elements uttered in streams lasting minutes a time and accompanied by various courtship behaviors. Warble song has no obvious sequential structure or patterned repetition of elements, raising questions as to which aspects of it are perceptually salient, whether budgerigars can detect changes in natural warble streams, and to what extent these capabilities are species-specific. Using operant conditioning and a psychophysical paradigm, we examined the sensitivity of budgerigars, canaries, and zebra finches to changes in long (>6?min) natural warble sequences of a male budgerigar. All three species could detect a single insertion of pure tones, zebra finch song syllables, budgerigar contact calls, or warble elements from another budgerigar’s warble. In each case, budgerigars were more sensitive to these changes than were canaries or finches. When warble elements from the ongoing warble stream were used as targets and inserted, out of order, into the natural warble stream so that the only cue available was the violation of the natural ordering of warble elements, only budgerigars performed above chance. When the experiment was repeated with all the ongoing warble stream elements presented in random order, the performance of budgerigars fell to chance. These results show species-specific advantages in budgerigars for detecting acoustic changes in natural warble sequences and indicate at least a limited sensitivity to sequential rules governing the structure of their species-specific warble songs.     

Effect of acoustic cue modifications on evoked vocal response to calls in zebra finches (Taeniopygia guttata)

Besides their song, which is usually a functionally well-defined communication signal with an elaborate acoustic structure, songbirds also produce a variety of shorter vocalizations named calls. While a considerable amount of work has focused on information coding in songs, little is known about how calls' acoustic structure supports communication processes. Because male and female zebra finches use calls during most of their interactions and answer to conspecific calls without visual contact, we aimed at identifying which calls' acoustic cues are necessary to elicit a vocal response. Using synthetic zebra finch calls, we examined evoked vocal response of male and female zebra finches to modified versions of the distance calls. Our results show that the vocal response of zebra finches to female calls requires the full harmonic structure of the call, whereas the frequency downsweep of male calls is necessary to evoke a vocal response. It is likely that both female and male calls require matching a similar frequency bandwidth to trigger a response in conspecific individuals.     

Ear differences in the recall of fricatives and vowels

Two experiments on the free recall of dichotically presented synthetic speech sounds are reported. The first shows that the right ear advantage for initial fricative consonants is not simply a function of the recognition response class, but that it is also a function of the particular acoustic cues used to achieve that response. This is true both for the whole response, and for the constituent phonetic features. The second experiment shows that when both the response class and the particular stimuli presented on certain trials are held constant, the right ear advantage for the constant stimuli can be influenced by the range of other stimuli occurring in the experiment. Vowels show a right ear advantage when, within the experiment, there is uncertainty as to vocal tract size, but they show no ear advantage when all the vowels in the experiment are from the same vocal tract. These results are interpreted as demonstrating that there are differences between the ears, and probably between the hemispheres, at some stage between the acoustic analysis of the signal and its identification as a phonetic category.     

Auditory perception of conspecific and heterospecific vocalizations in birds: evidence for special processes.

Budgerigars (Melopsittacus undulatus), canaries (Serinus canaria), and zebra finches (Poephila guttata castanotis) were tested for their ability to discriminate among distance calls of each species. For comparison, starlings (Sturnus vulgaris) were tested on the same sounds. Response latencies to detect a change in a repeating background of sound were taken as a measure of the perceptual similarity among calls. All 4 species showed clear evidence of 3 perceptual categories corresponding to the calls of the 3 species. Also, budgerigars, canaries, and zebra finches showed an enhanced ability to discriminate among calls of their own species over the calls of the others. Starlings discriminated more efficiently among canary calls than among budgerigar or zebra finch calls. The results show species differences in discrimination of species-specific acoustic communication signals and provide insight into the nature of specialized perceptual processes.     

Is acoustic evaluation in a non-primate mammal,the tree shrew,affected by context?

Sound categorisation plays a crucial role for processing ecological and social stimuli in a species’ natural environment. To explore the discrimination and evaluation of sound stimuli in human babies and nonhuman primates, a reciprocal habituation-dishabituation paradigm has been successfully introduced into auditory research. We applied the reciprocal paradigm for the first time to a non-primate mammal, the tree shrew (Tupaia belangeri), to examine to what extent non-primate mammals share the ability to evaluate communication calls with primates. Playback stimuli were three types of communication calls, differing distinctively in context and acoustic structure, as well as two artificial control sounds, differing solely in frequency. We assessed the attention towards the playback stimuli by the latency to respond to the test stimulus. Subjects evaluated pairs of communication call types as well as the artificial playback stimuli. Attention towards the test stimuli differed significantly in strength for one pair of communication calls, with subjects dishabituating faster to one category than the other. The comparison of a second pair of communication calls did not show significant differences. Interestingly, subjects also evaluated the artificial control sounds. Findings are only partly in line with results on human and non-human primates. They provided first evidence that in non-primate mammals acoustic evaluation is not solely affected by the sound-associated context but is also linked to unusualness and acoustic cues, such as peak frequency.     

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

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

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

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

Effects of lesions of the central nucleus of the anterior archistriatum on contact call and warble song production in the budgerigar (Melopsittacus undulatus)

We studied the effects of both unilateral and bilateral lesions of the central nucleus of the anterior archistriatum (AAc) on the production of contact calls and warble song in adult male and female budgerigars. Birds were sorted into three experimental groups based on the percentage of AAc destroyed and whether lesions were unilateral or bilateral. The experimental groups were Unilateral Lesion (N = 8), Partial Bilateral Lesion (N = 5), and Bilateral Lesion birds (N = 12). Each group contained both sexes. Unilateral lesions had no demonstrable effects on contact call or warble song production. Bilateral lesions resulted in immediate and permanent disruption of all learned temporal and spectral characteristics of contact calls, although call initiation was not dependent on the AAc. Partial bilateral lesion effects varied with lesion size and location. At least 20-30% sparing of the AAc, including sparing portions of both the dorsal (AAcd) and ventral (AAcv) subdivisions on the same side of the brain, is necessary for production of prelesion contact call patterns. Warble song was absent in birds with complete bilateral destruction. Two birds with large yet incomplete lesions of the AAc sang after surgery, although the warble song of these birds was extremely impoverished and contained only a few of the typical warble song elements. Lesion results indicate that the AAc mediates the production of learned vocal features in male and female budgerigars, with each hemisphere capable of supporting a normal vocal repertoire.     

Horse (Equus caballus) whinnies: a source of social information

Many animal species that rely mainly on calls to communicate produce individual acoustic structures, but we wondered whether individuals of species better known as visual communicants, with small vocal repertoires, would also exhibit individual distinctiveness in calls. Moreover, theoretical advances concerning the evolution of social intelligence are usually based on primate species data, but relatively little is known about the social cognitive capacities of non-primate mammals. However, some non-primate species demonstrate auditory recognition of social categories and possess mental representation of their social network. Horses (Equus caballus) form stable social networks and although they display a large range of visual signals, they also use long-distance whinny calls to maintain contact. Here, we investigated the potential existence of individual acoustic signatures in whinny calls and the ability of horses to discriminate by ear individuals varying in their degree of familiarity. Our analysis of the acoustic structure of whinnies of 30 adult domestic horses (ten stallions, ten geldings, ten mares) revealed that some of the frequency and temporal parameters carried reliable information about the caller’s sex, body size and identity. However, no correlations with age were found. Playback experiments evaluated the behavioural significance of this variability. Twelve horses heard either control white noise or whinnies emitted by group members, familiar neighbours or unfamiliar horses. While control sounds did not induce any particular response, horses discriminated the social category of the callers and reacted with a sound-specific behaviour (vigilance and attraction varied with familiarity). Our results support the existence of social knowledge in horses and suggest a process of vocal coding/decoding of information.     

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

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

When voices get emotional: A corpus of nonverbal vocalizations for research on emotion processing

Nonverbal vocal expressions, such as laughter, sobbing, and screams, are an important source of emotional information in social interactions. However, the investigation of how we process these vocal cues entered the research agenda only recently. Here, we introduce a new corpus of nonverbal vocalizations, which we recorded and submitted to perceptual and acoustic validation. It consists of 121 sounds expressing four positive emotions (achievement/triumph, amusement, sensual pleasure, and relief) and four negative ones (anger, disgust, fear, and sadness), produced by two female and two male speakers. For perceptual validation, a forced choice task was used (n = 20), and ratings were collected for the eight emotions, valence, arousal, and authenticity (n = 20). We provide these data, detailed for each vocalization, for use by the research community. High recognition accuracy was found for all emotions (86 %, on average), and the sounds were reliably rated as communicating the intended expressions. The vocalizations were measured for acoustic cues related to temporal aspects, intensity, fundamental frequency (f0), and voice quality. These cues alone provide sufficient information to discriminate between emotion categories, as indicated by statistical classification procedures; they are also predictors of listeners’ emotion ratings, as indicated by multiple regression analyses. This set of stimuli seems a valuable addition to currently available expression corpora for research on emotion processing. It is suitable for behavioral and neuroscience research and might as well be used in clinical settings for the assessment of neurological and psychiatric patients. The corpus can be downloaded from Supplementary Materials.     

Generalizing prosodic patterns by a non-vocal learning mammal

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

Perception of mistuned harmonics in complex sounds by the bullfrog (Rana catesbeiana)

The ability of 73 male bullfrogs (Rana catesbeiana) to detect single mistuned harmonics in an otherwise periodic signal was studied. Bullfrogs in their natural environment were presented with playbacks of synthetic signals, resembling their species advertisement calls, that differed in the frequency of 1 harmonic component (out of 22). There were significant differences in the number and latency of the males' evoked vocal responses to these stimuli, suggesting that males were sensitive to the differences between the sounds. Differences in envelope shape (rate and depth of amplitude modulation) produced by the harmonic mistunings may underlie the differences in response. Frogs, like birds and humans, can discriminate sounds on the basis of harmonic structure, indicating that this is a general perceptual trait shared among vertebrates.     

Perception of distance calls by budgerigars (Melopsittacus undulatus) and zebra finches (Poephila guttata): assessing species-specific advantages

Budgerigars (Melopsittacus undulatus) and zebra finches (Poephila guttata) share a common functional class of vocalizations called distance calls. The perception of species-specific distance calls by both species was measured with a habituation-dishabituation operant paradigm. Changes in discrimination performance were noted as listening conditions were modified or stimulus properties were altered. Both species showed better performance for calls of their own species. For zebra finches this tendency increased slightly when a background noise was added to the testing environment. Shifting the frequency region of the calls affected the discrimination performance of male budgerigars but not females or zebra finches. Reversing the temporal order of the calls affected the perceptual advantage for conspecific vocalizations in zebra finches but not in budgerigars. These results highlight species differences in perceiving acoustic communication signals.