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Nonlinear analysis of irregular animal vocalizations.

Animal vocalizations range from almost periodic vocal-fold vibration to completely atonal turbulent noise. Between these two extremes, a variety of nonlinear dynamics such as limit cycles, subharmonics, biphonation, and chaotic episodes have been recently observed. These observations imply possible functional roles of nonlinear dynamics in animal acoustic communication. Nonlinear dynamics may also provide insight into the degree to which detailed features of vocalizations are under close neural control, as opposed to more directly reflecting biomechanical properties of the vibrating vocal folds themselves. So far, nonlinear dynamical structures of animal voices have been mainly studied with spectrograms. In this study, the deterministic versus stochastic (DVS) prediction technique was used to quantify the amount of nonlinearity in three animal vocalizations: macaque screams, piglet screams, and dog barks. Results showed that in vocalizations with pronounced harmonic components (adult macaque screams, certain piglet screams, and dog barks), deterministic nonlinear prediction was clearly more powerful than stochastic linear prediction. The difference, termed low-dimensional nonlinearity measure (LNM), indicates the presence of a low-dimensional attractor. In highly irregular signals such as juvenile macaque screams, piglet screams, and some dog barks, the detectable amount of nonlinearity was comparatively small. Analyzing 120 samples of dog barks, it was further shown that the harmonic-to-noise ratio (HNR) was positively correlated with LNM. It is concluded that nonlinear analysis is primarily useful in animal vocalizations with strong harmonic components (including subharmonics and biphonation) or low-dimensional chaos.

Animals↗

Meaning and emotion in animal vocalizations.

Historically, a dichotomy has been drawn between the semantic communication of human language and the apparently emotional calls of animals. Current research paints a more complicated picture. Just as scientists have identified elements of human speech that reflect a speaker's emotions, field experiments have shown that the calls of many animals provide listeners with information about objects and events in the environment. Like human speech, therefore, animal vocalizations simultaneously provide others with information that is both semantic and emotional. In support of this conclusion, we review the results of field experiments on the natural vocalizations of African vervet monkeys, diana monkeys, baboons, and suricates (a South African mongoose). Vervet and diana monkeys give acoustically distinct alarm calls in response to the presence of leopards, eagles, and snakes. Each alarm call type elicits a different, adaptive response from others nearby. Field experiments demonstrate that listeners compare these vocalizations not just according to their acoustic properties but also according to the information they convey. Like monkeys, suricates give acoustically distinct alarm calls in response to different predators. Within each predator class, the calls also differ acoustically according to the signaler's perception of urgency. Like speech, therefore, suricate alarm calls convey both semantic and emotional information. The vocalizations of baboons, like those of many birds and mammals, are individually distinctive. As a result, when one baboon hears a sequence of calls exchanged between two or more individuals, the listener acquires information about social events in its group. Baboons, moreover, are skilled "eavesdroppers:" their response to different call sequences provides evidence of the sophisticated information they acquire from other individuals' vocalizations. Baboon males give loud "wahoo" calls during competitive displays. Like other vocalizations, these highly emotional calls provide listeners with information about the caller's dominance rank, age, and competitive ability. Although animal vocalizations, like human speech, simultaneously encode both semantic and emotional information, they differ from language in at least one fundamental respect. Although listeners acquire rich information from a caller's vocalization, callers do not, in the human sense, intend to provide it. Listeners acquire information as an inadvertent consequence of signaler behavior.

Acoustics↗

Wireless microphone for studies of animal vocalizations.

A microphone collar for obtaining good quality recordings of animal vocalizations is described. An inexpensive, commercially available wireless microphone was modified and mounted on a collar with a hearing-aidbattery pack. The complete assembly weighs 25 g, and is readily accepted by domestic cats.

Animals↗

The influence of surface atmospheric conditions on the range and area reached by animal vocalizations.

Low-level vertical changes in temperature and wind exert powerful and predictable influences on the area ensonified by animal vocalizations. Computer modelling of low-frequency sound propagation in measured atmospheric conditions predicts that the calls of the savanna elephant at these frequencies can have ranges exceeding 10 km and that the calls will be highly directional in the presence of wind shear. Calling area is maximized under temperature inversions with low wind speeds. Calling area changes substantially over 24 h periods; on any given day, the calling area undergoes an expansion and contraction which may be as large as one order of magnitude. This cycle is modulated by topography, regional weather patterns, seasonality and possibly by climate variation. Similar influences affect the somewhat higher-frequency calls of lions and may be a selective pressure towards their crepuscular and nocturnal calling behaviour. Coyotes and wolves, which also live in areas with strong and prevalent nocturnal temperature inversions, show similar calling patterns, maximizing their chances of being heard over the longest possible distances. The pronounced dawn and evening vocalization peaks in other animals including birds, frogs and insects may reflect the same influences in combination with other factors which selectively limit high-frequency sound propagation. Atmospheric conditions therefore need to be taken into account in many field studies of animal behaviour. A simplified method for estimating sound propagation during field studies is presented.

Animals↗

Using self-organizing maps to recognize acoustic units associated with information content in animal vocalizations.

Kohonen self-organizing neural networks, also called self-organizing maps (SOMs), have been used successfully to recognize human phonemes and in this way to aid in human speech recognition. This paper describes how SOMS also can be used to associate specific information content with animal vocalizations. A SOM was used to identify acoustic units in Gunnison's prairie dog alarm calls that were vocalized in the presence of three different predator species. Some of these acoustic units and their combinations were found exclusively in the alarm calls associated with a particular predator species and were used to associate predator species information with individual alarm calls. This methodology allowed individual alarm calls to be classified by predator species with an average of 91% accuracy. Furthermore, the topological structure of the SOM used in these experiments provided additional insights about the acoustic units and their combinations that were used to classify the target alarm calls. An important benefit of the methodology developed in this paper is that it could be used to search for groups of sounds associated with information content for any animal whose vocalizations are composed of multiple simultaneous frequency components.

Animals↗

Generalized perceptual linear prediction features for animal vocalization analysis.

A new feature extraction model, generalized perceptual linear prediction (gPLP), is developed to calculate a set of perceptually relevant features for digital signal analysis of animal vocalizations. The gPLP model is a generalized adaptation of the perceptual linear prediction model, popular in human speech processing, which incorporates perceptual information such as frequency warping and equal loudness normalization into the feature extraction process. Since such perceptual information is available for a number of animal species, this new approach integrates that information into a generalized model to extract perceptually relevant features for a particular species. To illustrate, qualitative and quantitative comparisons are made between the species-specific model, generalized perceptual linear prediction (gPLP), and the original PLP model using a set of vocalizations collected from captive African elephants (Loxodonta africana) and wild beluga whales (Delphinapterus leucas). The models that incorporate perceptional information outperform the original human-based models in both visualization and classification tasks.

Acoustics↗

The phonetic potential of nonhuman vocal tracts: comparative cineradiographic observations of vocalizing animals.

For more than a century it has been noted that the adult human vocal tract differs from that of other mammals, in that the resting position of the larynx is much lower in humans. While animals habitually breathe with the larynx inserted into the nasal cavity, adult humans are unable to do this. This anatomical difference has been cited as an important factor limiting the vocal potential of nonhuman animals, because the low larynx of humans allows a wider range of vocal tract shapes and thus formant patterns than is available to other species. However, it is not clear that the static anatomy of dead animals provides an accurate guide to the phonetic potential of the living animal's vocal tract. Here I present X-ray video observations of four mammal species (dogs Canis familiaris, goats Capra hircus, pigs Sus scrofa and cotton-top tamarins Sagunius oedipus). In all four species, the larynx was lowered from the nasopharynx, and the velum was closed, during loud calls. In dogs this temporary lowering was particularly pronounced. Although preliminary, these results suggest that the nonhuman vocal tract is more flexible than previously supposed, and that static postmortem anatomy provides an incomplete guide to the phonetic potential of nonhuman animals. The implications of these findings for theories of speech evolution are discussed.

Adult↗

A microprocessor system for the digital synthesis of pulsed and continuous discharges of electric fish (or animal vocalizations).

Traditionally, the sensitivity of electric fish to electric stimuli has been investigated using a variety of electronically generated signal functions, for example sine, square, and sawtooth waves (both continuous and pulsed). None of these resemble the species- or sex-specific electric organ discharges (EODs) of fish. Therefore, EODs recorded on magnetic tape were used in open-loop playback experiments. However, as shown in the present paper, the waveforms of EODs reproduced from magnetic tape are distorted, and cannot be manipulated with speed and accuracy as to frequency or pulse repetition rate by feedback from the experiment. Good EOD imitations are generated by our microprocessor-based system for the digital synthesis of EODs which is controlled by a small 'personal computer'. Digitized EOD samples edited by computer are output by the fast digital-to-analogue converter of the microprocessor system. This system was devised for the synthesis of pulse-type (discontinuous) and wave type (continuous) EODs with continuous, on-line frequency and amplitude control. The rate of digital synthesis is 500 kHz in pulse-type EODs, and 250-500 kHz in wave type EODs at 0.06-0.24 Hz frequency resolution, depending on the repetition frequency of the synthesized wave EOD. The present paper describes the steps in EOD synthesis, and indicates some applications which benefit from the playback of high-fidelity imitations of natural EODs at amplitudes and frequencies selected by the experimenter, or automatically controlled by feedback from the experiment in closed-loop applications.

Analog-Digital Conversion↗

Is voice processing species-specific in human auditory cortex? An fMRI study.

Recent studies suggested a sensitivity of regions of the human superior temporal sulcus (STS) to the sound of the human voice. However, the question of the species specificity of this response is still open. Healthy adult volunteers were scanned in an event-related fMRI design to compare responses in the STS to human and animal vocalizations, as well as to control nonvocal sounds (e.g., musical instruments). Bilateral activation of anterior STS was observed for human vocalizations, when contrasted with both nonvocal sounds and animal vocalizations. Animal vocalizations, compared to nonvocal sounds, elicited a more restricted left STS activation, although this region responded even more strongly to human vocalizations. This study provides the first evidence suggesting a species specificity in STS responses to vocalizations in humans.

Acoustic Stimulation↗

[Function and morphology of the larynx of the domestic guinea pig. An animal model for laryngologic and phoniatric research?].

The present study was undertaken to collect data on fundamental functional and morphological features of the guinea pig larynx using frequency analysis of animal vocalizations and light and scanning electron microscopy. Vocalizations of healthy animals were recorded in an anechoic chamber and were analyzed with short-time fourier transformation (color spectrograms). From the multitude of vocalization patterns produced by the guinea pig, distress squeals were selected as a typical, reproducible, voiced sound. These were stereotyped, upward-frequency modulated, multiharmonic signals with a formant-like structure. The fundamental frequency of this sound rose by about 1.5 octaves and reached up to 6 kHz near the end of the call. The different regions of the endolaryngeal epithelia showed morphological properties that corresponded to proposed functional significance. Keratinized squamous epithelium covered the supraglottic region. The marginal rim of the vocal cord was covered by a very thin epithelium with very flat cells covered with short microvilli. The subepithelial space was filled with loose connective tissue. The subglottic region was covered by respiratory epithelia. Based on these findings, we propose that the larynx of the guinea pig can be used as a model in phoniatric and laryngological research.

Animals↗

Template-based automatic recognition of birdsong syllables from continuous recordings.

The application of dynamic time warping (DTW) to the automated analysis of continuous recordings of animal vocalizations is evaluated. The DTW algorithm compares an input signal with a set of predefined templates representative of categories chosen by the investigator. It directly compares signal spectrograms, and identifies constituents and constituent boundaries, thus permitting the identification of a broad range of signals and signal components. When applied to vocalizations of an indigo bunting (Passerina cyanea) and a zebra finch (Taeniopygia guttata) collected from a low-clutter, low-noise environment, the recognizer identifies syllables in stereotyped songs and calls with greater than 97% accuracy. Syllables of the more variable and lower amplitude indigo bunting plastic song are identified with approximately 84% accuracy. Under restricted recordings conditions, this technique apparently has general applicability to analysis of a variety of animal vocalizations and can dramatically decrease the amount of time spent on manual identification of vocalizations.

Animals↗

Aggression, anxiety and vocalizations in animals: GABAA and 5-HT anxiolytics.

A continuing challenge for preclinical research on anxiolytic drugs is to capture the affective dimension that characterizes anxiety and aggression, either in their adaptive forms or when they become of clinical concern. Experimental protocols for the preclinical study of anxiolytic drugs typically involve the suppression of conditioned or unconditioned social and exploratory behavior (e.g., punished drinking or social interactions) and demonstrate the reversal of this behavioral suppression by drugs acting on the benzodiazepine-GABAA complex. Less frequently, aversive events engender increases in conditioned or unconditioned behavior that are reversed by anxiolytic drugs (e.g., fear-potentiated startle). More recently, putative anxiolytics which target 5-HT receptor subtypes produced effects in these traditional protocols that often are not systematic and robust. We propose ethological studies of vocal expressions in rodents and primates during social confrontations, separation from social companions, or exposure to aversive environmental events as promising sources of information on the affective features of behavior. This approach focuses on vocal and other display behavior with clear functional validity and homology. Drugs with anxiolytic effects that act on the benzodiazepine-GABAA receptor complex and on 5-HT1A receptors systematically and potently alter specific vocalizations in rodents and primates in a pharmacologically reversible manner; the specificity of these effects on vocalizations is evident due to the effectiveness of low doses that do not compromise other physiological and behavioral processes. Antagonists at the benzodiazepine receptor reverse the effects of full agonists on vocalizations, particularly when these occur in threatening, startling and distressing contexts. With the development of antagonists at 5-HT receptor subtypes, it can be anticipated that similar receptor-specificity can be established for the effects of 5-HT anxiolytics.

Aggression↗

Behavioral, immunocytochemical and biochemical studies in rats differing in their sensitivity to pain.

The aim of the study was to further explore the anatomical and neurochemical background of differences in response to the conditioned aversive stimuli. The different patterns of behavioral coping strategies (a conditioned freezing response and ultrasonic vocalization) were analyzed in animals differing in their response to the acute painful stimulation, a foot-shock (HS: high sensitivity rats, LS: low sensitivity rats, and MS: medium sensitivity rats, according to their behavior in the flinch-jump pre-test), and correlated with plasma corticosterone levels, expression of c-Fos protein, and distribution of 5-HT innervation, in different brain structures. It was found that HS rats showed significantly more freezing behavior, whereas LS animals vocalized much more intensively. The behavior of LS group (less freezing response and stronger vocalization) was related to activation of prefrontal cortex (PFCX), increased activity of adrenal glands and stronger serotonin immunostaining in the PFCX, in comparison with HS animals. The more passive strategy of coping with the aversive event of HS group was related to increased activity of amygdalar nuclei and some areas of the hippocampus, and stronger 5-HT immunostaining in the baso-lateral nucleus of the amygdala, in comparison with LS rats. The present findings suggest that animals more vulnerable to stress might have innate deficits in the activity of brain systems controlling the hypothalamic-pituitary-adrenal axis that would normally allow them to cope with stressful situations. It appears also that response to pain may determine other patterns of emotional behavior, probably reflecting different activation thresholds of some brain structures controlling anxiety, e.g. prefrontal and secondary motor cortex.

Adrenal Glands↗

Detection of natural complex sounds by cells in the primary auditory cortex of the cat.

The neural mechanisms involved in the detection of natural complex sounds were studied by recording single-neuron responses from 132 cells in the primary auditory cortex of the cat. The cats were paralyzed and under neuroleptanalgesia (NLA). The cells were first stimulated with pure tones; the responses were then compared with those evoked by many different types of complex sounds, most of which were animal vocalizations. Per-stimulus-time (PST) histograms constructed from the responses to repetitive stimuli were compared with the corresponding sound spectrograms formed from the sounds used as stimuli. Of 100 cells 68 per cent gave predictable responses to complex sounds on the basis of their responses to different pure tone frequencies. In 32 per cent of the cells the responses were unpredictable. Half of these cells did not react to pure tones at all but responded to one or more animal vocalizations or generator sounds with different patterns. Some cells reacted to pure tones in quite a different way than to certain complex sounds, e.g. with inhibition instead of excitation. These results indicate that cells in the primary auditory cortex of the cat reacting in an unpredictable way to sounds with a complex structure have a more or less specialized function, in detecting and analyzing natural and other complex sound patterns. Cells reacting phasically to pure tones seem to be involved in the detection of transient sound elements.

Acoustic Stimulation↗

Dynamics of gamma-band activity induced by auditory pattern changes in humans.

Increasing evidence suggests separate auditory pattern and space processing streams. The present paper describes two magnetoencephalogram studies examining gamma-band activity to changes in auditory patterns using consonant-vowel syllables (experiment 1), animal vocalizations and artificial noises (experiment 2). Two samples of each sound type were presented to passively listening subjects in separate oddball paradigms with 80% standards and 20% deviants differing in their spectral composition. Evoked magnetic mismatch fields peaking approximately 190 ms poststimulus showed a trend for a left-hemisphere advantage for syllables, but no hemispheric differences for the other sounds. Frequency analysis and statistical probability mapping of the differences between deviants and standards revealed increased gamma-band activity above 60 Hz over left anterior temporal/ventrolateral prefrontal cortex for all three types of stimuli. This activity peaked simultaneously with the mismatch responses for animal sounds (180 ms) but was delayed for noises (260 ms) and syllables (320 ms). Our results support the hypothesized role of anterior temporal/ventral prefrontal regions in the processing of auditory pattern change. They extend earlier findings of gamma-band activity over posterior parieto-temporal cortex during auditory spatial processing that supported the putative auditory dorsal stream. Furthermore, earlier gamma-band responses to animal vocalizations may suggest faster processing of fear-relevant information.

Adult↗

Computer models for masked hearing experiments with beluga whales (Delphinapterus leucas).

Environmental assessments of manmade noise and its effects on marine mammals need to address the question of how noise interferes with animal vocalizations. Seeking the answer with animal experiments is very time consuming, costly, and often infeasible. This article examines the possibility of estimating results with software models. A matched filter, spectrogram cross-correlation, critical band cross-correlation, and a back-propagation neural network detected a beluga vocalization in three types of ocean noise. Performance was compared to masked hearing experiments with a beluga whale [C. Erbe and D. M. Farmer, Deep-Sea Res. II 45, 1373-1388 (1998)]. The artificial neural network simulated the animal data most closely and raised confidence in its ability to predict the interference of a variety of noise source with a variety of vocalizations.

Animals↗

Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons.

Comparative, production-based research on animal vocalizations can allow assessments of continuity in vocal communication processes across species, including humans, and may aid in the development of general frameworks relating specific constitutional attributes of callers to acoustic-structural details of their vocal output. Analyses were undertaken on vowel-like baboon grunts to examine variation attributable to caller identity and the intensity of the affective state underlying call production. Six hundred six grunts from eight adult females were analyzed. Grunts derived from 128 bouts of calling in two behavioral contexts: concerted group movements and social interactions involving mothers and their young infants. Each context was subdivided into a high- and low-arousal condition. Thirteen acoustic features variously predicted to reflect variation in either caller identity or arousal intensity were measured for each grunt bout, including tempo-, source- and filter-related features. Grunt bouts were highly individually distinctive, differing in a variety of acoustic dimensions but with some indication that filter-related features contributed disproportionately to individual distinctiveness. In contrast, variation according to arousal condition was associated primarily with tempo- and source-related features, many matching those identified as vehicles of affect expression in other nonhuman primate species and in human speech and other nonverbal vocal signals.

Affect↗

Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain.

Physiological studies in vocal animals such as songbirds indicate that vocalizations drive auditory neurons particularly well. But the neural mechanisms whereby vocalizations are encoded differently from other sounds in the auditory system are unknown. We used spectrotemporal receptive fields (STRFs) to study the neural encoding of song versus the encoding of a generic sound, modulation-limited noise, by single neurons and the neuronal population in the zebra finch auditory midbrain. The noise was designed to match song in frequency, spectrotemporal modulation boundaries, and power. STRF calculations were balanced between the two stimulus types by forcing a common stimulus subspace. We found that 91% of midbrain neurons showed significant differences in spectral and temporal tuning properties when birds heard song and when birds heard modulation-limited noise. During the processing of noise, spectrotemporal tuning was highly variable across cells. During song processing, the tuning of individual cells became more similar; frequency tuning bandwidth increased, best temporal modulation frequency increased, and spike timing became more precise. The outcome was a population response to song that encoded rapidly changing sounds with power and precision, resulting in a faithful neural representation of the temporal pattern of a song. Modeling responses to song using the tuning to modulation-limited noise showed that the population response would not encode song as precisely or robustly. We conclude that stimulus-dependent changes in auditory tuning during song processing facilitate the high-fidelity encoding of the temporal pattern of a song.

Acoustic Stimulation↗