Natural Vocalizations Research Articles

Temporal information in tones, broadband noise, and natural vocalizations is conveyed by differential spiking responses in the superior paraolivary nucleus.

Communication sounds across all mammals consist of multiple frequencies repeated in sequence. The onset and offset of vocalizations are potentially important cues for recognizing distinct units, such as phonemes and syllables, which are needed to perceive meaningful communication. The superior paraolivary nucleus (SPON) in the auditory brainstem has been implicated in the processing of rhythmic sounds. Here, we compared how best frequency tones (BFTs), broadband noise (BBN), and natural mouse calls elicit onset and offset spiking in the mouse SPON. The results demonstrate that onset spiking typically occurs in response to BBN, but not BFT stimulation, while spiking at the sound offset occurs for both stimulus types. This effect of stimulus bandwidth on spiking is consistent with two of the established inputs to the SPON from the octopus cells (onset spiking) and medial nucleus of the trapezoid body (offset spiking). Natural mouse calls elicit two main spiking peaks. The first spiking peak, which is weak or absent with BFT stimulation, occurs most consistently during the call envelope, while the second spiking peak occurs at the call offset. This suggests that the combined spiking activity in the SPON elicited by vocalizations reflects the entire envelope, that is, the coarse amplitude waveform. Since the output from the SPON is purely inhibitory, it is speculated that, at the level of the inferior colliculus, the broadly tuned first peak may improve the signal-to-noise ratio of the subsequent, more call frequency-specific peak. Thus, the SPON may provide a dual inhibition mechanism for tracking phonetic boundaries in social-vocal communication.

Familiar But Unexpected: Effects of Sound Context Statistics on Auditory Responses in the Songbird Forebrain.

Rapid discrimination of salient acoustic signals in the noisy natural environment may depend, not only on specific stimulus features, but also on previous experience that generates expectations about upcoming events. We studied the neural correlates of expectation in the songbird forebrain by using natural vocalizations as stimuli and manipulating the category and familiarity of context sounds. In our paradigm, we recorded bilaterally from auditory neurons in awake adult male zebra finches with multiple microelectrodes during repeated playback of a conspecific song, followed by further playback of this test song in different interleaved sequences with other conspecific or heterospecific songs. Significant enhancement in the auditory response to the test song was seen when its acoustic features differed from the statistical distribution of context song features, but not when it shared the same distribution. Enhancement was also seen when the time of occurrence of the test song was uncertain. These results show that auditory forebrain responses in awake animals in the passive hearing state are modulated dynamically by previous auditory experience and imply that the auditory system can identify the category of a sound based on the global features of the acoustic context. Furthermore, this probability-dependent enhancement in responses to surprising stimuli is independent of stimulus-specific adaptation, which tracks familiarity, suggesting that the two processes could coexist in auditory processing. These findings establish the songbird as a model system for studying these phenomena and contribute to our understanding of statistical learning and the origin of human ERP phenomena to unexpected stimuli.SIGNIFICANCE STATEMENT Traditional auditory neurophysiology has mapped acoustic features of sounds to the response properties of neurons; however, growing evidence suggests that neurons can also encode the probability of sounds. We recorded responses of songbird auditory neurons in a novel paradigm that presented a familiar test stimulus in a sequence with similar or dissimilar sounds. The responses encode, not only stimulus familiarity, but also the expectation for a class of sounds based on the recent statistics of varying sounds in the acoustic context. Our approach thus provides a model system that uses a controlled stimulus paradigm to understand the mechanisms by which top-down processes (expectation and memory) and bottom-up processes (based on stimulus features) interact in sensory coding.

Phonetic characteristics of vocalizations during pain.

There have, yet, been only few attempts to phonetically characterize the vocalizations of pain, although there is wide agreement that moaning, groaning, or other nonverbal utterance can be indicative of pain. We studied the production of vowels "u," "a," "i", and "schwa" (central vowel, sounding like a darker "e" as in hesitations like "ehm")-as experimental approximations to natural vocalizations. In 50 students vowel production and self-report ratings were assessed during painful and nonpainful heat stimulation (hot water immersion) as well as during baseline (no-stimulation). The phonetic parameters extracted were pitch (mean F0), phonatory fluctuations (range F0) and loudness (acoustic energy level). Only for the vowels "u" and "schwa," which might be considered best approximations to moaning and groaning, did pitch and loudness increase during pain. Furthermore, changes from nonpainful to painful stimulations in these parameters also significantly predicted concurrent changes in pain ratings. Vocalization characteristics of pain seem to be best described by an increase in pitch and in loudness. Future studies using more specific and comprehensive phonetic analyses will surely help to provide an even more precise characterization of vocalizations because of pain.

Vocal sequences suppress spiking in the bat auditory cortex while evoking concomitant steady-state local field potentials.

The mechanisms by which the mammalian brain copes with information from natural vocalization streams remain poorly understood. This article shows that in highly vocal animals, such as the bat species Carollia perspicillata, the spike activity of auditory cortex neurons does not track the temporal information flow enclosed in fast time-varying vocalization streams emitted by conspecifics. For example, leading syllables of so-called distress sequences (produced by bats subjected to duress) suppress cortical spiking to lagging syllables. Local fields potentials (LFPs) recorded simultaneously to cortical spiking evoked by distress sequences carry multiplexed information, with response suppression occurring in low frequency LFPs (i.e. 2–15 Hz) and steady-state LFPs occurring at frequencies that match the rate of energy fluctuations in the incoming sound streams (i.e. >50 Hz). Such steady-state LFPs could reflect underlying synaptic activity that does not necessarily lead to cortical spiking in response to natural fast time-varying vocal sequences.

Contextual effects of noise on vocalization encoding in primary auditory cortex.

The understanding of where and how auditory scene analysis is accomplished is of broad interest to neuroscientists. In this paper, we systematically investigated neuronal coding of multiple vocalizations degraded by two distinct noises at various signal-to-noise ratios in nonhuman primates. In the process, we uncovered heterogeneity of single-unit representations for different auditory scenes yet homogeneity of responses across the population.

Do we hear what birds hear in birdsong?

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, Taeniopygia guttata, 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.

Discrimination of frequency modulated sweeps by mice.

Mice often produce ultrasonic vocalizations (USVs) that sweep upwards in frequency from around 60 to around 80 kHz and downwards in frequency from 80 to 60 kHz. Whether or not these USVs are used for communication purposes is still unknown. Here, mice were trained and tested using operant conditioning procedures and positive reinforcement to discriminate between synthetic upsweeps and downsweeps. The stimuli varied in bandwidth, duration, and direction of sweep. The mice performed significantly worse when discriminating between background and test stimuli when the stimuli all occupied the same bandwidths. Further, the mice's discrimination performance became much worse for stimuli that had durations similar to those natural vocalizations of the mice. Sweeps composed of different frequency ranges and longer durations had improved discrimination. These results collected using artificial stimuli created to mimic natural USVs indicate that the bandwidth of the vocalizations may be much more important for communication than the frequency contours of the vocalizations.

Expression of c-Fos in rat auditory and limbic systems following 22-kHz calls

In the present study, adult Long-Evans rats were exposed either to natural conspecific aversive 22-kHz vocalizations or to artificial call-like stimuli with comparable frequency-temporal features, followed by c-Fos immunohistochemistry. The natural 22-kHz vocalizations was either played from a recording or produced by a foot-shocked animal located nearby (live vocalizations). In comparison with controls (non-exposed animals), c-Fos immunoreactivity was significantly increased in the inferior colliculus (IC), auditory cortex (AC), periaqueductal grey (PAG), basolateral amygdala (BA), and hippocampus (Hip) of rats exposed to either live or recorded 22-kHz natural vocalizations. Exposure to live natural vocalizations of the foot-shocked animal resulted in a similar pattern of c-Fos activity, as did exposure to the playback of the natural vocalizations. In contrast to this, foot-shocked rats (emitting the 22-kHz vocalizations) had the c-Fos positivity increased markedly in the PAG and only slightly in the AC. The expression of c-Fos also increased in the IC, AC, and in the PAG in animals exposed to the artificial call-like stimuli, when compared to controls; however, the increase was much less pronounced. In this case, c-Fos expression was not increased in the hippocampus or basolateral amygdala. Interestingly, almost no c-Fos expression was found in the medial nucleus of the geniculate body in any of the experimental groups. These findings suggest that differences exist between the processing of important natural conspecific vocalizations and artificial call-like stimuli with similar frequency-temporal features, and moreover they suggest the specific role of individual brain structures in the processing of such calls.

Natural Vocalizations in the Mammalian Inferior Colliculus are Broadly Encoded by a Small Number of Independent Multi-Units.

How complex natural sounds are represented by the main converging center of the auditory midbrain, the central inferior colliculus, is an open question. We applied neural discrimination to determine the variation of detailed encoding of individual vocalizations across the best frequency gradient of the central inferior colliculus. The analysis was based on collective responses from several neurons. These multi-unit spike trains were recorded from guinea pigs exposed to a spectrotemporally rich set of eleven species-specific vocalizations. Spike trains of disparate units from the same recording were combined in order to investigate whether groups of multi-unit clusters represent the whole set of vocalizations more reliably than only one unit, and whether temporal response correlations between them facilitate an unambiguous neural representation of the vocalizations. We found a spatial distribution of the capability to accurately encode groups of vocalizations across the best frequency gradient. Different vocalizations are optimally discriminated at different locations of the best frequency gradient. Furthermore, groups of a few multi-unit clusters yield improved discrimination over only one multi-unit cluster between all tested vocalizations. However, temporal response correlations between units do not yield better discrimination. Our study is based on a large set of units of simultaneously recorded responses from several guinea pigs and electrode insertion positions. Our findings suggest a broadly distributed code for behaviorally relevant vocalizations in the mammalian inferior colliculus. Responses from a few non-interacting units are sufficient to faithfully represent the whole set of studied vocalizations with diverse spectrotemporal properties.

Transmission properties of vocalizations in a year-round territorial bird

Acoustic Adaptation Hypothesis (AAH) predicts that acoustic signals using in long-distance communication should be optimized for transmission through its natural environment. To test if White-eared Ground-sparrows (Melozone leucotis) vocalizations are adapted to transmit long distances, I conducted two sound transmission experiments where I broadcast and re-recorded different calls, songs, and duets. This ground-sparrows use vocal communication year round for territory defense and mate attraction. I conducted the experiments inside ground-sparrows territories in Costa Rica, broadcasting natural vocalizations at different combination of distances, speaker and microphone heights to quantified the signal-to-noise ratio, tail-to-signal ratio, blur ratio, and excess attenuation. Songs and duets of White-eared Ground-sparrows showed similar patterns of degradation with distance and with proximity to the ground, suggesting that vocalizations facilitate communication with receivers at similar shorter distances (in less than a typical territory’s diameter). Chip calls showed higher degradation in comparison to tseet calls with the distance, suggesting that tseet calls are design for longer distance communication. To my surprise, chip calls, songs, and duets has not experienced strong selection for long distance communication, because results do not support the AHH, and probably these vocalization characteristics are under other selective forces as sexual selection or phylogenetic constrain.

Spectrotemporal response properties of core auditory cortex neurons in awake monkey.

So far, most studies of core auditory cortex (AC) have characterized the spectral and temporal tuning properties of cells in non-awake, anesthetized preparations. As experiments in awake animals are scarce, we here used dynamic spectral-temporal broadband ripples to study the properties of the spectrotemporal receptive fields (STRFs) of AC cells in awake monkeys. We show that AC neurons were typically most sensitive to low ripple densities (spectral) and low velocities (temporal), and that most cells were not selective for a particular spectrotemporal sweep direction. A substantial proportion of neurons preferred amplitude-modulated sounds (at zero ripple density) to dynamic ripples (at non-zero densities). The vast majority (>93%) of modulation transfer functions were separable with respect to spectral and temporal modulations, indicating that time and spectrum are independently processed in AC neurons. We also analyzed the linear predictability of AC responses to natural vocalizations on the basis of the STRF. We discuss our findings in the light of results obtained from the monkey midbrain inferior colliculus by comparing the spectrotemporal tuning properties and linear predictability of these two important auditory stages.

Vocal generalization depends on gesture identity and sequence.

Generalization, the brain's ability to transfer motor learning from one context to another, occurs in a wide range of complex behaviors. However, the rules of generalization in vocal behavior are poorly understood, and it is unknown how vocal learning generalizes across an animal's entire repertoire of natural vocalizations and sequences. Here, we asked whether generalization occurs in a nonhuman vocal learner and quantified its properties. We hypothesized that adaptive error correction of a vocal gesture produced in one sequence would generalize to the same gesture produced in other sequences. To test our hypothesis, we manipulated the fundamental frequency (pitch) of auditory feedback in Bengalese finches (Lonchura striata var. domestica) to create sensory errors during vocal gestures (song syllables) produced in particular sequences. As hypothesized, error-corrective learning on pitch-shifted vocal gestures generalized to the same gestures produced in other sequential contexts. Surprisingly, generalization magnitude depended strongly on sequential distance from the pitch-shifted syllables, with greater adaptation for gestures produced near to the pitch-shifted syllable. A further unexpected result was that nonshifted syllables changed their pitch in the direction opposite from the shifted syllables. This apparently antiadaptive pattern of generalization could not be explained by correlations between generalization and the acoustic similarity to the pitch-shifted syllable. These findings therefore suggest that generalization depends on the type of vocal gesture and its sequential context relative to other gestures and may reflect an advantageous strategy for vocal learning and maintenance.

Integration over Multiple Timescales in Primary Auditory Cortex

Speech and other natural vocalizations are characterized by large modulations in their sound envelope. The timing of these modulations contains critical information for discrimination of important features, such as phonemes. We studied how depression of synaptic inputs, a mechanism frequently reported in cortex, can contribute to the encoding of envelope dynamics. Using a nonlinear stimulus-response model that accounted for synaptic depression, we predicted responses of neurons in ferret primary auditory cortex (A1) to stimuli with natural temporal modulations. The depression model consistently performed better than linear and second-order models previously used to characterize A1 neurons, and it produced more biologically plausible fits. To test how synaptic depression can contribute to temporal stimulus integration, we used nonparametric maximum a posteriori decoding to compare the ability of neurons showing and not showing depression to reconstruct the stimulus envelope. Neurons showing evidence for depression reconstructed stimuli over a longer range of latencies. These findings suggest that variation in depression across the cortical population supports a rich code for representing the temporal dynamics of natural sounds.

Estrogenic modulation of auditory processing: A vertebrate comparison

Sex-steroid hormones are well-known regulators of vocal motor behavior in several organisms. A large body of evidence now indicates that these same hormones modulate processing at multiple levels of the ascending auditory pathway. The goal of this review is to provide a comparative analysis of the role of estrogens in vertebrate auditory function. Four major conclusions can be drawn from the literature: First, estrogens may influence the development of the mammalian auditory system. Second, estrogenic signaling protects the mammalian auditory system from noise- and age-related damage. Third, estrogens optimize auditory processing during periods of reproductive readiness in multiple vertebrate lineages. Finally, brain-derived estrogens can act locally to enhance auditory response properties in at least one avian species. This comparative examination may lead to a better appreciation of the role of estrogens in the processing of natural vocalizations and mayprovide useful insights toward alleviating auditory dysfunctions emanating from hormonal imbalances.

Auditory processing for contrast enhancement of salient communication vocalizations

In a natural acoustic environment, coherent representations of auditory objects and sources are streamed from the myriad sounds that enter our ears. Features of those sounds that are familiar and behaviorally salient to us are detected and discriminated into invariant precepts that inform us about our external world. Research into how this occurs is increasingly converging on the idea that there is a transformation from the auditory periphery wherein an initial acoustically faithful representation by neurons becomes progressively altered to enhance the population neural representation of perceptually relevant aspects of the sound. How this occurs may vary for sounds whose meanings are acquired in different ways, perhaps depending on what actions and decisions must be executed upon recognition. We have investigated this process in a natural social context in which mouse mothers “learn” about the meaning of pup ultrasound vocalizations through their maternal care. Here we discuss our recent studies in awake mice using electrophysiological, behavioral, immunohistochemical, and computational methods. Our results suggest that experience with natural vocalizations may alter core auditory cortical neural responses so that the contrast in activity across the neural population enhances the detection and discrimination of salient calls.

Auditory processing for contrast enhancement of salient communication vocalizations.

In a natural acoustic environment, coherent representations of auditory objects and sources are streamed from the myriad sounds that enter our ears. Features of those sounds that are familiar and behaviorally salient to us are detected and discriminated into invariant precepts that inform us about our external world. Research into how this occurs is increasingly converging on the idea that there is a transformation from the auditory periphery wherein an initial acoustically faithful representation by neurons becomes progressively altered to enhance the population neural representation of perceptually relevant aspects of the sound. How this occurs may vary for sounds whose meanings are acquired in different ways, perhaps depending on what actions and decisions must be executed upon recognition. We have investigated this process in a natural social context in which mouse mothers "learn" about the meaning of pup ultrasound vocalizations through their maternal care. Here we discuss our recent studies in awake mice using electrophysiological, behavioral, immunohistochemical and computational methods. Our results suggest that experience with natural vocalizations may alter core auditory cortical neural responses so that the contrast in activity across the neural population enhances the detection and discrimination of salient calls.

Rule learning by zebra finches in an artificial grammar learning task: which rule?

A hallmark of the human language faculty is the use of syntactic rules. The natural vocalizations of animals are syntactically simple, but several studies indicate that animals can detect and discriminate more complex structures in acoustic stimuli. However, how they discriminate such structures is often not clear. Using an artificial grammar learning paradigm, zebra finches were tested in a Go/No-go experiment for their ability to distinguish structurally different three-element sound sequences. In Experiment 1, zebra finches learned to discriminate ABA and BAB from ABB, AAB, BBA, and ABB sequences. Tests with probe sounds consisting of four elements suggested that the discrimination was based on attending to the presence or absence of repeated A- and B-elements. One bird generalized the discrimination to a new element type. In Experiment 2, we continued the training by adding four-element songs following a 'first and last identical versus different' rule that could not be solved by attending to repetitions. Only two out of five birds learned the overall discrimination. Testing with novel probes demonstrated that discrimination was not based on using the 'first and last identical' rule, but on attending to the presence or absence of the individual training stimuli. The two birds differed in the strategies used. Our results thus demonstrate only a limited degree of abstract rule learning but highlight the need for extensive and critical probe testing to examine the rules that animals (and humans) use to solve artificial grammar learning tasks. They also underline that rule learning strategies may differ between individuals.

Revisiting the syntactic abilities of non-human animals: natural vocalizations and artificial grammar learning

The domain of syntax is seen as the core of the language faculty and as the most critical difference between animal vocalizations and language. We review evidence from spontaneously produced vocalizations as well as from perceptual experiments using artificial grammars to analyse animal syntactic abilities, i.e. abilities to produce and perceive patterns following abstract rules. Animal vocalizations consist of vocal units (elements) that are combined in a species-specific way to create higher order strings that in turn can be produced in different patterns. While these patterns differ between species, they have in common that they are no more complex than a probabilistic finite-state grammar. Experiments on the perception of artificial grammars confirm that animals can generalize and categorize vocal strings based on phonetic features. They also demonstrate that animals can learn about the co-occurrence of elements or learn simple 'rules' like attending to reduplications of units. However, these experiments do not provide strong evidence for an ability to detect abstract rules or rules beyond finite-state grammars. Nevertheless, considering the rather limited number of experiments and the difficulty to design experiments that unequivocally demonstrate more complex rule learning, the question of what animals are able to do remains open.

Social experience affects neuronal responses to male calls in adult female zebra finches

Plasticity studies have consistently shown that behavioural relevance can change the neural representation of sounds in the auditory system, but what occurs in the context of natural acoustic communication where significance could be acquired through social interaction remains to be explored. The zebra finch, a highly social songbird species that forms lifelong pair bonds and uses a vocalization, the distance call, to identify its mate, offers an opportunity to address this issue. Here, we recorded spiking activity in females while presenting distance calls that differed in their degree of familiarity: calls produced by the mate, by a familiar male, or by an unfamiliar male. We focused on the caudomedial nidopallium (NCM), a secondary auditory forebrain region. Both the mate's call and the familiar call evoked responses that differed in magnitude from responses to the unfamiliar call. This distinction between responses was seen both in single unit recordings from anesthetized females and in multiunit recordings from awake freely moving females. In contrast, control females that had not heard them previously displayed responses of similar magnitudes to all three calls. In addition, more cells showed highly selective responses in mated than in control females, suggesting that experience-dependent plasticity in call-evoked responses resulted in enhanced discrimination of auditory stimuli. Our results as a whole demonstrate major changes in the representation of natural vocalizations in the NCM within the context of individual recognition. The functional properties of NCM neurons may thus change continuously to adapt to the social environment.

Behavioural and neurobiological implications of linear and non-linear features in larynx phonations of horseshoe bats

Mammalian vocalizations exhibit large variations in their spectrotemporal features, although it is still largely unknown which result from intrinsic biomechanical properties of the larynx and which are under direct neuromuscular control. Here we show that mere changes in laryngeal air flow yield several non-linear effects on sound production, in an isolated larynx preparation from horseshoe bats. Most notably, there are sudden jumps between two frequency bands used for either echolocation or communication in natural vocalizations. These jumps resemble changes in “registers” as in yodelling. In contrast, simulated contractions of the main larynx muscle produce linear frequency changes, but are limited to echolocation or communication frequencies. Only by combining non-linear and linear properties can this larynx therefore produce sounds covering the entire frequency range of natural calls. This may give behavioural meaning to yodelling-like vocal behaviour and reshape our thinking about how the brain controls the multitude of spectral vocal features in mammals.