Species-specific Vocalizations Research Articles

Passive ocean acoustic waveguide remote sensing of vocalization behavior and spatial distribution of diverse marine mammal species in the Norwegian and Barents Sea

Leveraging data acquired using a 160-element coherent hydrophone array deployed in the Norwegian and Barents Seas during spring 2014, and the passive ocean acoustic waveguide remote sensing (POAWRS) technique is employed to enable instantaneous wide-area monitoring of marine mammal vocalizations over expanses exceeding 100 km in diameter. The vocalization behavior of diverse marine mammal species including Fin, Humpback, Minke, Sperm, and Beluga whales are analyzed, quantifying time-frequency characteristics and call patterns from their vocalization signals present in high-resolution beamformed power spectrograms. Previously developed automatic detection and machine learning algorithms are employed for clustering and classification of underwater acoustic events, facilitating the subsequent manual audio-visual inspection of whale calls. Bearing-time trajectories of repetitive species-specific vocalizations signals are utilized to estimate locations of the whale calls and hence their temporo-spatial distributions. Through comparative studies, we assess the presence and abundance of marine mammal species-specific vocalization signals in three distinct coastal regions off Norway, namely, Alesund, Lofoten, and Northern Finmark. In addition, we investigate correspondences of marine mammal distributions with concurrently imaged instantaneous wide-area fish distributions from distinct fish species to elucidate potential predator-prey interactions and habitat preferences.

Perceptual specializations for processing species-specific vocalizations in the common marmoset (Callithrix jacchus)

How humans and animals segregate sensory information into discrete, behaviorally meaningful categories is one of the hallmark questions in neuroscience. Much of the research around this topic in the auditory system has centered around human speech perception, in which categorical processes result in an enhanced sensitivity for acoustically meaningful differences and a reduced sensitivity for nonmeaningful distinctions. Much less is known about whether nonhuman primates process their species-specific vocalizations in a similar manner. We address this question in the common marmoset, a small arboreal New World primate with a rich vocal repertoire produced across a range of behavioral contexts. We first show that marmosets perceptually categorize their vocalizations in ways that correspond to previously defined call types for this species. Next, we show that marmosets are differentially sensitive to changes in particular acoustic features of their most common call types and that these sensitivity differences are matched to the population statistics of their vocalizations in ways that likely maximize category formation. Finally, we show that marmosets are less sensitive to changes in these acoustic features when within the natural range of variability of their calls, which possibly reflects perceptual specializations which maintain existing call categories. These findings suggest specializations for categorical vocal perception in a New World primate species and pave the way for future studies examining their underlying neural mechanisms.

Two conserved vocal central pattern generators broadly tuned for fast and slow rates generate species-specific vocalizations in Xenopus clawed frogs.

Across phyla, males often produce species-specific vocalizations to attract females. Although understanding the neural mechanisms underlying behavior has been challenging in vertebrates, we previously identified two anatomically distinct central pattern generators (CPGs) that drive the fast and slow clicks of male Xenopus laevis, using an ex vivo preparation that produces fictive vocalizations. Here, we extended this approach to four additional species, X. amieti, X. cliivi, X. petersii, and X. tropicalis, by developing ex vivo brain preparation from which fictive vocalizations are elicited in response to a chemical or electrical stimulus. We found that even though the courtship calls are species-specific, the CPGs used to generate clicks are conserved across species. The fast CPGs, which critically rely on reciprocal connections between the parabrachial nucleus and the nucleus ambiguus, are conserved among fast-click species, and slow CPGs are shared among slow-click species. In addition, our results suggest that testosterone plays a role in organizing fast CPGs in fast-click species, but not in slow-click species. Moreover, fast CPGs are not inherited by all species but monopolized by fast-click species. The results suggest that species-specific calls of the genus Xenopus have evolved by utilizing conserved slow and/or fast CPGs inherited by each species.

Acoustic Presence of Cetaceans in the Miaodao Archipelago, China.

Once an important cetacean habitat, the Miaodao Archipelago has been altered by human-induced disturbances over several decades. While cetacean diversity is known to have decreased, no recent data on species diversity around Miaodao are known to exist. Capitalizing on the high vocal activity of cetaceans, three passive acoustic surveys, including towed and stationary types, were undertaken to detect the presence of species-specific vocalizations in May 2021, October 2021, and July 2022, as most cetacean sightings occurred during May and August in recent years. The results revealed that the East Asian finless porpoise is the sole cetacean species that can be reliably observed around the archipelago, as no other species were detected. The acoustic data also revealed potentially clumped distributions of finless porpoises with some seasonal variation. While not acoustically detected during any of the surveys, humpback whales, minke whales, and killer whales have been visually sighted in the region. The lack of acoustic detection of these species suggests that they are likely to be temporary visitors to the region, or at least exhibit strong seasonality in their presence within the region. These new data provide the latest snapshot of cetacean presence around the Miaodao Archipelago that can help inform future research and conservation.

The prefrontal cortex of the Mexican free-tailed bat is more selective to communication calls than primary auditory cortex.

In this study, we examined the auditory responses of a prefrontal area, the frontal auditory field (FAF), of an echolocating bat (Tadarida brasiliensis) and presented a comparative analysis of the neuronal response properties between the FAF and the primary auditory cortex (A1). We compared single-unit responses from the A1 and the FAF elicited by pure tones, downward frequency-modulated sweeps (dFMs), and species-specific vocalizations. Unlike the A1, FAFs were not frequency tuned. However, progressive increases in dFM sweep rate elicited a systematic increase of response precision, a phenomenon that does not take place in the A1. Call selectivity was higher in the FAF versus A1. We calculated the neuronal spectrotemporal receptive fields (STRFs) and spike-triggered averages (STAs) to predict responses to the communication calls and provide an explanation for the differences in call selectivity between the FAF and A1. In the A1, we found a high correlation between predicted and evoked responses. However, we did not generate reasonable STRFs in the FAF, and the prediction based on the STAs showed lower correlation coefficient than that of the A1. This suggests nonlinear response properties in the FAF that are stronger than the linear response properties in the A1. Stimulating with a call sequence increased call selectivity in the A1, but it remained unchanged in the FAF. These data are consistent with a role for the FAF in assessing distinctive acoustic features downstream of A1, similar to the role proposed for primate ventrolateral prefrontal cortex.NEW & NOTEWORTHY In this study, we examined the neuronal responses of a frontal cortical area in an echolocating bat to behaviorally relevant acoustic stimuli and compared them with those in the primary auditory cortex (A1). In contrast to the A1, neurons in the bat frontal auditory field are not frequency tuned but showed a higher selectivity for social signals such as communication calls. The results presented here indicate that the frontal auditory field may represent an additional processing center for behaviorally relevant sounds.

Assessing acoustic competition between sibling frog species using rhythm analysis.

Male frog advertisement calls are species‐specific vocalizations used to attract females for breeding. However, it is possible for environmental or biological sounds to overlap these calls in both frequency and duration resulting in signal confusion, influencing female decision and/or location abilities. It is therefore important for vocal species competing for the same acoustic space to partition their calls either spatially or temporally (via call alternation or suppression). However, frog species previously isolated from each other may not have developed appropriate adaptive behaviors, resulting in acoustic competition. This study applied rhythm analysis to track changes in calling behavior, namely changes in calling frequency (as in beats per second), of the wallum sedgefrog and the eastern sedgefrog when vocalizing alone versus in the presence of each other to assess potential acoustic competition. Our main findings demonstrated that both species significantly altered their calling behavior when exposed to each other. While we expected the increased calling activity of one species to inhibit the activity of the other to avoid signal confusion, we instead found that both species greatly increased the beat frequency of their calls when calling in the presence of each other. We also found evidence of beat frequency development in the wallum sedgefrog whereby there was always a strong initial increase in call frequency in reaction to the first vocal interruption by the eastern sedgefrog. These results support the hypothesis that the eastern sedgefrog and the wallum sedgefrog are in competition for the acoustic space in habitats where they occur together. This highlights a new threat to the vulnerable wallum sedgefrog species and may serve to inform future management practices. Using rhythm analyses to track changes in acoustic behavior can help inform on important population dynamics such as health, trajectory, and response to management, and therefore be of great benefit to the conservation of vocal species.

Facial expressions can be categorized along the upper-lower facial axis, from a perceptual perspective.

A critical question, fundamental for building models of emotion, is how to categorize emotions. Previous studies have typically taken one of two approaches: (a) they focused on the pre-perceptual visual cues, how salient facial features or configurations were displayed; or (b) they focused on the post-perceptual affective experiences, how emotions affected behavior. In this study, we attempted to group emotions at a peri-perceptual processing level: it is well known that humans perceive different facial expressions differently, therefore, can we classify facial expressions into distinct categories in terms of their perceptual similarities? Here, using a novel non-lexical paradigm, we assessed the perceptual dissimilarities between 20 facial expressions using reaction times. Multidimensional-scaling analysis revealed that facial expressions were organized predominantly along the upper-lower face axis. Cluster analysis of behavioral data delineated three superordinate categories, and eye-tracking measurements validated these clustering results. Interestingly, these superordinate categories can be conceptualized according to how facial displays interact with acoustic communications: One group comprises expressions that have salient mouth features. They likely link to species-specific vocalization, for example, crying, laughing. The second group comprises visual displays with diagnosing features in both the mouth and the eye regions. They are not directly articulable but can be expressed prosodically, for example, sad, angry. Expressions in the third group are also whole-face expressions but are completely independent of vocalization, and likely being blends of two or more elementary expressions. We propose a theoretical framework to interpret the tripartite division in which distinct expression subsets are interpreted as successive phases in an evolutionary chain.

Species and sex differences in vocalizations between sex-role reversed shorebirds, Northern Jacana (Jacana spinosa) and Wattled Jacana (J. jacana)

Species-specific vocalizations can act as a reproductive isolating mechanism between closely related populations. We analyzed vocal differences between 2 hybridizing species of sex-role reversed polyandrous shorebirds, the Northern Jacana (Jacana spinosa) and Wattled Jacana (J. jacana). We found that Northern Jacana calls have higher fundamental frequency and peak frequency than Wattled Jacana calls. We also compared calls between females and males, as both jacana species are sex-role reversed and females compete for male mates. Males produce calls with a higher fundamental and peak frequency and shorter notes than females. These results suggest that vocal differences between Northern and Wattled jacanas have the potential to act as a behavioral mediator of interspecific interactions, and that sex differences in vocalizations may relate to sex-role reversal in territorial defense and mate attraction.

Electrophysiological Evidence of Early Cortical Sensitivity to Human Conspecific Mimic Voice as a Distinct Category of Natural Sound.

Purpose From an anthropological perspective of hominin communication, the human auditory system likely evolved to enable special sensitivity to sounds produced by the vocal tracts of human conspecifics whether attended or passively heard. While numerous electrophysiological studies have used stereotypical human-produced verbal (speech voice and singing voice) and nonverbal vocalizations to identify human voice-sensitive responses, controversy remains as to when (and where) processing of acoustic signal attributes characteristic of "human voiceness" per se initiate in the brain. Method To explore this, we used animal vocalizations and human-mimicked versions of those calls ("mimic voice") to examine late auditory evoked potential responses in humans. Results Here, we revealed an N1b component (96-120 ms poststimulus) during a nonattending listening condition showing significantly greater magnitude in response to mimics, beginning as early as primary auditory cortices, preceding the time window reported in previous studies that revealed species-specific vocalization processing initiating in the range of 147-219 ms. During a sound discrimination task, a P600 (500-700 ms poststimulus) component showed specificity for accurate discrimination of human mimic voice. Distinct acoustic signal attributes and features of the stimuli were used in a classifier model, which could distinguish most human from animal voice comparably to behavioral data-though none of these single features could adequately distinguish human voiceness. Conclusions These results provide novel ideas for algorithms used in neuromimetic hearing aids, as well as direct electrophysiological support for a neurocognitive model of natural sound processing that informs both neurodevelopmental and anthropological models regarding the establishment of auditory communication systems in humans. Supplemental Material https://doi.org/10.23641/asha.12903839.

Cyto- and myeloarchitectural brain atlas of the pale spear-nosed bat (Phyllostomus discolor) in CT Aided Stereotaxic Coordinates

The pale spear-nosed bat Phyllostomus discolor, a microchiropteran bat, is well established as an animal model for research on the auditory system, echolocation and social communication of species-specific vocalizations. We have created a brain atlas of Phyllostomus discolor that provides high-quality histological material for identification of brain structures in reliable stereotaxic coordinates to strengthen neurobiological studies of this key species. The new atlas combines high-resolution images of frontal sections alternately stained for cell bodies (Nissl) and myelinated fibers (Gallyas) at 49 rostrocaudal levels, at intervals of 350 µm. To facilitate comparisons with other species, brain structures were named according to the widely accepted Paxinos nomenclature and previous neuroanatomical studies of other bat species. Outlines of auditory cortical fields, as defined in earlier studies, were mapped onto atlas sections and onto the brain surface, together with the architectonic subdivisions of the neocortex. X-ray computerized tomography (CT) of the bat’s head was used to establish the relationship between coordinates of brain structures and the skull. We used profile lines and the occipital crest as skull landmarks to line up skull and brain in standard atlas coordinates. An easily reproducible protocol allows sectioning of experimental brains in the standard frontal plane of the atlas. An electronic version of the atlas plates and supplementary material is available from https://doi.org/10.12751/g-node.8bbcxy

Experience-Dependent Coding of Time-Dependent Frequency Trajectories by Off Responses in Secondary Auditory Cortex.

Time-dependent frequency trajectories are an inherent feature of many behaviorally relevant sounds, such as species-specific vocalizations. Dynamic frequency trajectories, even in short sounds, often convey meaningful information, which may be used to differentiate sound categories. However, it is not clear what and where neural responses in the auditory cortical pathway are critical for conveying information about behaviorally relevant frequency trajectories, and how these responses change with experience. Here, we uncover tuning to subtle variations in frequency trajectories in auditory cortex of female mice. We found that auditory cortical responses could be modulated by variations in a pure tone trajectory as small as 1/24th of an octave, comparable to what has been reported in primates. In particular, late spiking after the end of a sound stimulus was more often sensitive to the sound's subtle frequency variation compared with spiking during the sound. Such “Off” responses in the adult A2, but not those in core auditory cortex, were plastic in a way that may enhance the representation of a newly acquired, behaviorally relevant sound category. We illustrate this with the maternal mouse paradigm for natural vocalization learning. By using an ethologically inspired paradigm to drive auditory responses in higher-order neurons, our results demonstrate that mouse auditory cortex can track fine frequency changes, which allows A2 Off responses in particular to better respond to pitch trajectories that distinguish behaviorally relevant, natural sound categories.SIGNIFICANCE STATEMENT A whistle's pitch conveys meaning to its listener, as when dogs learn that distinct pitch trajectories whistled by their owner differentiate specific commands. Many species use pitch trajectories in their own vocalizations to distinguish sound categories, such as in human languages, such as Mandarin. How and where auditory neural activity encodes these pitch trajectories as their meaning is learned but not well understood, especially for short-duration sounds. We studied this in mice, where infants use ultrasonic whistles to communicate to adults. We found that late neural firing after a sound ends can be tuned to how the pitch changes in time, and that this response in a secondary auditory cortical field changes with experience to acquire a pitch change's meaning.

Experience- and Sex-Dependent Intrinsic Plasticity in the Zebra Finch Auditory Cortex during Song Memorization.

For vocal communicators like humans and songbirds, survival and reproduction depend on highly developed auditory processing systems that can detect and differentiate nuanced differences in vocalizations, even amid noisy environments. Early auditory experience is critical to the development of these systems. In zebra finches and other songbirds, there is a sensitive period when young birds memorize a song that will serve as a model for their own vocal production. In addition to learning a specific tutor's song, the auditory system may also undergo critical developmental processes that support auditory perception of vocalizations more generally. Here, we investigate changes in intrinsic spiking dynamics among neurons in the caudal mesopallium, a cortical-level auditory area implicated in discriminating and learning species-specific vocalizations. A subset of neurons in this area only fire transiently at the onset of current injections (i.e., phasic firing), a dynamical property that can enhance the reliability and selectivity of neural responses to complex acoustic stimuli. At the beginning of the sensitive period, just after zebra finches have fledged from the nest, there is an increase in the proportion of caudal mesopallium neurons with phasic excitability, and in the proportion of neurons expressing Kv1.1, a low-threshold channel that facilitates phasic firing. This plasticity requires exposure to a complex, noisy environment and is greater in males, the only sex that sings in this species. This shift to more phasic dynamics is therefore an experience-dependent adaptation that could facilitate auditory processing in noisy, acoustically complex conditions during a key stage of vocal development.SIGNIFICANCE STATEMENT Auditory experience early in life shapes how humans and songbirds perceive the vocal communication sounds produced by their species. However, the changes that occur in the brain as this learning takes place are poorly understood. In this study, we show that in young zebra finches that are just beginning to learn the structure of their species' song, neurons in a key cortical area adapt their intrinsic firing patterns in response to the acoustic environment. In the complex, cocktail-party-like environment of a colony, more neurons adopt transient firing dynamics, which can facilitate neural coding of songs amid such challenging conditions.

Rapid modulations of the vocal structure in marmoset monkeys

Humans and some animal species show flexibility in vocal production either voluntarily or in response to environmental cues. Studies have shown rapid spectrotemporal changes in speech or vocalizations during altered auditory feedback in humans, songbirds and bats. Non-human primates, however, have long been considered lacking the ability to modify spectrotemporal structures of their vocalizations. Here we tested the ability of the common marmoset (Callithrix jacchus), a highly vocal New World primate species to alter spectral and temporal structures of their species-specific vocalizations in the presence of perturbation signals. By presenting perturbation noises while marmosets were vocalizing phee calls, we showed that they were able to change in real-time the duration or spectral trajectory of an ongoing phee phrase by either terminating it before its completion, making rapid shifts in fundamental frequency or in some cases prolonging the duration beyond the natural range of phee calls. In some animals, we observed fragmented phee calls which were not produced by marmosets in their natural environment. Interestingly, some perturbation-induced changes persisted even in the absence of the perturbation noises. These observations provide further evidence that marmoset monkeys are capable of rapidly modulating their vocal structure and suggested potential voluntary vocal control by this non-human primate species.

Long-term and persistent vocal plasticity in adult bats

Bats exhibit a diverse and complex vocabulary of social communication calls some of which are believed to be learned during development. This ability to produce learned, species-specific vocalizations – a rare trait in the animal kingdom – requires a high-degree of vocal plasticity. Bats live extremely long lives in highly complex and dynamic social environments, which suggests that they might also retain a high degree of vocal plasticity in adulthood, much as humans do. Here, we report persistent vocal plasticity in adult bats (Rousettus aegyptiacus) following exposure to broad-band, acoustic perturbation. Our results show that adult bats can not only modify distinct parameters of their vocalizations, but that these changes persist even after noise cessation – in some cases lasting several weeks or months. Combined, these findings underscore the potential importance of bats as a model organism for studies of vocal plasticity, including in adulthood.

Processing of fast amplitude modulations in bat auditory cortex matches communication call-specific sound features.

Bats use a large repertoire of calls for social communication. In the bat Phyllostomus discolor, social communication calls are often characterized by sinusoidal amplitude and frequency modulations with modulation frequencies in the range of 100-130 Hz. However, peaks in mammalian auditory cortical modulation transfer functions are typically limited to modulation frequencies below 100 Hz. We investigated the coding of sinusoidally amplitude modulated sounds in auditory cortical neurons in P. discolor by constructing rate and temporal modulation transfer functions. Neuronal responses to playbacks of various communication calls were additionally recorded and compared with the neurons' responses to sinusoidally amplitude-modulated sounds. Cortical neurons in the posterior dorsal field of the auditory cortex were tuned to unusually high modulation frequencies: rate modulation transfer functions often peaked around 130 Hz (median: 87 Hz), and the median of the highest modulation frequency that evoked significant phase-locking was also 130 Hz. Both values are much higher than reported from the auditory cortex of other mammals, with more than 51% of the units preferring modulation frequencies exceeding 100 Hz. Conspicuously, the fast modulations preferred by the neurons match the fast amplitude and frequency modulations of prosocial, and mostly of aggressive, communication calls in P. discolor. We suggest that the preference for fast amplitude modulations in the P. discolor dorsal auditory cortex serves to reliably encode the fast modulations seen in their communication calls. NEW & NOTEWORTHY Neural processing of temporal sound features is crucial for the analysis of communication calls. In bats, these calls are often characterized by fast temporal envelope modulations. Because auditory cortex neurons typically encode only low modulation frequencies, it is unclear how species-specific vocalizations are cortically processed. We show that auditory cortex neurons in the bat Phyllostomus discolor encode fast temporal envelope modulations. This property improves response specificity to communication calls and thus might support species-specific communication.

Early amygdala damage alters the way rhesus macaques process species-specific audio-visual vocalizations.

Perceiving, integrating, and interpreting multimodal signals are essential for social success, but the neural substrates mediating these functions are not fully understood. This study examined the role of the amygdala in processing bimodal species-specific vocalizations using eye tracking in rhesus macaques. Looking behavior of 6 adult rhesus monkeys with neonatal amygdala lesions (Neo-Aibo; 3M, 3F) was compared with that of 6 sham-operated controls (Neo-C; 3M, 3F). Two side-by-side videos of unknown male conspecifics emitting different vocalizations were presented with the audio signal matching one video. The percentage of time spent looking at each video was used to assess crossmodal integration ability and the percentages of time spent looking at a priori regions of interest (ROIs; eyes, mouth, and rest of each video) were used to characterize scanning patterns. Both groups looked more to one video, indicating that early amygdalar damage did not impair crossmodal integration of complex social signals. However, scanning patterns differed across groups as a function of sex and stimulus parameter. Whereas Neo-C males exhibited differential viewing to the eye and mouth regions as a function of the relative identity of the stimulus animals and Neo-C females made similar distinctions as a function of the relative valence of the vocalizations in females, Neo-Aibo males and females scanned these regions similarly across all trial types. The results suggest that neonatal amygdala damage alters the ability to perceive the social relevance of stimulus features, and are consistent with a role of the amygdala in the recognition of the social salience of complex cues. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Putting it in Context: Linking Auditory Processing with Social Behavior Circuits in the Vertebrate Brain.

Context is critical to the adaptive value of communication. Sensory systems such as the auditory system represent an important juncture at which information on physiological state or social valence can be added to communicative information. However, the neural pathways that convey context to the auditory system are not well understood. The serotonergic system offers an excellent model to address these types of questions. Serotonin fluctuates in the mouse inferior colliculus (IC), an auditory midbrain region important for species-specific vocalizations, during specific social and non-social contexts. Furthermore, serotonin is an indicator of the valence of event-based changes within individual social interactions. We propose a model in which the brain's social behavior network serves as an afferent effector of the serotonergic dorsal raphe nucleus in order to gate contextual release of serotonin in the IC. Specifically, discrete vasopressinergic nuclei within the hypothalamus and extended amygdala that project to the dorsal raphe are functionally engaged during contexts in which serotonin fluctuates in the IC. Since serotonin strongly influences the responses of IC neurons to social vocalizations, this pathway could serve as a feedback loop whereby integrative social centers modulate their own sources of input. The end result of this feedback would be to produce a process that is geared, from sensory input to motor output, toward responding appropriately to a dynamic external world.

Brain Functional Asymmetry of Chimpanzees (Pan troglodytes): the Example of Auditory Laterality

Abstract The aim of this study was to verify whether chimpanzees (Pan troglodytes) demonstrate an auditory laterality during the orientation reaction, and which hemisphere is responsible for processing the emotional stimuli and which for the species-specific vocalizations. The study involved nine chimpanzees from the Warsaw Municipal Zoological Garden. They were tested individually in their bedrooms. Chimpanzees approached a tube filled with food, located in the centre of the cage. Randomly selected sounds were played from the speakers when the subject was focused on getting food. Individual reactions were observed and outcomes reported. The four types of sound used: thunderstorm, dog barking, chimpanzee vocalization and a zookeeper’s voice. To test whether chimpanzees demonstrate auditory laterality we used a single sample X2 test. The existence of auditory laterality has been confirmed. The sound of the storm caused the orientation reaction to the left, while chimpanzee vocalization - to the right. On this basis we can conclude that among chimpanzees, arousing stimuli are being processed by the right hemisphere, and species-specific vocalizations by the left. However, the set of stimuli was limited so the study did not unequivocally resolve this issue.

Spectral summation and facilitation in on- and off-responses for optimized representation of communication calls in mouse inferior colliculus.

Selectivity for processing of species-specific vocalizations and communication sounds has often been associated with the auditory cortex. The midbrain inferior colliculus, however, is the first center in the auditory pathways of mammals integrating acoustic information processed in separate nuclei and channels in the brainstem and, therefore, could significantly contribute to enhance the perception of species' communication sounds. Here, we used natural wriggling calls of mouse pups, which communicate need for maternal care to adult females, and further 15 synthesized sounds to test the hypothesis that neurons in the central nucleus of the inferior colliculus of adult females optimize their response rates for reproduction of the three main harmonics (formants) of wriggling calls. The results confirmed the hypothesis showing that average response rates, as recorded extracellularly from single units, were highest and spectral facilitation most effective for both onset and offset responses to the call and call models with three resolved frequencies according to critical bands in perception. In addition, the general on- and/or off-response enhancement in almost half the investigated 122 neurons favors not only perception of single calls but also of vocalization rhythm. In summary, our study provides strong evidence that critical-band resolved frequency components within a communication sound increase the probability of its perception by boosting the signal-to-noise ratio of neural response rates within the inferior colliculus for at least 20% (our criterion for facilitation). These mechanisms, including enhancement of rhythm coding, are generally favorable to processing of other animal and human vocalizations, including formants of speech sounds.

Call combinations, vocal exchanges and interparty movement in wild bonobos

The vocal repertoire of nonhuman primates is largely fixed. Individuals produce their species-specific vocalizations from a young age, and do not acquire new call types over their lifetime. Despite these limitations, however, monkeys and apes are able to increase their vocal flexibility in several ways, including subtle acoustic modification, call combinations, turn-taking and call persistence. Although primates have been observed to utilize these communicative features, the extent to which they integrate these abilities is not known. Here we show that certain long-distance calls produced by wild bonobos, Pan paniscus, assimilate several aspects of vocal flexibility in ways not previously documented in nonhuman primates. Communication between foraging parties exhibits context-specific call combinations relating to the movement of caller, call modifications that potentially target particular individuals, call-and-answer exchanges in which the initial caller's behaviour depends on the listener's reply, and possible persistence in call production. The selective pressure exerted by bonobos' fission–fusion social structure has likely favoured the integration of these communicative capabilities.