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1.  Efficiency of coding in macaque vocal communication 
Biology Letters  2010;6(4):469-471.
A key characteristic of human language efficiency is that more frequently used words tend to be shorter in length—the ‘law of brevity’. To date, no test of this relationship between frequency of use and length has been carried out on non-human animal vocal communication. We show here that the vocal repertoire of the Formosan macaque (Macaca cyclopis) conforms to the pattern predicted by the law of brevity, with an inverse relationship found between call duration and rate of utterance. This finding provides evidence for coding efficiency in the vocal communication system of this species, and indicates commonality in the basic structure of the coding system between human language and vocal communication in this non-human primate.
PMCID: PMC2936212  PMID: 20106854
Formosan macaque; communication; language; coding; primate
2.  Vocalization Induced CFos Expression in Marmoset Cortex 
All non-human primates communicate with conspecifics using vocalizations, a system involving both the production and perception of species-specific vocal signals. Much of the work on the neural basis of primate vocal communication in cortex has focused on the sensory processing of vocalizations, while relatively little data are available for vocal production. Earlier physiological studies in squirrel monkeys had shed doubts on the involvement of primate cortex in vocal behaviors. The aim of the present study was to identify areas of common marmoset (Callithrix jacchus) cortex that are potentially involved in vocal communication. In this study, we quantified cFos expression in three areas of marmoset cortex – frontal, temporal (auditory), and medial temporal – under various vocal conditions. Specifically, we examined cFos expression in these cortical areas during the sensory, motor (vocal production), and sensory–motor components of vocal communication. Our results showed an increase in cFos expression in ventrolateral prefrontal cortex as well as the medial and lateral belt areas of auditory cortex in the vocal perception condition. In contrast, subjects in the vocal production condition resulted in increased cFos expression only in dorsal premotor cortex. During the sensory–motor condition (antiphonal calling), subjects exhibited cFos expression in each of the above areas, as well as increased expression in perirhinal cortex. Overall, these results suggest that various cortical areas outside primary auditory cortex are involved in primate vocal communication. These findings pave the way for further physiological studies of the neural basis of primate vocal communication.
PMCID: PMC3004388  PMID: 21179582
immediate early gene expression; common marmoset; vocal communication; frontal cortex; auditory cortex; medial temporal cortex
3.  Social learning of vocal structure in a nonhuman primate? 
Non-human primate communication is thought to be fundamentally different from human speech, mainly due to vast differences in vocal control. The lack of these abilities in non-human primates is especially striking if compared to some marine mammals and bird species, which has generated somewhat of an evolutionary conundrum. What are the biological roots and underlying evolutionary pressures of the human ability to voluntarily control sound production and learn the vocal utterances of others? One hypothesis is that this capacity has evolved gradually in humans from an ancestral stage that resembled the vocal behavior of modern primates. Support for this has come from studies that have documented limited vocal flexibility and convergence in different primate species, typically in calls used during social interactions. The mechanisms underlying these patterns, however, are currently unknown. Specifically, it has been difficult to rule out explanations based on genetic relatedness, suggesting that such vocal flexibility may not be the result of social learning.
To address this point, we compared the degree of acoustic similarity of contact calls in free-ranging Campbell's monkeys as a function of their social bonds and genetic relatedness. We calculated three different indices to compare the similarities between the calls' frequency contours, the duration of grooming interactions and the microsatellite-based genetic relatedness between partners. We found a significantly positive relation between bond strength and acoustic similarity that was independent of genetic relatedness.
Genetic factors determine the general species-specific call repertoire of a primate species, while social factors can influence the fine structure of some the call types. The finding is in line with the more general hypothesis that human speech has evolved gradually from earlier primate-like vocal communication.
PMCID: PMC3260242  PMID: 22177339
4.  A Cervid Vocal Fold Model Suggests Greater Glottal Efficiency in Calling at High Frequencies 
PLoS Computational Biology  2010;6(8):e1000897.
Male Rocky Mountain elk (Cervus elaphus nelsoni) produce loud and high fundamental frequency bugles during the mating season, in contrast to the male European Red Deer (Cervus elaphus scoticus) who produces loud and low fundamental frequency roaring calls. A critical step in understanding vocal communication is to relate sound complexity to anatomy and physiology in a causal manner. Experimentation at the sound source, often difficult in vivo in mammals, is simulated here by a finite element model of the larynx and a wave propagation model of the vocal tract, both based on the morphology and biomechanics of the elk. The model can produce a wide range of fundamental frequencies. Low fundamental frequencies require low vocal fold strain, but large lung pressure and large glottal flow if sound intensity level is to exceed 70 dB at 10 m distance. A high-frequency bugle requires both large muscular effort (to strain the vocal ligament) and high lung pressure (to overcome phonation threshold pressure), but at least 10 dB more intensity level can be achieved. Glottal efficiency, the ration of radiated sound power to aerodynamic power at the glottis, is higher in elk, suggesting an advantage of high-pitched signaling. This advantage is based on two aspects; first, the lower airflow required for aerodynamic power and, second, an acoustic radiation advantage at higher frequencies. Both signal types are used by the respective males during the mating season and probably serve as honest signals. The two signal types relate differently to physical qualities of the sender. The low-frequency sound (Red Deer call) relates to overall body size via a strong relationship between acoustic parameters and the size of vocal organs and body size. The high-frequency bugle may signal muscular strength and endurance, via a ‘vocalizing at the edge’ mechanism, for which efficiency is critical.
Author Summary
More than 5,000 species of mammals share a basic larynx design. Many of them use the larynx to produce an enormous variability of sounds, but only in a handful of species has the physiology of sound production been studied. It is impracticable in most species because observation requires invasive techniques. Furthermore, many mammals do not spontaneously vocalize if they are manipulated or handled. We have constructed a finite element model of vocal fold tissue vibration on the basis of morphological and biomechanical features of the Rocky Mountain elk vocal organs. Operating within reasonable physiological parameter ranges, it allows the investigation of sound production efficiency as well as selective forces. The model can produce sounds with fundamental frequencies ranging between 60 and 1,200 Hz, covering not only some of the natural vocal repertoire of the elk's high-pitched bugle calls but also those of its close relative, the European Red Deer, who produces low-pitched roaring sounds with a similar anatomy. The approach is of broader interest, first because techniques can be adapted to other mammal species using only landmark anatomical and biomechanical features, and second, because simulations can serve as playbacks for perception studies investigating the role of vocalizations in communication.
PMCID: PMC2924247  PMID: 20808882
5.  The Effect of Habitat Acoustics on Common Marmoset Vocal Signal Transmission 
American journal of primatology  2013;75(9):904-916.
Noisy acoustic environments present several challenges for the evolution of acoustic communication systems. Among the most significant is the need to limit degradation of spectro-temporal signal structure in order to maintain communicative efficacy. This can be achieved by selecting for several potentially complementary processes. Selection can act on behavioral mechanisms permitting signalers to control the timing and occurrence of signal production to avoid acoustic interference. Likewise, the signal itself may be the target of selection, biasing the evolution of its structure to comprise acoustic features that avoid interference from ambient noise or degrade minimally in the habitat. Here, we address the latter topic for common marmoset (Callithrix jacchus) long-distance contact vocalizations, known as phee calls. Our aim was to test whether this vocalization is specifically adapted for transmission in a species-typical forest habitat, the Atlantic forests of northeastern Brazil. We combined seasonal analyses of ambient habitat acoustics with experiments in which pure tones, clicks, and vocalizations were broadcast and rerecorded at different distances to characterize signal degradation in the habitat. Ambient sound was analyzed from intervals throughout the day and over rainy and dry seasons, showing temporal regularities across varied timescales. Broadcast experiment results indicated that the tone and click stimuli showed the typically inverse relationship between frequency and signaling efficacy. Although marmoset phee calls degraded over distance with marked predictability compared with artificial sounds, they did not otherwise appear to be specially designed for increased transmission efficacy or minimal interference in this habitat. We discuss these data in the context of other similar studies and evidence of potential behavioral mechanisms for avoiding acoustic interference in order to maintain effective vocal communication in common marmosets.
PMCID: PMC3787903  PMID: 23592313
Callithrix jacchus; vocal communication; behavioral ecology; sound broadcasts; sound window
6.  Vocal communication in a complex multi-level society: constrained acoustic structure and flexible call usage in Guinea baboons 
Frontiers in Zoology  2013;10:58.
To understand the evolution of acoustic communication in animals, it is important to distinguish between the structure and the usage of vocal signals, since both aspects are subject to different constraints. In terrestrial mammals, the structure of calls is largely innate, while individuals have a greater ability to actively initiate or withhold calls. In closely related taxa, one would therefore predict a higher flexibility in call usage compared to call structure. In the present study, we investigated the vocal repertoire of free living Guinea baboons (Papio papio) and examined the structure and usage of the animals’ vocal signals. Guinea baboons live in a complex multi-level social organization and exhibit a largely tolerant and affiliative social style, contrary to most other baboon taxa. To classify the vocal repertoire of male and female Guinea baboons, cluster analyses were used and focal observations were conducted to assess the usage of vocal signals in the particular contexts.
In general, the vocal repertoire of Guinea baboons largely corresponded to the vocal repertoire other baboon taxa. The usage of calls, however, differed considerably from other baboon taxa and corresponded with the specific characteristics of the Guinea baboons’ social behaviour. While Guinea baboons showed a diminished usage of contest and display vocalizations (a common pattern observed in chacma baboons), they frequently used vocal signals during affiliative and greeting interactions.
Our study shows that the call structure of primates is largely unaffected by the species’ social system (including grouping patterns and social interactions), while the usage of calls can be more flexibly adjusted, reflecting the quality of social interactions of the individuals. Our results support the view that the primary function of social signals is to regulate social interactions, and therefore the degree of competition and cooperation may be more important to explain variation in call usage than grouping patterns or group size.
PMCID: PMC3849383  PMID: 24059742
Evolution; Vocal communication; Call structure; Call usage; Guinea baboon; Social complexity; Competition
7.  Wireless multi-channel single unit recording in freely moving and vocalizing primates 
Journal of neuroscience methods  2011;203(1):10.1016/j.jneumeth.2011.09.004.
The ability to record well-isolated action potentials from individual neurons in naturally behaving animals is crucial for understanding neural mechanisms underlying natural behaviors. Traditional neurophysiology techniques, however, require the animal to be restrained which often restricts natural behavior. An example is the common marmoset (Callithrix jacchus), a highly vocal New World primate species, used in our laboratory to study the neural correlates of vocal production and sensory feedback. When restrained by traditional neurophysiological techniques marmoset vocal behavior is severely inhibited. Tethered recording systems, while proven effective in rodents pose limitations in arboreal animals such as the marmoset that typically roam in a three-dimensional environment. To overcome these obstacles, we have developed a wireless neural recording technique that is capable of collecting single-unit data from chronically implanted multi-electrodes in freely moving marmosets. A lightweight, low power and low noise wireless transmitter (headstage) is attached to a multi-electrode array placed in the premotor cortex of the marmoset. The wireless headstage is capable of transmitting 15 channels of neural data with signal-to-noise ratio (SNR) comparable to a tethered system. To minimize radio-frequency (RF) and electro-magnetic interference (EMI), the experiments were conducted within a custom designed RF/EMI and acoustically shielded chamber. The individual electrodes of the multi-electrode array were periodically advanced to densely sample the cortical layers. We recorded single-unit data over a period of several months from the frontal cortex of two marmosets. These recordings demonstrate the feasibility of using our wireless recording method to study single neuron activity in freely roaming primates.
PMCID: PMC3848526  PMID: 21933683
Action potential; free-roaming; marmoset; multi-channel; multi-electrode array; natural behavior; neurophysiology; neural telemetry; primate; single-unit; vocalization; wireless
8.  Convergent Differential Regulation of Parvalbumin in the Brains of Vocal Learners 
PLoS ONE  2012;7(1):e29457.
Spoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds – songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associated brain pathways for vocal communication. However, it is not clear whether this behavioral and anatomical convergence is associated with molecular convergence. Here we used oligo microarrays to screen for genes differentially regulated in brain nuclei necessary for producing learned vocalizations relative to adjacent brain areas that control other behaviors in avian vocal learners versus vocal non-learners. A top candidate gene in our screen was a calcium-binding protein, parvalbumin (PV). In situ hybridization verification revealed that PV was expressed significantly higher throughout the song motor pathway, including brainstem vocal motor neurons relative to the surrounding brain regions of all distantly related avian vocal learners. This differential expression was specific to PV and vocal learners, as it was not found in avian vocal non-learners nor for control genes in learners and non-learners. Similar to the vocal learning birds, higher PV up-regulation was found in the brainstem tongue motor neurons used for speech production in humans relative to a non-human primate, macaques. These results suggest repeated convergent evolution of differential PV up-regulation in the brains of vocal learners separated by more than 65–300 million years from a common ancestor and that the specialized behaviors of learned song and speech may require extra calcium buffering and signaling.
PMCID: PMC3253077  PMID: 22238614
9.  Multilevel Societies in New World Primates? Flexibility May Characterize the Organization of Peruvian Red Uakaris (Cacajao calvus ucayalii) 
International Journal of Primatology  2012;33(5):1110-1124.
Researchers have described multilevel societies with one-male, multifemale units (OMUs) forming within a larger group in several catarrhine species, but not in platyrhines. OMUs in multilevel societies are associated with extremely large group sizes, often with >100 individuals, and the only platyrhine genus that forms groups of this size is Cacajao. We review available evidence for multilevel organization and the formation of OMUs in groups of Cacajao, and test predictions for the frequency distribution patterns of male–male and male–female interindividual distances within groups of red-faced uakaris (Cacajao calvus ucayalii), comparing year-round data with those collected at the peak of the breeding season, when group cohesion may be more pronounced. Groups of Cacajao fission and fuse, forming subgroup sizes at frequencies consistent with an OMU organization. In Cacajao calvus ucayalii and Cacajao calvus calvus, bachelor groups are also observed, a characteristic of several catarrhine species that form OMUs. However, researchers have observed both multimale–multifemale groups and groups with a single male and multiple females in Cacajao calvus. The frequency distributions of interindividual distances for male–male and male–female dyads are consistent with an OMU-based organization, but alternative interpretations of these data are possible. The distribution of interindividual distances collected during the peak breeding season differed from those collected year-round, indicating seasonal changes in the spatial organization of Cacajao calvus ucayalii. We suggest a high degree of flexibility may characterize the social organization of Cacajao calvus ucayalii, which may form OMUs under certain conditions. Further studies with identifiable individuals, thus far not possible in Cacajao, are required to confirm the social organization.
PMCID: PMC3456913  PMID: 23024445
Breeding system; Mating system; One-male unit; Pitheciine; Social structure
10.  Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates 
Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2–12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with ‘their’ females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.
PMCID: PMC3367700  PMID: 22641823
derived vocalizations; group size; homologous vocalizations; social complexity; vocal complexity; vocal repertoire
11.  Ultrasonic vocalizations in mouse models for speech and socio-cognitive disorders: insights into the evolution of vocal communication 
Genes, Brain, and Behavior  2011;10(1):17-27.
Comparative analyses used to reconstruct the evolution of traits associated with the human language faculty, including its socio-cognitive underpinnings, highlight the importance of evolutionary constraints limiting vocal learning in non-human primates. After a brief overview of this field of research and the neural basis of primate vocalizations, we review studies that have addressed the genetic basis of usage and structure of ultrasonic communication in mice, with a focus on the gene FOXP2 involved in specific language impairments and neuroligin genes (NL-3 and NL-4) involved in autism spectrum disorders. Knockout of FoxP2 leads to reduced vocal behavior and eventually premature death. Introducing the human variant of FoxP2 protein into mice, in contrast, results in shifts in frequency and modulation of pup ultrasonic vocalizations. Knockout of NL-3 and NL-4 in mice diminishes social behavior and vocalizations. Although such studies may provide insights into the molecular and neural basis of social and communicative behavior, the structure of mouse vocalizations is largely innate, limiting the suitability of the mouse model to study human speech, a learned mode of production. Although knockout or replacement of single genes has perceptible effects on behavior, these genes are part of larger networks whose functions remain poorly understood. In humans, for instance, deficiencies in NL-4 can lead to a broad spectrum of disorders, suggesting that further factors (experiential and/or genetic) contribute to the variation in clinical symptoms. The precise nature as well as the interaction of these factors is yet to be determined.
PMCID: PMC3047712  PMID: 20579107
Autism; communication; evolution; FOXP2; mice; neuroligin; speech; ultrasound; vocalization
12.  Plasticity in Primary Auditory Cortex of Monkeys with Altered Vocal Production 
Response properties of primary auditory cortical neurons in the adult common marmoset monkey (Callithrix jacchus) were modified by extensive exposure to altered vocalizations that were self-generated and rehearsed frequently. A laryngeal apparatus modification procedure permanently lowered the frequency content of the native twitter call, a complex communication vocalization consisting of a series of frequency modulation (FM) sweeps. Monkeys vocalized shortly after this procedure and maintained voicing efforts until physiological evaluation 5–15 months later. The altered twitter calls improved overtime, with FM sweeps approaching but never reaching the normal spectral range. Neurons with characteristic frequencies <4.3 kHz that had been weakly activated by native twitter calls were recruited to encode self-uttered altered twitter vocalizations. These neurons showed a decrease in response magnitude and an increase in temporal dispersion of response timing to twitter call and parametric FM stimuli but a normal response profile to pure tone stimuli. Tonotopic maps in voice-modified monkeys were not distorted. These findings suggest a previously unrecognized form of cortical plasticity that is specific to higher-order processes involved in the discrimination of more complex sounds, such as species-specific vocalizations.
PMCID: PMC4060626  PMID: 15758157
auditory cortex; plasticity; primate; vocalization; learning; twitter call
13.  Your attention please: increasing ambient noise levels elicits a change in communication behaviour in humpback whales (Megaptera novaeangliae) 
High background noise is an important obstacle in successful signal detection and perception of an intended acoustic signal. To overcome this problem, many animals modify their acoustic signal by increasing the repetition rate, duration, amplitude or frequency range of the signal. An alternative method to ensure successful signal reception, yet to be tested in animals, involves the use of two different types of signal, where one signal type may enhance the other in periods of high background noise. Humpback whale communication signals comprise two different types: vocal signals, and surface-generated signals such as ‘breaching’ or ‘pectoral slapping’. We found that humpback whales gradually switched from primarily vocal to primarily surface-generated communication in increasing wind speeds and background noise levels, though kept both signal types in their repertoire. Vocal signals have the advantage of having higher information content but may have the disadvantage of loosing this information in a noisy environment. Surface-generated sounds have energy distributed over a greater frequency range and may be less likely to become confused in periods of high wind-generated noise but have less information content when compared with vocal sounds. Therefore, surface-generated sounds may improve detection or enhance the perception of vocal signals in a noisy environment.
PMCID: PMC2894914  PMID: 20392731
acoustic communication; humpback whales; background noise; acoustic behaviour; communication strategy
14.  Social Vocalizations of Big Brown Bats Vary with Behavioral Context 
PLoS ONE  2012;7(9):e44550.
Bats are among the most gregarious and vocal mammals, with some species demonstrating a diverse repertoire of syllables under a variety of behavioral contexts. Despite extensive characterization of big brown bat (Eptesicus fuscus) biosonar signals, there have been no detailed studies of adult social vocalizations. We recorded and analyzed social vocalizations and associated behaviors of captive big brown bats under four behavioral contexts: low aggression, medium aggression, high aggression, and appeasement. Even limited to these contexts, big brown bats possess a rich repertoire of social vocalizations, with 18 distinct syllable types automatically classified using a spectrogram cross-correlation procedure. For each behavioral context, we describe vocalizations in terms of syllable acoustics, temporal emission patterns, and typical syllable sequences. Emotion-related acoustic cues are evident within the call structure by context-specific syllable types or variations in the temporal emission pattern. We designed a paradigm that could evoke aggressive vocalizations while monitoring heart rate as an objective measure of internal physiological state. Changes in the magnitude and duration of elevated heart rate scaled to the level of evoked aggression, confirming the behavioral state classifications assessed by vocalizations and behavioral displays. These results reveal a complex acoustic communication system among big brown bats in which acoustic cues and call structure signal the emotional state of a caller.
PMCID: PMC3436781  PMID: 22970247
15.  The covariation of acoustic features of infant cries and autonomic state 
Physiology & behavior  2013;120:10.1016/j.physbeh.2013.07.003.
The evolution of the autonomic nervous system provides an organizing principle to interpret the adaptive significance of physiological systems in promoting social behavior and responding to social challenges. This phylogenetic shift in neural regulation of the autonomic nervous system in mammals has produced a neuroanatomically integrated social engagement system, including neural mechanisms that regulate both cardiac vagal tone and muscles involved in vocalization. Mammalian vocalizations are part of a conspecific social communication system, with several mammalian species modulating acoustic features of vocalizations to signal affective state. Prosody, defined by variations in rhythm and pitch, is a feature of mammalian vocalizations that communicate emotion and affective state. While the covariation between physiological state and the acoustic frequencies of vocalizations is neurophysiologically based, few studies have investigated the covariation between vocal prosody and autonomic state. In response to this paucity of scientific evidence, the current study explored the utility of vocal prosody as a sensitive index of autonomic activity in human infants during the Still Face challenge. Overall, significant correlations were observed between several acoustic features of the infant vocalizations and autonomic state, demonstrating an association between shorter heart period and reductions in heart period and respiratory sinus arrhythmia following the challenge with the dampening of the modulation of acoustic features (fundamental frequency, variance, 50% bandwidth, and duration) that are perceived as prosody.
PMCID: PMC3843764  PMID: 23911689
Infant vocalizations; Prosody; Polyvagal Theory; Autonomic nervous system; Heart rate; Respiratory sinus arrhythmia
16.  Auditory Cortical Detection and Discrimination Correlates with Communicative Significance 
PLoS Biology  2007;5(7):e173.
Plasticity studies suggest that behavioral relevance can change the cortical processing of trained or conditioned sensory stimuli. However, whether this occurs in the context of natural communication, where stimulus significance is acquired through social interaction, has not been well investigated, perhaps because neural responses to species-specific vocalizations can be difficult to interpret within a systematic framework. The ultrasonic communication system between isolated mouse pups and adult females that either do or do not recognize the calls' significance provides an opportunity to explore this issue. We applied an information-based analysis to multi- and single unit data collected from anesthetized mothers and pup-naïve females to quantify how the communicative significance of pup calls affects their encoding in the auditory cortex. The timing and magnitude of information that cortical responses convey (at a 2-ms resolution) for pup call detection and discrimination was significantly improved in mothers compared to naïve females, most likely because of changes in call frequency encoding. This was not the case for a non-natural sound ensemble outside the mouse vocalization repertoire. The results demonstrate that a sensory cortical change in the timing code for communication sounds is correlated with the vocalizations' behavioral relevance, potentially enhancing functional processing by improving its signal to noise ratio.
Author Summary
Like a student in a foreign country immersed in an unfamiliar language or a young mother trying to decipher her baby's cries, we all encounter initially meaningless sounds that in fact carry meaning. As these sounds gain significance, we become better at detecting and discriminating between them. How does this occur? What happens in our brain to facilitate this improvement? We explored these questions in a mouse model by measuring how neurons in the auditory cortex of female mice respond when the ultrasonic calls of mouse pups are played back to the animals. Earlier studies demonstrated that mothers, but not virgin females, recognize these calls as behaviorally significant. Our results indicate that the timing and magnitude of the auditory cortical responses to these communicative sounds differ between these two groups of female mice and that this difference may provide the auditory system in mothers with the capacity for detecting and discriminating pup calls. The results demonstrate that behavioral significance can be correlated with quantifiable functional improvements in the sensory cortical representation of a communication sound.
Pup calls produce quicker and larger neural responses, which convey more information for pup call detection and discrimination, in the auditory cortex of mother mice compared with virgin female mice.
PMCID: PMC1891324  PMID: 17564499
17.  The Syntax and Meaning of Wild Gibbon Songs 
PLoS ONE  2006;1(1):e73.
Spoken language is a result of the human capacity to assemble simple vocal units into more complex utterances, the basic carriers of semantic information. Not much is known about the evolutionary origins of this behaviour. The vocal abilities of non-human primates are relatively unimpressive in comparison, with gibbon songs being a rare exception. These apes assemble a repertoire of call notes into elaborate songs, which function to repel conspecific intruders, advertise pair bonds, and attract mates. We conducted a series of field experiments with white-handed gibbons at Khao Yai National Park, Thailand, which showed that this ape species uses songs also to protect themselves against predation. We compared the acoustic structure of predatory-induced songs with regular songs that were given as part of their daily routine. Predator-induced songs were identical to normal songs in the call note repertoire, but we found consistent differences in how the notes were assembled into songs. The responses of out-of-sight receivers demonstrated that these syntactic differences were meaningful to conspecifics. Our study provides the first evidence of referential signalling in a free-ranging ape species, based on a communication system that utilises combinatorial rules.
PMCID: PMC1762393  PMID: 17183705
18.  Noise Pollution Filters Bird Communities Based on Vocal Frequency 
PLoS ONE  2011;6(11):e27052.
Human-generated noise pollution now permeates natural habitats worldwide, presenting evolutionarily novel acoustic conditions unprecedented to most landscapes. These acoustics not only harm humans, but threaten wildlife, and especially birds, via changes to species densities, foraging behavior, reproductive success, and predator-prey interactions. Explanations for negative effects of noise on birds include disruption of acoustic communication through energetic masking, potentially forcing species that rely upon acoustic communication to abandon otherwise suitable areas. However, this hypothesis has not been adequately tested because confounding stimuli often co-vary with noise and are difficult to separate from noise exposure.
Methodology/Principal Findings
Using a natural experiment that controls for confounding stimuli, we evaluate whether species vocal features or urban-tolerance classifications explain their responses to noise measured through habitat use. Two data sets representing nesting and abundance responses reveal that noise filters bird communities nonrandomly. Signal duration and urban tolerance failed to explain species-specific responses, but birds with low-frequency signals that are more susceptible to masking from noise avoided noisy areas and birds with higher frequency vocalizations remained. Signal frequency was also negatively correlated with body mass, suggesting that larger birds may be more sensitive to noise due to the link between body size and vocal frequency.
Our findings suggest that acoustic masking by noise may be a strong selective force shaping the ecology of birds worldwide. Larger birds with lower frequency signals may be excluded from noisy areas, whereas smaller species persist via transmission of higher frequency signals. We discuss our findings as they relate to interspecific relationships among body size, vocal amplitude and frequency and suggest that they are immediately relevant to the global problem of increases in noise by providing critical insight as to which species traits influence tolerance of these novel acoustics.
PMCID: PMC3212537  PMID: 22096517
19.  Temporal vocal features suggest different call-pattern generating mechanisms in mice and bats 
BMC Neuroscience  2013;14:99.
Mice produce ultrasonic vocalizations in various inter-individual encounters and with high call rates. However, it is so far virtually unknown how these vocal patterns are generated. On the one hand, these vocal patterns could be embedded into the normal respiratory cycle, as happens in bats and other mammals that produce similar call rates and frequencies. On the other, mice could possess distinct vocal pattern generating systems that are capable of modulating the respiratory cycle, which is what happens in non-human and human primates. In the present study, we investigated the temporal call patterns of two different mammalian species, bats and mice, in order to differentiate between these two possibilities for mouse vocalizations. Our primary focus was on comparing the mechanisms for the production of rapid, successive ultrasound calls of comparable frequency ranges in the two species.
We analyzed the temporal call pattern characteristics of mice, and we compared these characteristics to those of ultrasonic echolocation calls produced by horseshoe bats. We measured the distributions of call durations, call intervals, and inter-call intervals in the two species. In the bat, and consistent with previous studies, we found that call duration was independent of corresponding call intervals, and that it was negatively correlated with the corresponding inter-call interval. This indicates that echolocation call production mechanisms in the bat are highly correlated with the respiratory cycle. In contrast, call intervals in the mouse were directly correlated with call duration. Importantly, call duration was not, or was only slightly, correlated with inter-call intervals, consistent with the idea that vocal production in the mouse is largely independent of the respiratory cycle.
Our findings suggest that ultrasonic vocalizations in mice are produced by call-pattern generating mechanisms that seem to be similar to those that have been found in primates. This is in contrast to the production mechanisms of ultrasonic echolocation calls in horseshoe bats. These results are particularly interesting, especially since mouse vocalizations have recently attracted increased attention as potential indicators for the degree of progression of several disease patterns in mouse models for neurodegenerative and neurodevelopmental disorders of humans.
PMCID: PMC3846851  PMID: 24020588
Acoustic communication; Bat; Mammal; Mice; Mouse model; Vocal pattern generation
20.  Social drive and the evolution of primate hearing 
The structure and function of primate communication have attracted much attention, and vocal signals, in particular, have been studied in detail. As a general rule, larger social groups emit more types of vocal signals, including those conveying the presence of specific types of predators. The adaptive advantages of receiving and responding to alarm calls are expected to exert a selective pressure on the auditory system. Yet, the comparative biology of primate hearing is limited to select species, and little attention has been paid to the effects of social and vocal complexity on hearing. Here, we use the auditory brainstem response method to generate the largest number of standardized audiograms available for any primate radiation. We compared the auditory sensitivities of 11 strepsirrhine species with and without independent contrasts and show that social complexity explains a significant amount of variation in two audiometric parameters—overall sensitivity and high-frequency limit. We verified the generality of this latter result by augmenting our analysis with published data from nine species spanning the primate order. To account for these findings, we develop and test a model of social drive. We hypothesize that social complexity has favoured enhanced hearing sensitivities, especially at higher frequencies.
PMCID: PMC3367701  PMID: 22641824
Strepsirrhini; hearing; auditory brainstem response; evoked potential audiogram; sensory ecology; acoustic communication
21.  Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini) 
Genetics and Molecular Biology  2009;32(4):786-791.
In order to study the intra- and interspecific variability of the 14/15 association in Platyrrhini, we analyzed 15 species from 13 genera, including species that had not been described yet. The DNA libraries of human chromosomes 14 and 15 were hybridized to metaphases of Alouatta guariba clamitans, A. caraya, A. sara, Ateles paniscus chamek, Lagothrix lagothricha, Brachyteles arachnoides, Saguinus midas midas, Leontopithecus chrysomelas, Callimico goeldii, Callithrix sp., Cebus apella, Aotus nigriceps, Cacajao melanocephalus,Chiropotes satanas and Callicebus caligatus. The 14/15 hybridization pattern was present in 13 species, but not in Alouatta sara that showed a 14/15/14 pattern and Aotus nigriceps that showed a 15/14/15/14 pattern. In the majority of the species, the HSA 14 homologue retained synteny for the entire chromosome, whereas the HSA 15 homologue displayed fragmented segments. Within primates, the New World monkeys represent the taxon with the highest variability in chromosome number (2n = 16 to 62). The presence of the HSA 14/15 association in all species and subspecies studied herein confirms that this association is the ancestral condition for platyrrhines and that this association has been retained in most platyrrhines, despite the occurrence of extensive inter- and intrachromosomal rearrangements in this infraorder of Primates.
PMCID: PMC3036896  PMID: 21637455
HSA 14/15 synteny; homologies; chromosomal evolution; Platyrrhini; New World monkeys
22.  Segmental concatenation of individual signatures and context cues in banded mongoose (Mungos mungo) close calls 
BMC Biology  2012;10:97.
All animals are anatomically constrained in the number of discrete call types they can produce. Recent studies suggest that by combining existing calls into meaningful sequences, animals can increase the information content of their vocal repertoire despite these constraints. Additionally, signalers can use vocal signatures or cues correlated to other individual traits or contexts to increase the information encoded in their vocalizations. However, encoding multiple vocal signatures or cues using the same components of vocalizations usually reduces the signals' reliability. Segregation of information could effectively circumvent this trade-off. In this study we investigate how banded mongooses (Mungos mungo) encode multiple vocal signatures or cues in their frequently emitted graded single syllable close calls.
The data for this study were collected on a wild, but habituated, population of banded mongooses. Using behavioral observations and acoustical analysis we found that close calls contain two acoustically different segments. The first being stable and individually distinct, and the second being graded and correlating with the current behavior of the individual, whether it is digging, searching or moving. This provides evidence of Marler's hypothesis on temporal segregation of information within a single syllable call type. Additionally, our work represents an example of an identity cue integrated as a discrete segment within a single call that is independent from context. This likely functions to avoid ambiguity between individuals or receivers having to keep track of several context-specific identity cues.
Our study provides the first evidence of segmental concatenation of information within a single syllable in non-human vocalizations. By reviewing descriptions of call structures in the literature, we suggest a general application of this mechanism. Our study indicates that temporal segregation and segmental concatenation of vocal signatures or cues is likely a common, but so far neglected, dimension of information coding in animal vocal communication. We argue that temporal segregation of vocal signatures and cues evolves in species where communication of multiple unambiguous signals is crucial, but is limited by the number of call types produced.
PMCID: PMC3529192  PMID: 23206242
vocal signature; vocal cue; syllable; close call; segregation of information; graded calls; banded mongoose; segmental concatenation
23.  The consequences of Zipf's law for syntax and symbolic reference 
Although many species possess rudimentary communication systems, humans seem to be unique with regard to making use of syntax and symbolic reference. Recent approaches to the evolution of language formalize why syntax is selectively advantageous compared with isolated signal communication systems, but do not explain how signals naturally combine. Even more recent work has shown that if a communication system maximizes communicative efficiency while minimizing the cost of communication, or if a communication system constrains ambiguity in a non-trivial way while a certain entropy is maximized, signal frequencies will be distributed according to Zipf's law. Here we show that such communication principles give rise not only to signals that have many traits in common with the linking words in real human languages, but also to a rudimentary sort of syntax and symbolic reference.
PMCID: PMC1578703  PMID: 15799952
Zipf's law; syntax; symbolic reference; human language
24.  Differential Expression of Glutamate Receptors in Avian Neural Pathways for Learned Vocalization 
Learned vocalization, the substrate for human language, is a rare trait. It is found in three distantly related groups of birds—parrots, hummingbirds, and songbirds. These three groups contain cerebral vocal nuclei for learned vocalization not found in their more closely related vocal nonlearning relatives. Here, we cloned 21 receptor subunits/subtypes of all four glutamate receptor families (AMPA, kainate, NMDA, and metabotropic) and examined their expression in vocal nuclei of songbirds. We also examined expression of a subset of these receptors in vocal nuclei of hummingbirds and parrots, as well as in the brains of dove species as examples of close vocal nonlearning relatives. Among the 21 subunits/subtypes, 19 showed higher and/or lower prominent differential expression in songbird vocal nuclei relative to the surrounding brain subdivisions in which the vocal nuclei are located. This included relatively lower levels of all four AMPA subunits in lMAN, strikingly higher levels of the kainite subunit GluR5 in the robust nucleus of the arcopallium (RA), higher and lower levels respectively of the NMDA subunits NR2A and NR2B in most vocal nuclei and lower levels of the metabotropic group I subtypes (mGluR1 and -5) in most vocal nuclei and the group II subtype (mGluR2), showing a unique expression pattern of very low levels in RA and very high levels in HVC. The splice variants of AMPA subunits showed further differential expression in vocal nuclei. Some of the receptor subunits/subtypes also showed differential expression in hummingbird and parrot vocal nuclei. The magnitude of differential expression in vocal nuclei of all three vocal learners was unique compared with the smaller magnitude of differences found for nonvocal areas of vocal learners and vocal nonlearners. Our results suggest that evolution of vocal learning was accompanied by differential expression of a conserved gene family for synaptic transmission and plasticity in vocal nuclei. They also suggest that neural activity and signal transduction in vocal nuclei of vocal learners will be different relative to the surrounding brain areas.
PMCID: PMC2517240  PMID: 15236466
song system; song nuclei; neurotransmitter
25.  Assessing vocal performance in complex birdsong: a novel approach 
BMC Biology  2014;12(1):58.
Vocal performance refers to the ability to produce vocal signals close to physical limits. Such motor skills can be used by conspecifics to assess a signaler’s competitive potential. For example it is difficult for birds to produce repeated syllables both rapidly and with a broad frequency bandwidth. Deviation from an upper-bound regression of frequency bandwidth on trill rate has been widely used to assess vocal performance. This approach is, however, only applicable to simple trilled songs, and even then may be affected by differences in syllable complexity.
Using skylarks (Alauda arvensis) as a birdsong model with a very complex song structure, we detected another performance trade-off: minimum gap duration between syllables was longer when the frequency ratio between the end of one syllable and the start of the next syllable (inter-syllable frequency shift) was large. This allowed us to apply a novel measure of vocal performance - vocal gap deviation: the deviation from a lower-bound regression of gap duration on inter-syllable frequency shift. We show that skylarks increase vocal performance in an aggressive context suggesting that this trait might serve as a signal for competitive potential.
We suggest using vocal gap deviation in future studies to assess vocal performance in songbird species with complex structure.
Electronic supplementary material
The online version of this article (doi:10.1186/s12915-014-0058-4) contains supplementary material, which is available to authorized users.
PMCID: PMC4243327  PMID: 25096363
Aggressive signaling; Alauda arvensis; Birdsong; Complex song; Contextual variation; Production limits

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