Babbling opens the sensory phase for imitative vocal learning.

Zebra finches, a species of songbirds, learn to sing by creating an auditory template through the memorization of model songs (sensory learning phase) and subsequently translating these perceptual memories into motor skills (sensorimotor learning phase). It has been traditionally believed that babbling in juvenile birds initiates the sensorimotor phase while the sensory phase of song learning precedes the onset of babbling. However, our findings challenge this notion by demonstrating that testosterone-induced premature babbling actually triggers the onset of the sensory learning phase instead. We reveal that juvenile birds must engage in babbling and self-listening to acquire the tutor song as the template. Notably, the sensory learning of the template in songbirds requires motor vocal activity, reflecting the observation that prelinguistic babbling in humans plays a crucial role in auditory learning for language acquisition.

Multiple processes of vocal sensory-motor interaction in primate auditory cortex.

Sensory-motor interactions in the auditory system play an important role in vocal self-monitoring and control. These result from top-down corollary discharges, relaying predictions about vocal timing and acoustics. Recent evidence suggests such signals may be two distinct processes, one suppressing neural activity during vocalization and another enhancing sensitivity to sensory feedback, rather than a single mechanism. Single-neuron recordings have been unable to disambiguate due to overlap of motor signals with sensory inputs. Here, we sought to disentangle these processes in marmoset auditory cortex during production of multi-phrased 'twitter' vocalizations. Temporal responses revealed two timescales of vocal suppression: temporally-precise phasic suppression during phrases and sustained tonic suppression. Both components were present within individual neurons, however, phasic suppression presented broadly regardless of frequency tuning (gating), while tonic was selective for vocal frequencies and feedback (prediction). This suggests that auditory cortex is modulated by concurrent corollary discharges during vocalization, with different computational mechanisms.

The role of cerebellum in learned vocal communication in adult songbirds.

Injury, tumors, ischemia, and lesions in the cerebellum show the involvement of this region in human speech. The association of the cerebellum with learned birdsong has only been identified recently. Cerebellar dysfunction in young songbirds causes learning disabilities, but its role in adult songbirds has not been established. The aim of this study was to investigate the role of the deep cerebellar nuclei (DCN) in adult birdsong. We created bilateral excitotoxic lesions in the DCN of adult male zebra finches (Taeniopygia guttata) and recorded their songs for up to 4 months. Using magnetic resonance imaging (MRI) and immunohistochemistry, we validated the lesion efficacy. We found that the song duration significantly increased from 14 weeks post-op; the increase in duration was caused by a greater number of introductory notes as well as a greater number of syllables sung after the introductory notes. On the other hand, the motif duration decreased from 8 weeks after DCN lesions were induced, which was due to faster singing of syllables, not changes in inter-syllable interval length. DCN lesions also caused a decrease in the fundamental frequency of syllables. In summary, we showed that DCN lesions influence the temporal and acoustic features of birdsong. These results suggest that the cerebellum influences singing in adult songbirds.

Language-like efficiency and structure in house finch song.

Communication needs to be complex enough to be functional while minimizing learning and production costs. Recent work suggests that the vocalizations and gestures of some songbirds, cetaceans and great apes may conform to linguistic laws that reflect this trade-off between efficiency and complexity. In studies of non-human communication, though, clustering signals into types cannot be done a priori, and decisions about the appropriate grain of analysis may affect statistical signals in the data. The aim of this study was to assess the evidence for language-like efficiency and structure in house finch (Haemorhous mexicanus) song across three levels of granularity in syllable clustering. The results show strong evidence for Zipf's rank-frequency law, Zipf's law of abbreviation and Menzerath's law. Additional analyses show that house finch songs have small-world structure, thought to reflect systematic structure in syntax, and the mutual information decay of sequences is consistent with a combination of Markovian and hierarchical processes. These statistical patterns are robust across three levels of granularity in syllable clustering, pointing to a limited form of scale invariance. In sum, it appears that house finch song has been shaped by pressure for efficiency, possibly to offset the costs of female preferences for complexity.

Synthesizing avian dreams.

During sleep, sporadically, it is possible to find neural patterns of activity in areas of the avian brain that are activated during the generation of the song. It has recently been found that in the vocal muscles of a sleeping bird, it is possible to detect activity patterns during these silent replays. In this work, we employ a dynamical systems model for song production in suboscine birds in order to translate the vocal muscles activity during sleep into synthetic songs. Besides allowing us to translate muscle activity into behavior, we argue that this approach poses the biomechanics as a unique window into the avian brain, with biophysical models as its probe.

Vocal repertoire of Microhyla nilphamariensis from Delhi and comparison with closely related M. ornata populations from the western coast of India and Sri Lanka.

Advertisement calls in frogs have evolved to be species-specific signals of recognition and are therefore considered an essential component of integrative taxonomic approaches to identify species and delineate their distribution range. The species rich genus Microhyla is a particularly challenging group for species identification, discovery and conservation management due to the small size, conserved morphology and wide distribution of its members, necessitating the need for a thorough description of their vocalization. In this study, we provide quantitative description of the vocal behaviour of Microhyla nilphamariensis, a widely distributed south Asian species, from Delhi, India, based on call recordings of 18 individuals and assessment of 21 call properties. Based on the properties measured acrossed 360 calls, we find that a typical advertisement call of M. nilphamariensis lasts for 393.5 ±  57.5 ms, has 17 pulses on average and produce pulses at rate of 39 pulses/s. The overall call dominant frequency was found to be 2.8 KHz and the call spectrum consisted of two dominant frequency peaks centered at 1.6 KHz and 3.6 KHz, ranging between 1.5-4.1 KHz. Apart from its typical advertisement call, our study also reveals the presence of three 'rare' call types, previously unreported in this species. We describe variability in call properties and discuss their relation to body size and temperature. We found that overall dominant frequency 1 (spectral property) was found to be correlated with body size, while first pulse period (temporal property) was found to be correlated with temperature. Further, we compare the vocal repertoire of M. nilphamariensis with that of the congener Microhyla ornata from the western coast of India and Sri Lanka and also compare the call properties of these two populations of M. ornata to investigate intra-specific call variation. We find statistically significant differentiation in their acoustic repertoire in both cases. Based on 18 call properties (out of 20), individuals of each locality clearly segregate on PCA factor plane forming separate groups. Discriminant function analysis (DFA) using PCA factors shows 100% classification success with individuals of each locality getting classified to a discrete group. This confirms significant acoustic differentiation between these species as well as between geographically distant conspecifics. The data generated in this study will be useful for comparative bioacoustic analysis of Microhyla species and can be utilized to monitor populations and devise conservation management plan for threatened species in this group.

The Mouse Inferior Colliculus Responds Preferentially to Non-Ultrasonic Vocalizations.

The inferior colliculus (IC), the midbrain auditory integration center, analyzes information about social vocalizations and provides substrates for higher level processing of vocal signals. We used multichannel recordings to characterize and localize responses to social vocalizations and synthetic stimuli within the IC of female and male mice, both urethane anesthetized and unanesthetized. We compared responses to ultrasonic vocalizations (USVs) with other vocalizations in the mouse repertoire and related vocal responses to frequency tuning, IC subdivisions, and sex. Responses to lower frequency, broadband social vocalizations were widespread in IC, well represented throughout the tonotopic axis, across subdivisions, and in both sexes. Responses to USVs were much more limited. Although we observed some differences in tonal and vocal responses by sex and subdivision, representations of vocal responses by sex and subdivision were largely the same. For most units, responses to vocal signals occurred only when frequency response areas overlapped with spectra of the vocal signals. Since tuning to frequencies contained within the highest frequency USVs is limited (<15% of IC units), responses to these vocalizations are correspondingly limited (<5% of sound-responsive units). These results highlight a paradox of USV processing in some rodents: although USVs are the most abundant social vocalization, their representation and the representation of corresponding frequencies are less than lower frequency social vocalizations. We interpret this paradox in light of observations suggesting that USVs with lower frequency elements (<50 kHz) are associated with increased emotional intensity and engage a larger population of neurons in the mouse auditory system.

Register transitions in an in vivo canine model as a function of intrinsic laryngeal muscle stimulation, fundamental frequency, and sound pressure level.

Phonatory instabilities and involuntary register transitions can occur during singing. However, little is known regarding the mechanisms which govern such transitions. To investigate this phenomenon, we systematically varied laryngeal muscle activation and airflow in an in vivo canine larynx model during phonation. We calculated voice range profiles showing average nerve activations for all combinations of fundamental frequency (F0) and sound pressure level (SPL). Further, we determined closed-quotient (CQ) and minimum-posterior-area (MPA) based on high-speed video recordings. While different combinations of muscle activation favored different combinations of F0 and SPL, in the investigated larynx there was a consistent region of instability at about 400 Hz which essentially precluded phonation. An explanation for this region may be a larynx specific coupling between sound source and subglottal tract or an effect based purely on larynx morphology. Register transitions crossed this region, with different combinations of cricothyroid and thyroarytenoid muscle (TA) activation stabilizing higher or lower neighboring frequencies. Observed patterns in CQ and MPA dependent on TA activation reproduced patterns found in singers in previous work. Lack of control of TA stimulation may result in phonation instabilities, and enhanced control of TA stimulation may help to avoid involuntary register transitions, especially in the singing voice.

Observational study on the non-linear response of dolphins to the presence of vessels.

With the large increase in human marine activity, our seas have become populated with vessels that can be overheard from distances of even 20 km. Prior investigations showed that such a dense presence of vessels impacts the behaviour of marine animals, and in particular dolphins. While previous explorations were based on a linear observation for changes in the features of dolphin whistles, in this work we examine non-linear responses of bottlenose dolphins (Tursiops Truncatus) to the presence of vessels. We explored the response of dolphins to vessels by continuously recording acoustic data using two long-term acoustic recorders deployed near a shipping lane and a dolphin habitat in Eilat, Israel. Using deep learning methods we detected a large number of 50,000 whistles, which were clustered to associate whistle traces and to characterize their features to discriminate vocalizations of dolphins: both structure and quantities. Using a non-linear classifier, the whistles were categorized into two classes representing the presence or absence of a nearby vessel. Although our database does not show linear observable change in the features of the whistles, we obtained true positive and true negative rates exceeding 90% accuracy on separate, left-out test sets. We argue that this success in classification serves as a statistical proof for a non-linear response of dolphins to the presence of vessels.

Call combination in African forest elephants Loxodonta cyclotis.

Syntax, the combination of meaning-devoid phonemes into meaningful words, which in turn are combined in structurally and semantically complex sentences, is fundamental to the unlimited expressiveness of human languages. Studying the functions of call combinations in non-human species provides insights into the evolution of such syntactic capabilities. Here, we investigated the combination of high amplitude broadband calls with low frequency rumble vocalizations in a highly social species, the African forest elephant Loxodonta cyclotis. Rumbles play an integral role in coordinating social interactions by transmitting socially relevant information, including individual identity. By contrast, broadband calls, such as roars, are thought to function as signals of distress and urgency as they are typically produced in situations of high emotional intensity. Functional changes associated with the combination of these calls remain little understood. We found that call combinations were produced by all age-sex classes but were most prevalent in immature individuals. We found that rumbles used singularly occurred in all five investigated social contexts, whereas single broadband calls were restricted to two resource-related contexts. Call combinations also occurred in all five contexts, suggesting an increase in the functional use of broadband calls when combined with rumbles, analogous to the generativity brought about through syntax in human speech. Moreover, combining calls appeared to lead to functional shifts towards high-stake contexts. Call combinations were more likely in competition contexts compared to single rumbles, and more likely in separation contexts compared to single broadband calls. We suggest that call combination in forest elephants may aide to reduce message ambiguity in high-stake situation by simultaneously communicating distress and individual identity, which may be critical to secure access to resources, reduce the risk of injury and to reunite with or recruit the support of the family group.

Importance of the receiver's height for transmission studies in acoustic ecology.

In animal communication, the sound pressure level (SPL) of the acoustic signals has been studied in relation to various biological functions. Previous research reported that senders and receivers benefit from being at elevated positions. However, sometimes, researchers find contradictory results. Using a transmission experiment, we measured SPL of two acoustic stimuli: (i) white noise, and (ii) advertisement calls of the Iberian tree frog (Hyla molleri) at two different heights above ground level (0.05 and 0.75 m) and from six distances (1, 2, 4, 8, 16, and 32 m) from a loudspeaker. Calls of the Iberian tree frog have two spectral peaks centred at the frequencies of ca. 1 and 2 kHz. As expected, SPL decreased with distance, but following a distinct attenuation pattern across height above the ground and frequency. Our findings show that the ground effect may critically alter frequency attenuation and, therefore, signal composition and discrimination at the listener's location, even at low heights above the ground. We suggest that recording devices should be positioned at the same height that natural listeners are usually located in nature, to facilitate the replication and comparison of experiments in the field of acoustic ecology and, also, bioacoustics.

A new species of the Scinax cruentomma group (Anura: Hylidae) from the Ucayali River basin of Loreto, Peru.

We describe a new species of the Scinax cruentomma species group, with a red streak in the iris and a weakly bilobate vocal sac. It is known from oligotrophic soils in the sedimentary basin of the Ucayali River near Jenaro Herrera (province of Requena, Peru) and Ro Blanco (buffer zone of the Matses Indigenous territory and reserve). The new species can be distinguished from the other species of the S. cruentomma group by its small snout-vent length, body and iris color patterns, weakly bilobate vocal sac, myological characters, and the number of notes and pulses of the advertisement call. It is morphologically most similar to S. strussmannae, from which the advertisement call, nostril, canthus rostralis, and loreal region can distinguish it.

Behavioural plasticity compensates for adaptive loss of cricket song.

Behavioural flexibility might help animals cope with costs of genetic variants under selection, promoting genetic adaptation. However, it has proven challenging to experimentally link behavioural flexibility to the predicted compensation of population-level fitness. We tested this prediction using the field cricket Teleogryllus oceanicus. In Hawaiian populations, a mutation silences males and protects against eavesdropping parasitoids. To examine how the loss of this critical acoustic communication signal impacts offspring production and mate location, we developed a high-resolution, individual-based tracking system for low-light, naturalistic conditions. Offspring production did not differ significantly in replicate silent versus singing populations, and fitness compensation in silent conditions was associated with significantly increased locomotion in both sexes. Our results provide evidence that flexible behaviour can promote genetic adaptation via compensation in reproductive output and suggest that rapid evolution of animal communication systems may be less constrained than previously appreciated.

Acute Aromatase Inhibition Impairs Neural and Behavioral Auditory Scene Analysis in Zebra Finches.

Auditory perception can be significantly disrupted by noise. To discriminate sounds from noise, auditory scene analysis (ASA) extracts the functionally relevant sounds from acoustic input. The zebra finch communicates in noisy environments. Neurons in their secondary auditory pallial cortex (caudomedial nidopallium, NCM) can encode song from background chorus, or scenes, and this capacity may aid behavioral ASA. Furthermore, song processing is modulated by the rapid synthesis of neuroestrogens when hearing conspecific song. To examine whether neuroestrogens support neural and behavioral ASA in both sexes, we retrodialyzed fadrozole (aromatase inhibitor, FAD) and recorded in vivo awake extracellular NCM responses to songs and scenes. We found that FAD affected neural encoding of songs by decreasing responsiveness and timing reliability in inhibitory (narrow-spiking), but not in excitatory (broad-spiking) neurons. Congruently, FAD decreased neural encoding of songs in scenes for both cell types, particularly in females. Behaviorally, we trained birds using operant conditioning and tested their ability to detect songs in scenes after administering FAD orally or injected bilaterally into NCM. Oral FAD increased response bias and decreased correct rejections in females, but not in males. FAD in NCM did not affect performance. Thus, FAD in the NCM impaired neuronal ASA but that did not lead to behavioral disruption suggesting the existence of resilience or compensatory responses. Moreover, impaired performance after systemic FAD suggests involvement of other aromatase-rich networks outside the auditory pathway in ASA. This work highlights how transient estrogen synthesis disruption can modulate higher-order processing in an animal model of vocal communication.

Isochronous rhythms: Facilitating song coordination across taxa?

The biological expression of isochronous rhythms - rhythms like those produced by a metronome - was once thought to be unique to humans. A new study reports that faster and more isochronous rhythms lead to more successful duets in singing gibbons: isochronous rhythms might be an important component of song coordination across taxa.

Application of a seismic network to baleen whale call detection and localization in the Panama basin-a Bryde's whale example.

Baleen whales use sounds of various characteristics for different tasks and interactions. This study focuses on recordings from the Costa Rica Rift, in the Eastern Tropical Pacific Ocean, made by 25 ocean-bottom seismographs and a vertical array of 12 hydrophones between January and February 2015. The whale calls observed are of two kinds: more commonly, repetitive 4-5 s-long signals separated into two frequency bands centered at ∼20 and ∼36 Hz; less commonly, a series of ∼0.5 to 1.0 s-long, lower amplitude signals with frequencies between 80 and 160 Hz. These characteristics are similar to calls attributed to Bryde's whales which are occasionally sighted in this region. In this study, the repetitive calls are detected using both the short-term average/long-term average approach and a network empirical subspace detector. In total, 188 and 1891 calls are obtained for each method, demonstrating the value of the subspace detector for highly similar signals. These signals are first localized using a non-linear grid search algorithm and then further relocalized using the double-difference technique. The high-resolution localizations reveal the presence of at least seven whales during the recording period, often crossing the instrument network from southwest to northeast.

Development of a machine learning detector for North Atlantic humpback whale song.

The study of humpback whale song using passive acoustic monitoring devices requires bioacousticians to manually review hours of audio recordings to annotate the signals. To vastly reduce the time of manual annotation through automation, a machine learning model was developed. Convolutional neural networks have made major advances in the previous decade, leading to a wide range of applications, including the detection of frequency modulated vocalizations by cetaceans. A large dataset of over 60 000 audio segments of 4 s length is collected from the North Atlantic and used to fine-tune an existing model for humpback whale song detection in the North Pacific (see Allen, Harvey, Harrell, Jansen, Merkens, Wall, Cattiau, and Oleson (2021). Front. Mar. Sci. 8, 607321). Furthermore, different data augmentation techniques (time-shift, noise augmentation, and masking) are used to artificially increase the variability within the training set. Retraining and augmentation yield F-score values of 0.88 on context window basis and 0.89 on hourly basis with false positive rates of 0.05 on context window basis and 0.01 on hourly basis. If necessary, usage and retraining of the existing model is made convenient by a framework (AcoDet, acoustic detector) built during this project. Combining the tools provided by this framework could save researchers hours of manual annotation time and, thus, accelerate their research.

Male and female red-cheeked cordon bleus sing similar yet individualistic songs.

Birdsong is an excellent system for studying complex vocal signaling in both males and females. Historically, most research in captivity has focused only on male song. This has left a gap in our understanding of the environmental, neuroendocrine, and mechanistic control of female song. Here, we report the overall acoustic features, repertoire, and stereotypy of both male and female Red-Cheeked Cordon Bleus (Uraeginthus bengalus) (RCCBs) songs in the lab. We found few sex differences in the acoustic structure, song repertoire, and song stereotypy of RCCBs. Both sexes had similar song entropy, peak frequency, and duration. Additionally, individuals of both sexes sang only a single song type each and had similar levels of song and syllable stereotypy. However, we did find that female RCCBs had higher song bandwidth but lower syllable repertoires. Finally, and most strikingly, we found highly individualistic songs in RCCBs. Each individual produced a stereotyped and unique song with no birds sharing song types and very few syllable types being shared between birds of either sex. We propose that RCCBs represent a promising species for future investigations of the acoustic sex differences in song in a lab environment, and also for understanding the evolutionary driving forces behind individualistic songs.

Hemispheric dominance in HVC is experience-dependent in juvenile male zebra finches.

Juvenile male zebra finches (Taeniopygia guttata) must be exposed to an adult tutor during a sensitive period to develop normal adult song. The pre-motor nucleus HVC (acronym used as a proper name), plays a critical role in song learning and production (cf. Broca's area in humans). In the human brain, left-side hemispheric dominance in some language regions is positively correlated with proficiency in linguistic skills. However, it is unclear whether this pattern depends upon language learning, develops with normal maturation of the brain, or is the result of pre-existing functional asymmetries. In juvenile zebra finches, even though both left and right HVC contribute to song production, baseline molecular activity in HVC is left-dominant. To test if HVC exhibits hemispheric dominance prior to song learning, we raised juvenile males in isolation from adult song and measured neuronal activity in the left and right HVC upon first exposure to an auditory stimulus. Activity in the HVC was measured using the immediate early gene (IEG) zenk (acronym for zif-268, egr-1, NGFI-a, and krox-24) as a marker for neuronal activity. We found that neuronal activity in the HVC of juvenile male zebra finches is not lateralized when raised in the absence of adult song, while normally-reared juvenile birds are left-dominant. These findings show that there is no pre-existing asymmetry in the HVC prior to song exposure, suggesting that lateralization of the song system depends on learning through early exposure to adult song and subsequent song-imitation practice.

Breathing control of vocalization.

A crucial brainstem circuit for vocal-respiratory coordination of the larynx is revealed.