Estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal pattern generator

Estrogens rapidly regulate neuronal activity within seconds-to-minutes, yet it is unclear how estrogens interact with neural circuits to rapidly coordinate behavior. This study examines whether 17-beta-estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal control circuit. Adult plainfin midshipman fish emit vocalizations that mainly differ in duration, and rhythmic activity of a hindbrain–spinal vocal pattern generator (VPG) directly establishes the temporal features of midshipman vocalizations. VPG activity is therefore predictive of natural calls, and ‘fictive calls’ can be elicited by electrical microstimulation of the VPG. Prior studies show that intramuscular estradiol injection rapidly (within 5 min) increases fictive call duration in midshipman. Here, we delivered opioid antagonists near the VPG prior to estradiol injection. Rapid estradiol actions on fictive calling were completely suppressed by the broad-spectrum opioid antagonist naloxone and the mu-opioid antagonist beta-funaltrexamine, but were unaffected by the kappa-opioid antagonist nor-binaltorphimine. Unexpectedly, prior to estradiol administration, all three opioid antagonists caused immediate, transient reductions in fictive call duration. Together, our results indicate that: (1) vocal activity is modulated by opioidergic networks, confirming hypotheses from birds and mammals, and (2) the rapid actions of estradiol on vocal patterning depend on interactions with a mu-opioid modulatory network.     

Is the Capacity for Vocal Learning in Vertebrates Rooted in Fish Schooling Behavior?

The capacity to learn and reproduce vocal sounds has evolved in phylogenetically distant tetrapod lineages. Vocal learners in all these lineages express similar neural circuitry and genetic factors when perceiving, processing, and reproducing vocalization, suggesting that brain pathways for vocal learning evolved within strong constraints from a common ancestor, potentially fish. We hypothesize that the auditory-motor circuits and genes involved in entrainment have their origins in fish schooling behavior and respiratory-motor coupling. In this acoustic advantages hypothesis, aural costs and benefits played a key role in shaping a wide variety of traits, which could readily be exapted for entrainment and vocal learning, including social grouping, group movement, and respiratory-motor coupling. Specifically, incidental sounds of locomotion and respiration (ISLR) may have reinforced synchronization by communicating important spatial and temporal information between school-members and extending windows of silence to improve situational awareness. This process would be mutually reinforcing. Neurons in the telencephalon, which were initially involved in linking ISLR with forelimbs, could have switched functions to serve vocal machinery (e.g. mouth, beak, tongue, larynx, syrinx). While previous vocal learning hypotheses invoke transmission of neurons from visual tasks (gestures) to the auditory channel, this hypothesis involves the auditory channel from the onset. Acoustic benefits of locomotor-respiratory coordination in fish may have selected for genetic factors and brain circuitry capable of synchronizing respiratory and limb movements, predisposing tetrapod lines to synchronized movement, vocalization, and vocal learning. We discuss how the capacity to entrain is manifest in fish, amphibians, birds, and mammals, and propose predictions to test our acoustic advantages hypothesis.     

Rapid elevations in both steroid hormones and vocal signaling during playback challenge: a field experiment in Gulf toadfish

It is well known that plasma androgens are rapidly released in response to aggressive or sexual stimuli in a broad array of vertebrates. However, experimental work on behavioral functions of rapid androgen elevation is rare. A combination of field-based behavioral experiments and lab-based neuroendocrinological approaches is beginning to show how steroid hormones rapidly regulate the expression of vocal communication signals in Gulf toadfish (Opsanus beta). Male toadfish emit multiharmonic "boatwhistles" and shorter-duration, broadband "grunts" during intraspecific communication. Neurophysiology experiments demonstrate that androgens and glucocorticoids rapidly modify vocal motor patterning in male toadfish. In this study, we simulated territorial intrusions (vocal "challenges") with acoustic playbacks to toadfish in the field, and observed simultaneous, rapid (within 5-20 min) changes in vocalizations and steroid hormones. Both plasma androgens and vocal activity increased following the presentation of pure tones that mimic the duration of natural boatwhistles (275 ms), while they remained unchanged following playbacks of tone stimuli that mimic the duration of grunts (75 ms) or the upper-range of boatwhistles (475 ms). Circulating glucocorticoids were elevated in calling vs. non-calling males but were unaffected by playback stimuli, suggesting a role in the energetics of vocalization. These results strongly suggest that one function of rapid androgen elevation in response to social challenge is to mediate similarly rapid changes in territorial vocal signaling. Given the conserved organization of neuroendocrine and vocal motor systems, rapid steroid action on vocalization mechanisms may be true of other vocal vertebrates as well, including birds and mammals.     

The role of auditory feedback in vocal learning and maintenance

Auditory experience is critical for the acquisition and maintenance of learned vocalizations in both humans and songbirds. Despite the central role of auditory feedback in vocal learning and maintenance, where and how auditory feedback affects neural circuits important to vocal control remain poorly understood. Recent studies of singing birds have uncovered neural mechanisms by which feedback perturbations affect vocal plasticity and also have identified feedback-sensitive neurons at or near sites of auditory and vocal motor interaction. Additionally, recent studies in marmosets have underscored that even in the absence of vocal learning, vocalization remains flexible in the face of changing acoustical environments, pointing to rapid interactions between auditory and vocal motor systems. Finally, recent studies show that a juvenile songbird's initial auditory experience of a song model has long-lasting effects on sensorimotor neurons important to vocalization, shedding light on how auditory memories and feedback interact to guide vocal learning.     

Songbird: a unique animal model for studying the molecular basis of disorders of vocal development and communication

Like humans, songbirds are one of the few animal groups that learn vocalization. Vocal learning requires coordination of auditory input and vocal output using auditory feedback to guide one’s own vocalizations during a specific developmental stage known as the critical period. Songbirds are good animal models for understand the neural basis of vocal learning, a complex form of imitation, because they have many parallels to humans with regard to the features of vocal behavior and neural circuits dedicated to vocal learning. In this review, we will summarize the behavioral, neural, and genetic traits of birdsong. We will also discuss how studies of birdsong can help us understand how the development of neural circuits for vocal learning and production is driven by sensory input (auditory information) and motor output (vocalization).     

Audio–vocal interactions during vocal communication in squirrel monkeys and their neurobiological implications

Several strategies have evolved in the vertebrate lineage to facilitate signal transmission in vocal communication. Here, I present a mechanism to facilitate signal transmission in a group of communicating common squirrel monkeys (Saimiri sciureus sciureus). Vocal onsets of a conspecific affect call initiation in all other members of the group in less than 100 ms. The probability of vocal onsets in a range of 100 ms after the beginning of a vocalization of another monkey was significantly decreased compared to the mean probability of call onsets. Additionally, the probability for vocal onsets of conspecifics was significantly increased just a few hundreds of milliseconds after call onset of others. These behavioral data suggest neural mechanisms that suppress vocal output just after the onset of environmental noise, such as vocalizations of conspecifics, and increase the probability of call initiation of group mates shortly after. These findings add new audio–vocal behaviors to the known strategies that modulate signal transmission in vocal communication. The present study will guide future neurobiological studies that explore how the observed audio–vocal behaviors are implemented in the monkey brain.     

Development of social vocalizations in mice

Adult mice are highly vocal animals, with both males and females vocalizing in same sex and cross sex social encounters. Mouse pups are also highly vocal, producing isolation vocalizations when they are cold or removed from the nest. This study examined patterns in the development of pup isolation vocalizations, and compared these to adult vocalizations. In three litters of CBA/CaJ mice, we recorded isolation vocalizations at ages postnatal day 5 (p5), p7, p9, p11, and p13. Adult vocalizations were obtained in a variety of social situations. Altogether, 28,384 discrete vocal signals were recorded using high-frequency-sensitive equipment and analyzed for syllable type, spectral and temporal features, and the temporal sequencing within bouts. We found that pups produced all but one of the 11 syllable types recorded from adults. The proportions of syllable types changed developmentally, but even the youngest pups produced complex syllables with frequency-time variations. When all syllable types were pooled together for analysis, changes in the peak frequency or the duration of syllables were small, although significant, from p5 through p13. However, individual syllable types showed different, large patterns of change over development, requiring analysis of each syllable type separately. Most adult syllables were substantially lower in frequency and shorter in duration. As pups aged, the complexity of vocal bouts increased, with a greater tendency to switch between syllable types. Vocal bouts from older animals, p13 and adult, had significantly more sequential structure than those from younger mice. Overall, these results demonstrate substantial changes in social vocalizations with age. Future studies are required to identify whether these changes result from developmental processes affecting the vocal tract or control of vocalization, or from vocal learning. To provide a tool for further research, we developed a MATLAB program that generates bouts of vocalizations that correspond to mice of different ages.     

Phase-Specific Vocalizations of Male Mice at the Initial Encounter during the Courtship Sequence

Mice produce ultrasonic vocalizations featuring a variety of syllables. Vocalizations are observed during social interactions. In particular, males produce numerous syllables during courtship. Previous studies have shown that vocalizations change according to sexual behavior, suggesting that males vary their vocalizations depending on the phase of the courtship sequence. To examine this process, we recorded large sets of mouse vocalizations during male–female interactions and acoustically categorized these sounds into 12 vocal types. We found that males emitted predominantly short syllables during the first minute of interaction, more long syllables in the later phases, and mainly harmonic sounds during mounting. These context- and time-dependent changes in vocalization indicate that vocal communication during courtship in mice consists of at least three stages and imply that each vocalization type has a specific role in a phase of the courtship sequence. Our findings suggest that recording for a sufficiently long time and taking the phase of courtship into consideration could provide more insights into the role of vocalization in mouse courtship behavior in future study.     

Defects in Ultrasonic Vocalization of Cadherin-6 Knockout Mice

Background

Although some molecules have been identified as responsible for human language disorders, there is still little information about what molecular mechanisms establish the faculty of human language. Since mice, like songbirds, produce complex ultrasonic vocalizations for intraspecific communication in several social contexts, they can be good mammalian models for studying the molecular basis of human language. Having found that cadherins are involved in the vocal development of the Bengalese finch, a songbird, we expected cadherins to also be involved in mouse vocalizations.

Methodology/Principal Findings

To examine whether similar molecular mechanisms underlie the vocalizations of songbirds and mammals, we categorized behavioral deficits including vocalization in cadherin-6 knockout mice. Comparing the ultrasonic vocalizations of cadherin-6 knockout mice with those of wild-type controls, we found that the peak frequency and variations of syllables were differed between the mutant and wild–type mice in both pup-isolation and adult-courtship contexts. Vocalizations during male-male aggression behavior, in contrast, did not differ between mutant and wild–type mice. Open-field tests revealed differences in locomotors activity in both heterozygote and homozygote animals and no difference in anxiety behavior.

Conclusions/Significance

Our results suggest that cadherin-6 plays essential roles in locomotor activity and ultrasonic vocalization. These findings also support the idea that different species share some of the molecular mechanisms underlying vocal behavior.     

Neural mechanisms of vocal production in songbirds.

Recent reports have described peripheral and central mechanisms of vocal production in songbirds. Respiratory patterning, individual syringeal muscles and the two syringeal halves have been shown to make specific contributions to learned vocalizations. New information on the function and organization of central pathways suggests how these production mechanisms may be controlled. The results are opening new avenues for further work on how acquired motor patterns are represented in this system.     

The Lombard effect and other noise‐induced vocal modifications: insight from mammalian communication systems

Humans and non‐human mammals exhibit fundamentally similar vocal responses to increased noise, including increases in vocalization amplitude (the Lombard effect) and changes to spectral and temporal properties of vocalizations. Different research focuses have resulted in significant discrepancies in study methodologies and hypotheses among fields, leading to particular knowledge gaps and techniques specific to each field. This review compares and contrasts noise‐induced vocal modifications observed from human and non‐human mammals with reference to experimental design and the history of each field. Topics include the effects of communication motivation and subject‐specific characteristics on the acoustic parameters of vocalizations, examination of evidence for a proposed biomechanical linkage between the Lombard effect and other spectral and temporal modifications, and effects of noise on self‐communication signals (echolocation). Standardized terminology, cross‐taxa tests of hypotheses, and open areas for future research in each field are recommended. Findings indicate that more research is needed to evaluate linkages among vocal modifications, context dependencies, and the finer details of the Lombard effect during natural communication. Studies of non‐human mammals could benefit from applying the tightly controlled experimental designs developed in human research, while studies of human speech in noise should be expanded to include natural communicative contexts. The effects of experimental design and behavioural context on vocalizations should not be neglected as they may impact the magnitude and type of noise‐induced vocal modifications.     

Echolocation calls and communication calls are controlled differentially in the brainstem of the bat Phyllostomus discolor

Background  

Echolocating bats emit vocalizations that can be classified either as echolocation calls or communication calls. Neural control of both types of calls must govern the same pool of motoneurons responsible for vocalizations. Electrical microstimulation in the periaqueductal gray matter (PAG) elicits both communication and echolocation calls, whereas stimulation of the paralemniscal area (PLA) induces only echolocation calls. In both the PAG and the PLA, the current thresholds for triggering natural vocalizations do not habituate to stimuli and remain low even for long stimulation periods, indicating that these structures have relative direct access to the final common pathway for vocalization. This study intended to clarify whether echolocation calls and communication calls are controlled differentially below the level of the PAG via separate vocal pathways before converging on the motoneurons used in vocalization.     

Vocal Production by a Language-Competent Pan paniscus

Human spoken language and nonhuman primate vocalization systems have traditionally been regarded as qualitatively different from one another with respect to their semanticity and the way in which individuals acquire and utilize these signals. However, recent studies of the vocal behaviors of both captive and free-ranging monkeys and apes suggest that this dichotomy may not be unequivocal. We examined the vocalizations produced by a linguistically-competent adult male bonobo (Pan paniscus) named Kanzi. We analyzed his vocalizations during communicative interactions with humans in order to determine whether they vary systematically according to the semantic context in which they are produced. We determined semantic contexts based upon a vocalization's co-occurrence with predefined behavioral correlates. Spectrographic and statistical analyses revealed that acoustic structure is similar among the vocalizations that occurred within a specific semantic context and structural differences are evident between the vocalizations produced in different contexts. The results provide evidence that, during communicative interactions with humans, Kanzi modulates his vocal output on both the temporal and spectral levels.     

Coos,booms, and hoots: The evolution of closed‐mouth vocal behavior in birds

Most birds vocalize with an open beak, but vocalization with a closed beak into an inflating cavity occurs in territorial or courtship displays in disparate species throughout birds. Closed‐mouth vocalizations generate resonance conditions that favor low‐frequency sounds. By contrast, open‐mouth vocalizations cover a wider frequency range. Here we describe closed‐mouth vocalizations of birds from functional and morphological perspectives and assess the distribution of closed‐mouth vocalizations in birds and related outgroups. Ancestral‐state optimizations of body size and vocal behavior indicate that closed‐mouth vocalizations are unlikely to be ancestral in birds and have evolved independently at least 16 times within Aves, predominantly in large‐bodied lineages. Closed‐mouth vocalizations are rare in the small‐bodied passerines. In light of these results and body size trends in nonavian dinosaurs, we suggest that the capacity for closed‐mouth vocalization was present in at least some extinct nonavian dinosaurs. As in birds, this behavior may have been limited to sexually selected vocal displays, and hence would have co‐occurred with open‐mouthed vocalizations.     

Temporal pattern of vocalization type usage in singing sessions of male tyrant flycatchers (Tyranninae)

It has been hypothesized that variation (e.g., of repertoire elements) in prolonged vocalization sessions of passerine birds can serve to minimize habituation by conspecifics. The repertoire of vocalization types limited in suboscine passerines, raising the question of how a limited set of elements can create patterns that minimize habituation. This question was studied by computational analysis of recorded singing sessions of 20 suboscine species from the subfamily Tyranninae, family Tyrannidae (tyrant flycatchers). The recordings of 12 of the species included two or more distinct vocalization types (VTs). In these species, the interval between vocalization units when the VT changed was on average shorter than that when the VT remained the same. In addition, when the VT changed, the mean interval length between successive vocalization units differed depending on which VT preceded the interval and which VT followed it. On the other hand, species with just a single VT in the session analyzed showed a surprisingly high degree of absolute difference between adjacent vocalization units with respect to both the length of the vocalization and percentage of time elapsed until peak amplitude. A change in the rhythm of vocalization accompanying a change in VT provided a potential means of drawing a conspecific listener's attention to the change in VT. The results showed that tyrant flycatchers use temporal patterning to achieve a high level of variety in vocalization sessions despite a limited vocal repertoire.     

Social vocalizations can release oxytocin in humans

Vocalizations are important components of social behaviour in many vertebrate species, including our own. Less well-understood are the hormonal mechanisms involved in response to vocal cues, and how these systems may influence the course of behavioural evolution. The neurohormone oxytocin (OT) partly governs a number of biological and social processes critical to fitness, such as attachment between mothers and their young, and suppression of the stress response after contact with trusted conspecfics. Rodent studies suggest that OT''s release is contingent upon direct tactile contact with such individuals, but we hypothesized that vocalizations might be capable of producing the same effect. To test our hypothesis, we chose human mother–daughter dyads and applied a social stressor to the children, following which we randomly assigned participants into complete contact, speech-only or no-contact conditions. Children receiving a full complement of comfort including physical, vocal and non-verbal contact showed the highest levels of OT and the swiftest return to baseline of a biological marker of stress (salivary cortisol), but a strikingly similar hormonal profile emerged in children comforted solely by their mother''s voice. Our results suggest that vocalizations may be as important as touch to the neuroendocrine regulation of social bonding in our species.     

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

Spectral call features provide information about the aggression level of greater mouse-eared bats (Myotis myotis) during agonistic interactions

Bats rely heavily on acoustic signals in order to communicate with each other in a variety of social contexts. Among those, agonistic interactions and accompanying vocalizations have received comparatively little study. Here, we studied the communicational behaviour between male greater mouse-eared bats (Myotis myotis) during agonistic encounters. Two randomly paired adult males were placed in a box that allowed us to record video and sound synchronously. We describe their vocal repertoire and compare the acoustic structure of vocalizations between two aggression levels, which we quantified via the bats’ behaviour. By inspecting thirty, one-minute long encounters, we identified a rich variety of social calls that can be described as two basic call types: echolocation-like, low-frequency sweeps and long, broadband squawks. Squawks, the most common vocalization, were often noisy, i.e. exhibited a chaotic spectral structure. We further provide evidence for individual signatures and the presence of nonlinear phenomena in this species’ vocal repertoire. As the usage and acoustic structure of vocalizations is known to encode the internal state of the caller, we had predicted that the spectral structure of squawks would be affected by the caller’s aggression level. Confirming our hypothesis, we found that increased aggression positively correlated with an increase in call frequency and tonality. We hypothesize that the extreme spectral variability between and within squawks can be explained by small fluctuations in vocal control parameters (e.g. subglottal pressure) that are caused by the elevated arousal, which is in turn influenced by the aggression level.