Birdsong: From behaviour to brain

Although vocal communication is wide-spread in animal kingdom, the use of learned (in contrast to innate) vocalization is very rare. We can find it only in few animal taxa: human, bats, whales and dolphins, elephants, parrots, hummingbirds, and songbirds. There are several parallels between human and songbird perception and production of vocal signals. Hence, many studies take interest in songbird singing for investigating the neural bases of learning and memory. Brain circuits controlling song learning and maintenance consist of two pathways — a vocal motor pathway responsible for production of learned vocalizations and anterior forebrain pathway responsible for learning and modifying the vocalizations. This review provides an overview of the song organization, its behavioural traits, and neural regulations. The recently expanding area of molecular mapping of the behaviour-driven gene expression in brain represents one of the modern approaches to the study the function of vocal and auditory areas for song learning and maintenance in birds.     

He hears,she hears: Are there sex differences in auditory processing?

Songbirds learn individually unique songs through vocal imitation and use them in courtship and territorial displays. Previous work has identified a forebrain auditory area, the caudomedial nidopallium (NCM), that appears specialized for discriminating and remembering conspecific vocalizations. In zebra finches (ZFs), only males produce learned vocalizations, but both sexes process these and other signals. This study assessed sex differences in auditory processing by recording extracellular multiunit activity at multiple sites within NCM. Juvenile female ZFs (n = 46) were reared in individual isolation and artificially tutored with song. In adulthood, songs were played back to assess auditory responses, stimulus‐specific adaptation, neural bias for conspecific song, and memory for the tutor's song, as well as recently heard songs. In a subset of females (n = 36), estradiol (E2) levels were manipulated to test the contribution of E2, known to be synthesized in the brain, to auditory responses. Untreated females (n = 10) showed significant differences in response magnitude and stimulus‐specific adaptation compared to males reared in the same paradigm (n = 9). In hormone‐manipulated females, E2 augmentation facilitated the memory for recently heard songs in adulthood, but neither E2 augmentation (n = 15) nor E2 synthesis blockade (n = 9) affected tutor song memory or the neural bias for conspecific song. The results demonstrate subtle sex differences in processing communication signals, and show that E2 levels in female songbirds can affect the memory for songs of potential suitors, thus contributing to the process of mate selection. The results also have potential relevance to clinical interventions that manipulate E2 in human patients. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 75: 302–314, 2015     

Subharmonics increase the auditory impact of female koala rejection calls

Although non‐linear phenomena are common in human and non‐human animal vocalisations, their functional relevance remains poorly understood. One theory posits that non‐linear phenomena generate unpredictability in vocalisations, which increases the auditory impact of vocal signals, and makes animals less likely to habituate to call repetition. Female koalas (Phascolarctos cinereus) produce vocal signals when they reject male copulation attempts that contain relatively high levels of non‐linear phenomena, and thus may function as attention grabbing vocal signals during the breeding season. To test this hypothesis, we used playback experiments: firstly, to determine whether female rejection calls induce heightened behavioural responses in free‐ranging male koalas during the breeding season, and secondly, to examine how the relative amount of non‐linear phenomena in rejection calls influences male behavioural response. The results show that male koalas look for longer towards speakers broadcasting playback sequences of male bellows followed by a series of female rejection calls than those broadcasting only male bellows. In addition, female rejection call sequences with more subharmonics, higher harmonics‐to‐noise ratios, and less biphonation produced the greatest male looking responses. Our findings support the hypothesis that female koala rejection calls function to grab male attention during the breeding season, and indicate that subharmonics are the main acoustic feature that increases the auditory impact of these vocal signals.     

A Lightweight,Headphones-based System for Manipulating Auditory Feedback in Songbirds

Experimental manipulations of sensory feedback during complex behavior have provided valuable insights into the computations underlying motor control and sensorimotor plasticity¹. Consistent sensory perturbations result in compensatory changes in motor output, reflecting changes in feedforward motor control that reduce the experienced feedback error. By quantifying how different sensory feedback errors affect human behavior, prior studies have explored how visual signals are used to recalibrate arm movements^2,3 and auditory feedback is used to modify speech production^4-7. The strength of this approach rests on the ability to mimic naturalistic errors in behavior, allowing the experimenter to observe how experienced errors in production are used to recalibrate motor output.Songbirds provide an excellent animal model for investigating the neural basis of sensorimotor control and plasticity^8,9. The songbird brain provides a well-defined circuit in which the areas necessary for song learning are spatially separated from those required for song production, and neural recording and lesion studies have made significant advances in understanding how different brain areas contribute to vocal behavior^9-12. However, the lack of a naturalistic error-correction paradigm - in which a known acoustic parameter is perturbed by the experimenter and then corrected by the songbird - has made it difficult to understand the computations underlying vocal learning or how different elements of the neural circuit contribute to the correction of vocal errors¹³.The technique described here gives the experimenter precise control over auditory feedback errors in singing birds, allowing the introduction of arbitrary sensory errors that can be used to drive vocal learning. Online sound-processing equipment is used to introduce a known perturbation to the acoustics of song, and a miniaturized headphones apparatus is used to replace a songbird''s natural auditory feedback with the perturbed signal in real time. We have used this paradigm to perturb the fundamental frequency (pitch) of auditory feedback in adult songbirds, providing the first demonstration that adult birds maintain vocal performance using error correction¹⁴. The present protocol can be used to implement a wide range of sensory feedback perturbations (including but not limited to pitch shifts) to investigate the computational and neurophysiological basis of vocal learning.     

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing,production and learning

Communication between auditory and vocal motor nuclei is essential for vocal learning. In songbirds, the nucleus interfacialis of the nidopallium (NIf) is part of a sensorimotor loop, along with auditory nucleus avalanche (Av) and song system nucleus HVC, that links the auditory and song systems. Most of the auditory information comes through this sensorimotor loop, with the projection from NIf to HVC representing the largest single source of auditory information to the song system. In addition to providing the majority of HVC’s auditory input, NIf is also the primary driver of spontaneous activity and premotor-like bursting during sleep in HVC. Like HVC and RA, two nuclei critical for song learning and production, NIf exhibits behavioral-state dependent auditory responses and strong motor bursts that precede song output. NIf also exhibits extended periods of fast gamma oscillations following vocal production. Based on the converging evidence from studies of physiology and functional connectivity it would be reasonable to expect NIf to play an important role in the learning, maintenance, and production of song. Surprisingly, however, lesions of NIf in adult zebra finches have no effect on song production or maintenance. Only the plastic song produced by juvenile zebra finches during the sensorimotor phase of song learning is affected by NIf lesions. In this review, we carefully examine what is known about NIf at the anatomical, physiological, and behavioral levels. We reexamine conclusions drawn from previous studies in the light of our current understanding of the song system, and establish what can be said with certainty about NIf’s involvement in song learning, maintenance, and production. Finally, we review recent theories of song learning integrating possible roles for NIf within these frameworks and suggest possible parallels between NIf and sensorimotor areas that form part of the neural circuitry for speech processing in humans.     

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.     

Correspondence between evoked vocal responses and auditory thresholds in Pleurodema thaul (Amphibia; Leptodactylidae)

Thresholds for evoked vocal responses and thresholds of multiunit midbrain auditory responses to pure tones and synthetic calls were investigated in males of Pleurodema thaul, as behavioral thresholds well above auditory sensitivity have been reported for other anurans. Thresholds for evoked vocal responses to synthetic advertisement calls played back at increasing intensity averaged 43 dB RMS SPL (range 31–52 dB RMS SPL), measured at the subjects’ position. Number of pulses increased with stimulus intensities, reaching a plateau at about 18–39 dB above threshold and decreased at higher intensities. Latency to call followed inverse trends relative to number of pulses. Neural audiograms yielded an average best threshold in the high frequency range of 46.6 dB RMS SPL (range 41–51 dB RMS SPL) and a center frequency of 1.9 kHz (range 1.7–2.6 kHz). Auditory thresholds for a synthetic call having a carrier frequency of 2.1 kHz averaged 44 dB RMS SPL (range 39–47 dB RMS SPL). The similarity between thresholds for advertisement calling and auditory thresholds for the advertisement call indicates that male P. thaul use the full extent of their auditory sensitivity in acoustic interactions, likely an evolutionary adaptation allowing chorusing activity in low-density aggregations.     

Auditory–vocal mirroring in songbirds

Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory–vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory–vocal mirror neurons in a sensorimotor region of the songbird''s brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory–vocal mirroring in the songbird''s brain.     

A bird's eye view: top down intracellular analyses of auditory selectivity for learned vocalizations

The "song system" refers to a group of interconnected brain nuclei necessary for the utterance of learned song and for the generation of vocal plasticity important to both song learning and adult song maintenance. Although song learning and, in some species, song maintenance depend on auditory feedback, how audition influences vocalization remains unknown. One attractive idea is that auditory signals propagate directly to those telencephalic nuclei implicated in song patterning, providing a convenient substrate for sensorimotor integration. Consistent with this idea, auditory neurons highly selective for the bird's own song have been detected in telencephalic song nuclei, and lesions of these structures can impair song perception as well as song production. This review discusses evidence for an auditory-perceptual role of the song system, the anatomical pathways by which auditory information enters the song system, the synaptic events underlying highly selective action potential responses to learned song, and the possible roles such activity could play in song learning and maintenance.     

Pure Ultrasonic Communication in an Endemic Bornean Frog

Huia cavitympanum, an endemic Bornean frog, is the first amphibian species known to emit exclusively ultrasonic (i.e., >20 kHz) vocal signals. To test the hypothesis that these frogs use purely ultrasonic vocalizations for intraspecific communication, we performed playback experiments with male frogs in their natural calling sites. We found that the frogs respond with increased calling to broadcasts of conspecific calls containing only ultrasound. The field study was complemented by electrophysiological recordings from the auditory midbrain and by laser Doppler vibrometer measurements of the tympanic membrane''s response to acoustic stimulation. These measurements revealed that the frog''s auditory system is broadly tuned over high frequencies, with peak sensitivity occurring within the ultrasonic frequency range. Our results demonstrate that H. cavitympanum is the first non-mammalian vertebrate described to communicate with purely ultrasonic acoustic signals. These data suggest that further examination of the similarities and differences in the high-frequency/ultrasonic communication systems of H. cavitympanum and Odorrana tormota, an unrelated frog species that produces and detects ultrasound but does not emit exclusively ultrasonic calls, will afford new insights into the mechanisms underlying vertebrate high-frequency communication.     

Sex‐specific responses to territorial intrusions in a communication network: Evidence from radio‐tagged great tits

Signals play a key role in the ecology and evolution of animal populations, influencing processes such as sexual selection and conflict resolution. In many species, sexually selected signals have a dual function: attracting mates and repelling rivals. Yet, to what extent males and females under natural conditions differentially respond to such signals remains poorly understood, due to a lack of field studies that simultaneously track both sexes. Using a novel spatial tracking system, we tested whether or not the spatial behavior of male and female great tits (Parus major) changes in relation to the vocal response of a territorial male neighbor to an intruder. We tracked the spatial behavior of male and female great tits (N = 44), 1 hr before and 1 hr after simulating territory intrusions, employing automatized Encounternet radio‐tracking technology. We recorded the spatial and vocal response of the challenged males and quantified attraction and repulsion of neighboring males and females to the intrusion site. We additionally quantified the direct proximity network of the challenged male. The strength of a male's vocal response to an intruder induced sex‐dependent movements in the neighborhood, via female attraction and male repulsion. Stronger vocal responders were older and in better body condition. The proximity networks of the male vocal responders, including the number of sex‐dependent connections and average time spent with connections, however, did not change directly following the intrusion. The effects on neighbor movements suggest that the strength of a male's vocal response can provide relevant social information to both the males and the females in the neighborhood, resulting in both sexes adjusting their spatial behavior in contrasting ways, while the social proximity network remained stable. This study underlines the importance of “silent” eavesdroppers within communication networks for studying the dual functioning and evolution of sexually selected signals.     

Brain activity in an awake chimpanzee in response to the sound of her own name

The brain activity of a fully awake chimpanzee being presented with her name was investigated. Event-related potentials (ERPs) were measured for each of the following auditory stimuli: the vocal sound of the subject''s own name (SON), the vocal sound of a familiar name of another group member, the vocal sound of an unfamiliar name and a non-vocal sound. Some differences in ERP waveforms were detected between kinds of stimuli at latencies at which P3 and Nc components are typically observed in humans. Following stimulus onset, an Nc-like negative shift at approximately 500 ms latency was observed, particularly in response to SON. Such specific ERP patterns suggest that the chimpanzee processes her name differently from other sounds.     

Clicks and Communication: The Behavioural and Social Contexts of Hector's Dolphin Vocalizations

Hector's dolphins (Cephalorhynchus hectori) have a simple vocal repertoire, consisting almost entirely of ultrasonic clicks. They produce no whistles, and very few audible sounds. To examine acoustic communication in this species I analysed the relationship between click types and behaviour. The proportion of complex click types was greater in large groups, suggesting that these sounds have social significance. Clicks having 2 peaks in their time envelope and two frequency peaks were strongly associated with behaviours indicative of feeding. High pulse rate sounds, in which the repetition rate of ultrasonic clicks was audible as a “cry”, were most strongly associated with aerial behaviours. These data suggest that echo-location is not the sole function of Hector's dolphin clicks, and that echo-location and communication are likely to be closely linked. I hypothesize that dolphins may have the ability to gather information from the echoes of each other's sonar pulses. This may reduce the need for a large number of vocal signals, and may explain the apparent simplicity of the acoustic repertoires of some odontocetes.     

Prioritization of emotional signals by the human auditory system: evidence from a perceptual hysteresis protocol

It is expected that natural selection has endowed our auditory apparatus with the ability to adaptively prioritize information that is crucial for survival and reproduction, such as vocal emotional signals emitted by our conspecifics, even in a noisy and dynamic natural environment (signals progressively emerge or fade away in noise as conspecifics move toward or away from us). Here, we tested the hypothesis that emotional signals are detected more easily (i.e., at lower signal-to-noise levels) and retained for a longer time (i.e., persisting in your sensory system at greater distance from the physical source) than signals bearing no emotional content, using a perceptual hysteresis protocol. Trials consisted of emotional signals (i.e., laughter and screams) or neutral signals (spectrally-rotated versions of the emotional stimuli) progressively emerging from white noise (ascending sequences) or progressively fading away in white noise (descending sequences). We demonstrated that vocal emotional signals were significantly detected at lower signal-to-noise levels than emotionally neutral signals in both ascending and descending sequences, suggesting that the human auditory system prioritizes signals bearing adaptive value.     

Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning

Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird''s own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning.     

Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds

Norepinephrine (NE) is thought to play important roles in the consolidation and retrieval of long-term memories, but its role in the processing and memorization of complex acoustic signals used for vocal communication has yet to be determined. We have used a combination of gene expression analysis, electrophysiological recordings and pharmacological manipulations in zebra finches to examine the role of noradrenergic transmission in the brain's response to birdsong, a learned vocal behavior that shares important features with human speech. We show that noradrenergic transmission is required for both the expression of activity-dependent genes and the long-term maintenance of stimulus-specific electrophysiological adaptation that are induced in central auditory neurons by stimulation with birdsong. Specifically, we show that the caudomedial nidopallium (NCM), an area directly involved in the auditory processing and memorization of birdsong, receives strong noradrenergic innervation. Song-responsive neurons in this area express α-adrenergic receptors and are in close proximity to noradrenergic terminals. We further show that local α-adrenergic antagonism interferes with song-induced gene expression, without affecting spontaneous or evoked electrophysiological activity, thus dissociating the molecular and electrophysiological responses to song. Moreover, α-adrenergic antagonism disrupts the maintenance but not the acquisition of the adapted physiological state. We suggest that the noradrenergic system regulates long-term changes in song-responsive neurons by modulating the gene expression response that is associated with the electrophysiological activation triggered by song. We also suggest that this mechanism may be an important contributor to long-term auditory memories of learned vocalizations.     

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).     

Female reproductive state influences the auditory midbrain response

Female behavioral responses to sensory stimuli can be highly variable across the reproductive cycle. Female green treefrogs (Hyla cinerea) use the male vocal signal to locate and choose a mate. Gravid females approach a vocalizing male to mate but do not approach if they have recently mated. Such differences in behavioral response may be due in part to shifts in the neural representation of auditory information in the brain. In this study, we investigated the influence of female reproductive state on neural responses in the auditory midbrain to both communication signals (advertisement calls) and non-communication sounds (band limited noise bursts). Recently mated females exhibited significantly reduced response strengths compared to females not recently mated. Reduced response strengths in post-mated females were in response to both noise bursts and male advertisement calls but were limited to the lower frequency range corresponding to the amphibian papilla of the peripheral auditory system. Our results therefore show that the ability of social signals to stimulate the auditory system differs in females depending on their reproductive state, and that the differential effect on low versus high spectral sensitivities may influence the way the two spectral peaks of male advertisement calls are represented.     

Mother-Infant Communication in the Lesser Spear-nosed Bat Phyllostomus discolor (Chiroptera,Phyllostomidae) — Evidence for Acoustic Learning

When mother-offspring couples of Phyllostomus discolor (lesser spear-nosed bat) are reunited after separation, an intensive exchange of infants' isolation calls and mothers' directive calls can be observed. The directive calls of each mother show a distinctive frequency-time structure, which appears to represent her individual vocal signature. During ontogenesis the isolation calls of the young change gradually, adapting increasingly to the mother's call type. A comparison of calls of separated pups at different ages with their mothers' directives demonstrated the individually distinct call characteristics of the mother also to be characteristic of the isolation calls of her young by about 50 days of age. This suggests that acoustic signals may be learned in Phyllostomus discolor.