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.     

Deafening drives cell-type-specific changes to dendritic spines in a sensorimotor nucleus important to learned vocalizations

Hearing loss prevents vocal learning and causes learned vocalizations to deteriorate, but how vocalization-related auditory feedback acts on neural circuits that control vocalization remains poorly understood. We deafened adult zebra finches, which rely on auditory feedback to maintain their learned songs, to test the hypothesis that deafening modifies synapses on neurons in a sensorimotor nucleus important to song production. Longitudinal in vivo imaging revealed that deafening selectively decreased the size and stability of dendritic spines on neurons that provide input to a striatothalamic pathway important to audition-dependent vocal plasticity, and changes in spine size preceded and predicted subsequent vocal degradation. Moreover, electrophysiological recordings from these neurons showed that structural changes were accompanied by functional weakening of both excitatory and inhibitory synapses, increased intrinsic excitability, and changes in spontaneous action potential output. These findings shed light on where and how auditory feedback acts within sensorimotor circuits to shape learned vocalizations.     

Sensitive periods and circuits for learned birdsong

Experience influences the development of certain behaviors and their associated neural circuits during a discrete period after birth. Songbirds, with their highly quantifiable vocal output and well-delineated vocal control circuitry, provide an excellent context in which to examine the neural mechanisms regulating sensitive periods for learning. Recent discoveries indicate that auditory input to the vocal control circuitry in songbirds is dynamically modulated and show that neural circuitry previously thought to be used only in plastic juvenile song may also actively maintain stable adult song. These findings provide important clues to how sensitive periods for auditory feedback and vocal plasticity are regulated during song development.     

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.     

Development of Auditory-Vocal Perceptual Skills in Songbirds

Songbirds are one of the few groups of animals that learn the sounds used for vocal communication during development. Like humans, songbirds memorize vocal sounds based on auditory experience with vocalizations of adult “tutors”, and then use auditory feedback of self-produced vocalizations to gradually match their motor output to the memory of tutor sounds. In humans, investigations of early vocal learning have focused mainly on perceptual skills of infants, whereas studies of songbirds have focused on measures of vocal production. In order to fully exploit songbirds as a model for human speech, understand the neural basis of learned vocal behavior, and investigate links between vocal perception and production, studies of songbirds must examine both behavioral measures of perception and neural measures of discrimination during development. Here we used behavioral and electrophysiological assays of the ability of songbirds to distinguish vocal calls of varying frequencies at different stages of vocal learning. The results show that neural tuning in auditory cortex mirrors behavioral improvements in the ability to make perceptual distinctions of vocal calls as birds are engaged in vocal learning. Thus, separate measures of neural discrimination and behavioral perception yielded highly similar trends during the course of vocal development. The timing of this improvement in the ability to distinguish vocal sounds correlates with our previous work showing substantial refinement of axonal connectivity in cortico-basal ganglia pathways necessary for vocal learning.     

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.     

Vocal Learning in Songbirds and Humans: A Retrospective in Honor of Peter Marler

Peter Marler made a number of significant contributions to the field of ethology, particularly in the area of animal communication. His research on birdsong learning gave rise to a thriving subfield. An important tenet of this growing subfield is that parallels between birdsong and human speech make songbirds valuable as models in comparative and translational research, particularly in the case of vocal learning and development. Decades ago, Marler pointed out several phenomena common to the processes of vocal development in songbirds and humans—including a dependence on early acoustic experience, sensitive periods, predispositions, auditory feedback, intrinsic reinforcement, and a progression through distinct developmental stages—and he advocated for the value of comparative study in this domain. We review Marler's original comparisons between birdsong and speech ontogeny and summarize subsequent progress in research into these and other parallels. We also revisit Marler's arguments in support of the comparative study of vocal development in the context of its widely recognized value today.     

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.     

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.     

鸟类的发声系统和调控机制

鸟类是具有复杂声行为的动物,其拥有特殊的发声器官——鸣管。尽管鸣禽与非鸣禽的发声特性和发声器官解剖学差异较大,但是两者发声运动控制模式相似。文章综述了近年来鸟类呜声研究的新进展,重点比较了呜禽和非鸣禽发声器官的结构功能特点和发声特性调控的异同。作为一种动物模型,鸟类发声系统能为人类语言学习等研究提供借鉴。     

听觉皮层信号处理

听觉系统和视觉系统的不同之处在于：听觉系统在外周感受器和听皮层间具有更长的皮层下通路和更多的突触联系。该特殊结构反应了听觉系统从复杂听觉环境中提取与行为相关信号的机制与其他感觉系统不同。听皮层神经信号处理包括两种重要的转换机制,声音信号的非同构转换以及从声音感受到知觉层面的转换。听觉皮层神经编码机制同时也受到听觉反馈和语言或发声过程中发声信号的调控。听觉神经科学家和生物医学工程师所面临的挑战便是如何去理解大脑中这些转换的编码机制。我将会用我实验室最近的一些发现来阐述听觉信号是如何在原听皮层中进行处理的,并讨论其对于言语和音乐在大脑中的处理机制以及设计神经替代装置诸如电子耳蜗的意义。我们使用了结合神经电生理技术和量化工程学的方法来研究这些问题。     

Sensory-motor interactions modulate a primate vocal behavior: antiphonal calling in common marmosets

A fundamental issue in neuroscience pertains to how different cortical systems interact to generate behavior. One of the most direct ways to address this issue is to investigate how sensory information is encoded and used to produce a motor response. Antiphonal calling is a natural vocal behavior that involves individuals producing their species-specific long distance vocalization in response to hearing the same call and engages both the auditory and motor systems, as well as the cognitive neural systems involved in decision making and categorization. Here we present results from a series of behavioral experiments investigating the auditory–vocal interactions during antiphonal calling in the common marmoset (Callithrix jacchus). We manipulated sensory input by placing subjects in different social contexts and found that the auditory input had a significant effect on call timing and propensity to call. Playback experiments tested the significance of the timing of vocal production in antiphonal calling and showed that a short latency between antiphonal calls was necessary to maintain reciprocal vocal interactions. Overall, this study shows that sensory-motor interactions can be experimentally induced and manipulated in a natural primate vocal behavior. Antiphonal calling represents a promising model system to examine these issues in non-human primates at both the behavioral and neural levels.     

From Birdsong to Human Speech Recognition: Bayesian Inference on a Hierarchy of Nonlinear Dynamical Systems

Our knowledge about the computational mechanisms underlying human learning and recognition of sound sequences, especially speech, is still very limited. One difficulty in deciphering the exact means by which humans recognize speech is that there are scarce experimental findings at a neuronal, microscopic level. Here, we show that our neuronal-computational understanding of speech learning and recognition may be vastly improved by looking at an animal model, i.e., the songbird, which faces the same challenge as humans: to learn and decode complex auditory input, in an online fashion. Motivated by striking similarities between the human and songbird neural recognition systems at the macroscopic level, we assumed that the human brain uses the same computational principles at a microscopic level and translated a birdsong model into a novel human sound learning and recognition model with an emphasis on speech. We show that the resulting Bayesian model with a hierarchy of nonlinear dynamical systems can learn speech samples such as words rapidly and recognize them robustly, even in adverse conditions. In addition, we show that recognition can be performed even when words are spoken by different speakers and with different accents—an everyday situation in which current state-of-the-art speech recognition models often fail. The model can also be used to qualitatively explain behavioral data on human speech learning and derive predictions for future experiments.     

Twitter evolution: converging mechanisms in birdsong and human speech

Vocal imitation in human infants and in some orders of birds relies on auditory-guided motor learning during a sensitive period of development. It proceeds from 'babbling' (in humans) and 'subsong' (in birds) through distinct phases towards the full-fledged communication system. Language development and birdsong learning have parallels at the behavioural, neural and genetic levels. Different orders of birds have evolved networks of brain regions for song learning and production that have a surprisingly similar gross anatomy, with analogies to human cortical regions and basal ganglia. Comparisons between different songbird species and humans point towards both general and species-specific principles of vocal learning and have identified common neural and molecular substrates, including the forkhead box P2 (FOXP2) gene.     

Neural correlates of learned song in the avian forebrain: simultaneous representation of self and others

Songbirds are extraordinary vocalists and sensitive listeners, singing to communicate identity, engage other birds in acoustical combat, and attract mates. These processes involve auditory plasticity in that birds rapidly learn to discriminate novel from familiar songs. Songbirds also are one of the few non-human animals that use auditory feedback to learn their vocalizations, thus auditory -- vocal interactions are likely to be important to vocal learning. Recent advances strengthen the connection between song recognition and processing of birdsong in the auditory telencephalon. New insights also have emerged into the mechanisms underlying the 'gating' of auditory responses and the emergence of highly selective responses, two processes that could facilitate auditory feedback important to song 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.     

Specialized Motor-Driven dusp1 Expression in the Song Systems of Multiple Lineages of Vocal Learning Birds

Mechanisms for the evolution of convergent behavioral traits are largely unknown. Vocal learning is one such trait that evolved multiple times and is necessary in humans for the acquisition of spoken language. Among birds, vocal learning is evolved in songbirds, parrots, and hummingbirds. Each time similar forebrain song nuclei specialized for vocal learning and production have evolved. This finding led to the hypothesis that the behavioral and neuroanatomical convergences for vocal learning could be associated with molecular convergence. We previously found that the neural activity-induced gene dual specificity phosphatase 1 (dusp1) was up-regulated in non-vocal circuits, specifically in sensory-input neurons of the thalamus and telencephalon; however, dusp1 was not up-regulated in higher order sensory neurons or motor circuits. Here we show that song motor nuclei are an exception to this pattern. The song nuclei of species from all known vocal learning avian lineages showed motor-driven up-regulation of dusp1 expression induced by singing. There was no detectable motor-driven dusp1 expression throughout the rest of the forebrain after non-vocal motor performance. This pattern contrasts with expression of the commonly studied activity-induced gene egr1, which shows motor-driven expression in song nuclei induced by singing, but also motor-driven expression in adjacent brain regions after non-vocal motor behaviors. In the vocal non-learning avian species, we found no detectable vocalizing-driven dusp1 expression in the forebrain. These findings suggest that independent evolutions of neural systems for vocal learning were accompanied by selection for specialized motor-driven expression of the dusp1 gene in those circuits. This specialized expression of dusp1 could potentially lead to differential regulation of dusp1-modulated molecular cascades in vocal learning circuits.     

Auditory feedback in learning and maintenance of vocal behaviour

Songbirds are one of the best-studied examples of vocal learners. Learning of both human speech and birdsong depends on hearing. Once learned, adult song in many species remains unchanging, suggesting a reduced influence of sensory experience. Recent studies have revealed, however, that adult song is not always stable, extending our understanding of the mechanisms involved in song maintenance, and their similarity to those active during song learning. Here we review some of the processes that contribute to song learning and production, with an emphasis on the role of auditory feedback. We then consider some of the possible neural substrates involved in these processes, particularly basal ganglia circuitry. Although a thorough treatment of human speech is beyond the scope of this article, we point out similarities between speech and song learning, and ways in which studies of these disparate behaviours complement each other in developing an understanding of general principles that contribute to learning and maintenance of vocal behaviour.     

Dynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica)

Species-specific behaviours gradually emerge, via incomplete patterns, to the final complete adult form. A classical example is birdsong, a learned behaviour ideally suited for studying the neural and molecular substrates of vocal learning. Young songbirds gradually transform primitive unstructured vocalizations (subsong, akin to human babbling) into complex, stereotyped sequences of syllables that constitute adult song. In comparison with birdsong, territorial and mating calls of vocal non-learner species are thought to exhibit little change during development. We revisited this issue using the crowing behaviour of domestic Japanese quail (Coturnix coturnix japonica). Crowing activity was continuously recorded in young males maintained in social isolation from the age of three weeks to four months. We observed developmental changes in crow structure, both the temporal and the spectral levels. Speed and trajectories of these developmental changes exhibited an unexpected high inter-individual variability. Mechanisms used by quails to transform sounds during ontogeny resemble those described in oscines during the sensorimotor phase of song learning. Studies on vocal non-learners could shed light on the specificity and evolution of vocal learning.