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The Songbird as a Model for the Generation and Learning of Complex Sequential Behaviors
Abstract and Figures
Over the past four decades songbirds have become a widely used model organism for neuroscientists studying complex sequential
behaviors and sensory-guided motor learning. Like human babies, young songbirds learn many of the sounds they use for communication
by imitating adults. This remarkable behavior emerges as a product of genetic predispositions and specific individual experiences.
Research on different aspects of this behavior has elucidated key principles that may underlie vertebrate motor learning and
motor performance in general, including (1) the mechanisms by which neural circuits generate sequential behaviors, (2) the
existence of specialized neuronal circuits for the generation of exploratory variability, (3) the importance of basal ganglia–forebrain
circuits for learning sequentially patterned behaviors, including speech and language, and (4) the existence of genetic toolkits
that may have been coopted multiple times during evolution to play a role in learned vocal communication, such as the transcription
factor FoxP2 and its molecular targets. This review presents new techniques, experiments, and findings in areas where songbirds
have made significant contributions toward understanding of some of the most fundamental questions in neuroscience.
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... In vocal learners, vocal skills are typically acquired over postnatal development, when the body is growing, and maintained over adulthood. Especially for songbirdswidely accepted as the closest animal analogue for human speech acquisition 3,4the critical contribution of reshaping sensory and motor circuits to song learning is well established 3,[5][6][7][8] . However, whether vocal muscles require motor practice to improve and maintain performance, and if such changes directly affect vocal output remains unknown for any vocalizing vertebrate, including humans 9 . ...
... Individual syllable production and sequence is highly stereotyped. Like human speech auditory feedback corrects the motor code for deviations from the song template 5,81 . Altered acoustic feedback can drive changes in e.g. ...
Vocal signals, including human speech and birdsong, are produced by complicated , precisely coordinated body movements, whose execution is fitness-determining in resource competition and mate choice. While the acquisition and maintenance of motor skills generally requires practice to develop and maintain both motor circuitry and muscle performance, it is unknown whether vocal muscles, like limb muscles, exhibit exercise-induced plasticity. Here, we show that juvenile and adult zebra finches (Taeniopygia castanotis) require daily vocal exercise to first gain and subsequently maintain peak vocal muscle performance. Experimentally preventing male birds from singing alters both vocal muscle physiology and vocal performance within days. Furthermore, we find females prefer song of vocally exercised males in choice experiments. Vocal output thus contains information on recent exercise status, and acts as an honest indicator of past exercise investment in songbirds, and possibly in all vocalising vertebrates. Producing complex learned vocalizations, such as human speech and birdsong, comprises some of the most intricate, temporally precisely coordinated movements of the vertebrate body. The precise motor control and execution of these vocal motor skills ultimately plays a decisive role in mate choice and resource competition 1,2. The acquisition and maintenance of motor skills requires motor practice i) to develop and maintain motor circuitry and ii) to improve and maintain muscle performance. In vocal learners, vocal skills are typically acquired over postnatal development, when the body is growing, and maintained over adulthood. Especially for songbirds-widely accepted as the closest animal analogue for human speech acquisition 3,4-the critical contribution of reshaping sensory and motor circuits to song learning is well established 3,5-8. However, whether vocal muscles require motor practice to improve and maintain performance, and if such changes directly affect vocal output remains unknown for any vocalizing vertebrate, including humans 9 .
... In vocal learners, vocal skills are typically acquired over postnatal development, when the body is growing, and maintained over adulthood. Especially for songbirdswidely accepted as the closest animal analogue for human speech acquisition 3,4the critical contribution of reshaping sensory and motor circuits to song learning is well established 3,[5][6][7][8] . However, whether vocal muscles require motor practice to improve and maintain performance, and if such changes directly affect vocal output remains unknown for any vocalizing vertebrate, including humans 9 . ...
... Individual syllable production and sequence is highly stereotyped. Like human speech auditory feedback corrects the motor code for deviations from the song template 5,81 . Altered acoustic feedback can drive changes in e.g. ...
Vocal signals, including human speech and birdsong, are produced by complicated, precisely coordinated body movements, whose execution is fitness-determining in resource competition and mate choice. While the acquisition and maintenance of motor skills generally requires practice to develop and maintain both motor circuitry and muscle performance, it is unknown whether vocal muscles, like limb muscles, exhibit exercise-induced plasticity. Here, we show that juvenile and adult zebra finches (Taeniopygia castanotis) require daily vocal exercise to first gain and subsequently maintain peak vocal muscle performance. Experimentally preventing male birds from singing alters both vocal muscle physiology and vocal performance within days. Furthermore, we find females prefer song of vocally exercised males in choice experiments. Vocal output thus contains information on recent exercise status, and acts as an honest indicator of past exercise investment in songbirds, and possibly in all vocalising vertebrates.
... The SCS is a set of cytoarchitecturally discrete brain nuclei that control vocal learning, song memory, and song production (Brenowitz et al. 1997;Fee and Scharf 2010;Ball 2016). These nuclei are divided into an anterior pathway that controls song learning, memory and sensory feedback; and posterior pathway involved in song production (Fee and Scharff 2010). The anterior forebrain pathway begins in HVC (the acronym is the proper name) and projects to Area X of the medial striatum and then to the medial portion of the dorsolateral thalamic nucleus (DLM). ...
... The anterior forebrain pathway begins in HVC (the acronym is the proper name) and projects to Area X of the medial striatum and then to the medial portion of the dorsolateral thalamic nucleus (DLM). Subsequently, the anterior pathway projects to the lateral magnocellular nucleus of the anterior nidopallium (LMAN) and finally to the robust nucleus of the arcopallium (RA) (Fee and Scharff 2010). Conversely, the posterior pathway connects directly from the HVC to the RA and then eventually on to the syrinx and other muscles used in vocal production. ...
Birdsong is a relatively well-studied behavior, both due to its importance as a model for vocal production learning and as an intriguing complex social behavior. Until the last few decades, work on birdsong focused almost exclusively on males. However, it is now widely accepted that female song not only exists, but is fairly common throughout the oscine passerines. Despite this, and the large number of researchers who have begun exploring female song in the field, researchers in the lab have been slow to adopt model species with female song. Studying female song in the lab is critical for our understanding of sex-specific factors in the physiology controlling this fascinating behavior. Additionally, as a model for vocal production learning in humans, understanding the mechanistic and neuroendocrine control of female song is clearly important. In this study, we examined the red-cheeked cordon bleu (RCCB), an Estrildid finch species with extensive female song. Specifically, we found that there were no significant sex differences in circulating levels of testosterone and progesterone, nor in song production rate. There were no significant differences in cell densities in the three nuclei of the song control system we examined. Additionally, the volume of the robust nucleus of the arcopallium was not significantly different and we report the smallest sex difference in HVC yet published in a songbird. Finally, we demonstrated similar levels of motor driven immediate early gene expression in both males and females after song production.
... In vocal learners, vocal skills are typically acquired over postnatal development, when the body is growing, and maintained over adulthood. Especially for songbirdswidely accepted as the closest animal analogue for human speech acquisition 3,4the critical contribution of reshaping sensory and motor circuits to song learning is well established 3,[5][6][7][8] . However, whether vocal muscles require motor practice to improve and maintain performance, and if such changes directly affect vocal output remains unknown for any vocalizing vertebrate, including humans 9 . ...
... Individual syllable production and sequence is highly stereotyped. Like human speech auditory feedback corrects the motor code for deviations from the song template 5,81 . Altered acoustic feedback can drive changes in e.g. ...
Vocal signals mediate much of human and non-human communication. Key performance traits - such as repertoire size, speed and accuracy of delivery - affect communication efficacy in fitness-decisive contexts such as mate choice and resource competition1. Specialized fast vocal muscles2,3 are central to accurate sound production4, but it is unknown whether vocal, like limb muscles5,6, need exercise to gain and maintain peak performance7,8. Here, we show that for song development in juvenile songbirds, the closest analogue to human speech acquisition9, regular vocal muscle exercise is crucial to achieve adult peak muscle performance. Furthermore, adult vocal muscle performance reduces within two days of abolishing exercise, leading to downregulation of critical proteins transforming fast to slower muscle fibre types. Daily vocal exercise is thus required to both gain and maintain peak vocal muscle performance, and if absent changes vocal output. We show that conspecifics can detect these acoustic changes and females prefer the song of exercised males. Song thus contains information on recent exercise status of the sender. Daily investment in vocal exercise to maintain peak performance is an unrecognized cost of singing and could explain why many birds sing daily even under adverse conditions10. Because neural regulation of syringeal and laryngeal muscle plasticity is equivalent, vocal output may reflect recent exercise status in all vocalizing vertebrates.
... Birdsong and the supporting network of brain nuclei, the vocal control system, have emerged as a widely used model system to analyse biological mechanisms underlying important phenomenon including vocal learning, brain plasticity, brain lateralization, steroid action on brain and behavior, and also sex differences in brain and behavior (reviewed in [1][2][3][4][5][6][7]). In many songbird species including canaries, syllables are building blocks, and can come in different types. ...
Background
Behavioral sex differences are widespread in the animal world. These differences can be qualitative (i.e., behavior present in one sex but not the other, a true sex dimorphism) or quantitative (behavior is present at a higher rate or quality in one sex compared to the other). Singing in oscine songbirds is associated with both types of differences. In canaries, female rarely sing spontaneously but they can be induced to do so by treatments with steroids. Song in these females is, however, not fully masculinized and exhibits relatively subtle differences in quality as compared with male song. We analyzed here sex differences in syllable content and syllable use between singing male and female canaries.
Methods
Songs were recorded from three groups of castrated male and three groups of photoregressed female canaries that had received Silastic™ implants filled with testosterone (T), with T plus estradiol (E2), or left empty (control). After 6 weeks of hormone treatment, 30 songs were recorded from each of the 47 subjects. Songs were segmented and each syllable was annotated. Various metrics of syllable diversity were extracted and network analysis was employed to characterize syllable sequences.
Results
Male and female songs were characterized by marked sex differences related to syllable use. Compared to females, males had a larger syllable-type repertoire and their songs contained more syllable types. Network analysis of syllable sequences showed that males follow more fixed patterns of syllable transitions than females. Both sexes, however, produced song of the same duration containing the same number of syllables produced at similar rates (numbers per second).
Conclusions
Under the influence of T, canaries of both sexes are able to produce generally similar vocalizations that nevertheless differ in specific ways. The development of song during ontogeny appears to be a very sophisticated process that is presumably based on genetic and endocrine mechanisms but also on specific learning processes. These data highlight the importance of detailed behavioral analyses to identify the many dimensions of a behavior that can differ between males and females.
... Just as the cortico-basal ganglia network is necessary for learning sequences of syllables in birds, it has also been found to be fundamental for sequential learning and chunking in mammals (Boyd et al. 2009;Fee and Scharff 2010;Graybiel 1998). In this section, studies involving lesions, electrophysiological recordings, pharmacological interventions and optogenetic manipulations of the basal ganglia during sequential learning tasks are reviewed. ...
Integrating individual actions into coherent, organised behavioural units, a process called chunking, is a fundamental, evolutionarily conserved process that renders actions automatic. In vertebrates, evidence points to the basal ganglia - a complex network believed to be involved in action selection - as a key component of action sequence encoding, although the underlying mechanisms are only just beginning to be understood. Central pattern generators control many innate automatic behavioural sequences that form some of the most basic behaviours in an animal's repertoire, and in vertebrates, brainstem and spinal pattern generators are under the control of higher order structures such as the basal ganglia. Evidence suggests that the basal ganglia play a crucial role in the concatenation of simpler behaviours into more complex chunks, in the context of innate behavioural sequences such as chain grooming in rats, as well as sequences in which innate capabilities and learning interact such as birdsong, and sequences that are learned from scratch, such as lever press sequences in operant behaviour. It has been proposed that the role of the striatum, the largest input structure of the basal ganglia, might lie in selecting and allowing the relevant central pattern generators to gain access to the motor system in the correct order, while inhibiting other behaviours. As behaviours become more complex and flexible, the pattern generators seem to become more dependent on descending signals. Indeed, during learning, the striatum itself may adopt the functional characteristics of a higher order pattern generator, facilitated at the microcircuit level by striatal neuropeptides.
... Zebra finches, canaries, and other tiny finches like Lonchura stratum Domestica are among the most favored songbird species for neurological study, because their tiny size makes it easier in groups to maintain and propagate the zebra finches in research settings (Schmidt 2010). Additionally, studies are conducted on their behavioral characteristics, including sexual dimorphisms, ability to sing all year round, and ability to learn songs with age (Fee and Scharff 2010). A variety of psychological and neuroscientific studies have been conducted on pigeons (Columba livia), including tests for cognitive functions, neural anatomy, and neuroendocrinology (Shanahan et al. 2013). ...
Cancer has traditionally been the center of human interest all around the world, making it a medical research hotspot. Animal models are categorized based on the method used to induce cancer in the animal. The mouse has been the standard animal model for fundamental and preclinical cancer research, although other species, such as zebrafish, serve essential and complementary roles as cancer research models. A number of treatments, including chemical or physical mutagenesis, viral infection, transgene insertion, homologous recombination, and the recently established gene edition, have resulted in genetically altered mouse and zebrafish cancer models. As research advances, the methods for creating cancer animal models become increasingly diversified, including chemical induction, xenotransplantation, gene programming, and so forth. The introduction of genetically engineered animal models has greatly aided in the understanding of the illness. Animal models can be utilized not only to study the biochemical and physiological mechanisms of cancer incidence and progression in objects but also for cancer medication screening and gene therapy research. Animal models are useful for researching the biology and genetics of human malignancies, as well as for preclinical research into anti-cancer medicines and cancer prevention. Major strides have been achieved in the development of animal models of cancer, which have become increasingly complex via the use of new technologies and the incorporation of clinical data from patients.
We humans are one of the rare animals that imitate others. Imitation enables us to transmit language, music, and other skills and knowledge across generations, contributing to the growth of complex cultures and civilizations. Among mammals, only a handful of species have been reported to imitate others, whereas vocal imitation is oddly common in some avian species including songbirds. Similar to human speech, birdsong is a sequence of complex vocalizations transmitted across generations through imitative learning. Recent advances in neuroscience have begun to elucidate specialized neural circuits underlying the vocal imitation in songbirds. This chapter focuses on songbirds and some other social animals with vocal imitation and discusses how studies on these animals can be useful to understand not only our imitation ability, but also our sociality and complex cultures.Keywords
Songbird
Birdsong
Vocal learning
Imitation
Cultural transmission
Artificial intelligence researchers have been attracted by the idea of having robots learn how to accomplish a task, rather than being told explicitly. Reinforcement learning has been proposed as an appealing framework to be used in controlling mobile agents. Robot learning research, as well as research in biological systems, face many similar problems in order to display high flexibility in performing a variety of tasks. In this work, the controlling of a vehicle in an avoidance task by a previously developed operant learning model (a form of animal learning) is studied. An environment in which a mobile robot with proximity sensors has to minimize the punishment for colliding against obstacles is simulated. The results were compared with the Q-Learning algorithm, and the proposed model had better performance. In this way a new artificial intelligence agent inspired by neurobiology, psychology, and ethology research is proposed.
In addition to the goal of acquiring a precise description of the acoustic environment, central auditory processing also provides useful information for animal behaviors, such as navigation and communication. Singing is a learned behavior of male songbirds for protecting territories and attracting females (Konishi, 1985; Catchpole and Slater, 1995). It has been experimentally shown that singing behavior depends on auditory information in two ways. First, the phonetic features of a bird’s song depends on the bird’s auditory experience during a limited period after birth. Second, the development of songs of a juvenile bird depends on the auditory feedback of its own vocalization.
The development of singing in birds ranks as a prime biological model for understanding how nature and nurture interact, and how they jointly affect the growth of behavioral competence. Research on this subject benefits from contributions from many different disciplines, including neurobiology and genetics, as well as behavioral biology. There are further advantages. Behavioral studies offer the prospect of uncovering aspects of song development at three different levels. Besides an investigation of so-called developmental trajectories, including rules that describe the many transformations of a juvenile's vocal utterances, there are two kinds of reference patterns to which each vocalization can be compared; the stimulus patterns that a bird has experienced earlier, and the target songs that he finally performs as an adult. Learning to sing takes some time. Usually it begins when a young bird leaves the nest, and then continues for several months. It comes to an end only shortly before the bird establishes his own territory and flags its turf by singing. Although some species also learn new songs later in life, the first year of song development is crucial in all songbirds. Their many accomplishments can be subdivided into two major stages: the auditory phase of song memorization, and the motor phase of song development. The chapter treats the various aspects of learning to sing in some detail, keeping as a framework of typical biological concepts that are often used to explain the behavioral accomplishments of organisms, either as a consequence of evolutionary adaptation, or as mechanisms to solve a particular problem successfully.
