Song behavior refers to complex vocalizations used in the context of mate attraction and territorial defense. Birds that produce such sounds are commonly called songbirds. Technically songbirds constitute species in the avian order Passeriformes. This is by far the largest avian order and contains about half of the more than 9,000 living bird species. The songbird order, one of the most recently evolved, includes familiar avian groups such as sparrows, swallows, starlings, canaries, finches, warblers, jays, titmice, crows, wrens, robins, and buntings. This order can be further divided into two suborders, the Oscines (members of the suborder Passeres) and the sub-Oscines (a much smaller group that includes the flycatchers of North America), which appeared earlier in evolutionary history and is thought to be more primitive. All songbirds produce complex vocalizations, but there do appear to be qualitative differences between Oscine species and sub-Oscine species in vocal development and in the neural substrate mediating vocal learning and production.
The Basics of Birdsong
All songbirds have a repertoire of up to twenty or so distinct vocal sounds that they use for communication about danger, food, sex, group movements, and for many other purposes. One can usually make a distinction between a bird's calls, which are usually brief and monosyllabic, and its songs, which are more extended patterns of sound and often tonal and melodic. The decision to classify a vocalization as a song or a call is usually based on the perceived function. The main functions that have been ascribed to song behavior are territory defense (or spacing behavior) and mate attraction, as opposed to calls, which are involved in such functions as signaling danger or food and maintaining flock cohesion. Songs, especially among songbird species in the temperate zone, are usually produced by males. Among tropical species females as well as males often sing. In some species, males and females sing a coordinated song that is known as a duet.
Unlike most calls, songs are learned: They develop abnormally if a young male is reared out of hearing of the sounds of adults (see Figure 1). Among species
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in the songbird order only the Oscines clearly learn their songs; in the few sub-Oscine species investigated song learning does not appear to occur thus providing a natural comparison between closely related species that vary in one key aspect of their vocal behavior. A common consequence of this dependence on learning among Oscines is the emergence of local song dialects, varying on much the same geographic scale as dialects in human speech. These dialect boundaries have been shown to serve as imperfect barriers for gene flow in species such as the white-crowned sparrow indicating that this intraspecific geographic variation is meaningful (MacDougall-Shackleton and MacDougall-Shackleton, 2001).
Songbirds are unique among animals in the many analogies that can be struck between song learning and the acquisition of human speech (Doupe and Kuhl, 1999). Avian vocal development provides one of the few tractable animal models for studying the behavioral, hormonal, and neural bases of vocal plasticity (Ball and Hulse, 1998). No known nonhuman primate depends upon learning to develop its natural vocal repertoire. Other than humans, cetaceans and perhaps some bats are the only mammals that appear to rely on learning for vocal development. The avian groups known to have learned songs include hummingbirds, parrots, and all Oscine songbirds.
Sensitive Periods and the Timing of Song Learning
There is an underlying pattern in the steps typically required in learning to sing. First is the acquisition phase, when a bird hears songs and commits some to memory. These are stored for a period that varies in duration from species to species—from days to months—until the bird begins to recall songs from memory and starts to produce imitations, sometimes faithful to the original model, sometimes far different. Thus there is a separation in time between the acquisition or sensory phase and the production or sensorimotor phase, ending with the production of crystallized, adult song (Marler, 1997).
There are often sensitive periods for song acquisition, sometimes restricted to a short period early in life, and sometimes extending into adulthood. Even close relatives, such as sparrows and canaries, may differ in this respect. Several species of sparrows have a sensitive period for acquiring songs beginning at about twenty days of age, soon after young males become independent from their parents, and ending four to six weeks later (Nelson, 1997). Such sensitive periods for learning are variable within limits, depending on the strength of song stimulation and the influence of physiological factors, such as hormonal states, that vary with the season. If young are hatched late in the season and singing has already ceased for that year, closure of the sensitive period may be delayed until the following spring. The experimental withholding of stimulation by songs of the birds' own species can also delay closure of the learning (Kroodsma and Pickert, 1980; Baptista and Gaunt, 1997). Species that learn song only during a sensitive period early in ontogeny are known as age-limited learners. Species that continue to learn new songs throughout their lives (such as canaries and European starlings) are referred to as age-independent learners. In addition, there are species that fall in between these extreme cases in terms of song development.
Effects of Isolation and Deafness
Regardless of whether or not they have had the chance to learn, songbirds can always produce some aspects of the normal song of their species. When sparrows are raised in isolation, for example, the note structure and tonal quality of their songs is abnormal, but each species still produces some basic features of normal song "syntax" (see Figure 1). These features are produced irrespective of whether they were represented in any songs a male may have learned.
Insight into the basis of this ability to produce certain normal song features is gained by studying the songs of deaf birds, which are highly abnormal and variable in structure (see Figure 1). This degraded form of singing is observed both if a male becomes deaf before song stimulation and if he is deafened after song stimulation but before the development of singing. There seems to be no internal brain circuitry that makes memorized songs directly available to guide motor development. To transform a memorized song into a produced song, the bird must be able to hear its own voice. One can infer that there are auditory memories for song, involved in guiding song production, conceived of as neural mechanisms in the auditory circuitry of the songbird brain that must vary in their specifications from species to species (Konishi, 1965; Marler, 1997).
The Nature of the Auditory Memory Guiding Song Learning
One aspect of the process of memory formation needed for song learning is that it involves "selective" or "guided" learning. In several sparrow species, for example, species-typical vocalizations appear to be privileged because they are learned preferentially. Such preferences have even been observed for specific subspecies (Nelson, 2000). Another aspect of this memory, strongly advocated by Peter Marler and colleagues, is that the memory encodes species-typical patterns of vocal behavior even before it hears the song of its own species. This idea of an innate specification of species-typical vocalizations would be one way to explain why even in isolated-reared sparrows many species-typical attributes of their vocalizations are still apparent in the abnormal songs produced by these birds. According to this view of song learning, the formation of the auditory memory guiding song learning would result from a memorization by selective activation and attrition of innate circuits rather than from a selective instruction process (Marler, 1997). Researchers have not yet resolved the relative validity of these two opposing models of auditory memory formation.
Song Overproduction, Social Interactions, and Action-Based Learning
The young male songbird typically begins singing sometime after he has memorized learned songs, but the imitations are not fully formed. Instead, the young male starts with subsong, an amorphous, noisy twittering that changes gradually, first into plastic song, which also is highly variable but contains the first obvious signs of mature song structure, finally crystallizing into the stable patterns of mature, adult song (see Figure 2). Subsong resembles the babbling of human infants and may be important for developing the motor skills of singing and other prerequisites for song learning, such as the ability to guide the voice by the ear. Rehearsal of previously memorized song patterns begins in plastic song. Often more plastic song themes are produced than are needed for mature singing (see Figure 3), and many are discarded when song crystallization occurs. Interactions between a male and his neighbors can influence which of the overproduced songs will be selected for crystallization and inclusion into the final repertoire (Nelson, 1997). Songs most similar to the neighbor's songs are retained; those that are different are rejected. It is as if a process akin to operant conditioning influences which songs are selected for later crystallization among those in auditory memory. Marler and Douglas A. Nelson (1993) refer to this process as "action-based" learning to contrast it with "memory-based" learning. The latter refers to cases where crystallized songs are produced in reference to previously formed memories independently of social interactions during the sensorimotor period.
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The Song System
A discrete set of brain areas discovered by F. Nottebohm (Nottebohm, 1996), often called the song system, controls song learning and production. The song system suggests a possible location for the neural changes associated with song learning. The song system consists of numerous interconnected nuclei and occupies a relatively large volume of brain (see Figure 4). The brain area nXIIts (the tracheosyringeal portion of the hypoglossal nucleus) contains the motor neurons that control the musculature of the bird's vocal organ, the syrinx. The pathway from Nif (the nucleus interface) through HVc (or high vocal center) to RA (the robust nucleus of the archistriatum) and then to nXIIts constitutes a motor pathway specialized for song production. RA also projects to brainstem areas controlling respiration, which needs to be coordinated with song (Wild, 1997). The anterior forebrain song nuclei lMAN (the lateral part of the magnocellular nucleus of the anterior neostriatum) and area X, as well as the thalamic nucleus that interconnects them, DLM (the medial portion of the dorsolateral nucleus of the thalamus), form a second pathway connecting HVc to RA. All of the song nuclei are present bilaterally, and the thalamic song nucleus Uva (the uvaeform nucleus) forms a connection between the two sides.
The presence of a song system is particularly associated with the learning of song, not just with song production. These brain areas are found only in birds that sing and that learn their song by reference to auditory information. For example, sub-Oscine song-birds that do not learn their vocalizations do not seem to have telencephalic song nuclei such as HVc or RA. The vast majority of vocal learners are Passerine songbirds, but evolutionarily unrelated species that are vocal mimics, such as parrots or hummingbirds, which require conspecific learning to produce their complex vocalizations, are also found to have fore-brain structures resembling nuclei in the song system including HVc and RA (Jarvis and Mello, 2000; Jarvis et al., 2000; Gahr, 2000).
A Motor Pathway for Song
Evidence for a specialized motor pathway for song comes from three sources. Behavioral studies show that lesions of HVc, RA, or the hypoglossal nerve cause severe disruption of adult song. Also, electrophysiological recordings in Nif, HVc, and RA of awake birds reveal neurons whose activity is highly correlated with singing (Yu and Margoliash, 1996). These data indicate a hierarchy in motor processing with activity in HVc correlated with syllable production and activity in RA correlated with note production (Yu and Margoliash, 1996). Nif may be the bird-song pattern generator, because section of the tract from Nif to HVc destroys the patterning of song, while lesions of Uva do not (McCasland, 1987). Motor-driven immediate early gene induction also occurs in nuclei such as HVc and RA in that song production is correlated with such induction in deaf birds induced to sing (Jarvis and Nottebohm, 1997).
The song motor commands must ultimately be translated into a pattern of syringeal muscle activation and respiratory control. The output nucleus of the song system, nXIIts, has a map of the muscles of the syrinx: All motor neurons projecting to a particular syringeal muscle are clustered together in discrete zones within the motor nucleus. RA also has zones of premotor neurons that project to the corresponding muscle control area in nXIIts. The dorsal portion of RA does not project to nXIIts but to the dorsomedial nucleus (DM) of the midbrain, an area thought to be involved in vocalization and respiration in all birds, including nonsongbirds (see Figure 4; Vicario, 1991). Neurons in DM then project to nXIIts, suggesting that RA has two parallel and perhaps functionally different inputs to the syringeal motor neurons.
Intrabronchial measurements of both airflow and sound from each syringeal side have clarified how the syrinx functions to produce sound (Suthers, Goller, and Pytte, 1999). The syrinx contains two separate sound sources, each with an independent motor control. There is extensive species variability in how these two separate sources are used to produce a species-typical vocalization. Thus initial claims that control of song production is lateralized similarly to speech production is an oversimplification. It seems that asymmetries in syringeal control when they do occur reflect a peripheral asymmetry rather than a hemispheric specialization, as is the case in humans.
Song-Selective Auditory Pathways and Feedback Mechanisms
Because auditory feedback is used to correct vocal motor output during song learning, there must be a link between the auditory system and the vocal motor pathway. In addition, there must be brain mechanisms for very specific recognition of song and song-like vocalizations. Auditory information is relayed to the songbird forebrain as in all other birds, traveling from the cochlear nuclei through the thalamus to the forebrain primary auditory area, Field L. Anatomical experiments show that subdivisions of Field L projects to the vicinity of HVc and RA (Vates, Broome, Mello, and Nottebohm, 1996; see Figure 4). However, electrophysiological investigations also suggest that auditory information gains access to HVc via Nif (Janata and Margoliash, 1999). Field L projects to the caudolateral ventral hyperstriatum (clHV) that in turn projects to Nif (Vates, Broome, Mello, and Nottebohm, 1996). In addition to song-related motor neurons, HVc also contains neurons that respond to auditory stimuli. Some of these HVc auditory neurons are song-selective: They respond best of all to the bird's own song, even in comparison with very similar songs of conspecifics (Margoliash, 1986). HVc song-selective neurons are also sensitive to temporal order: They are activated more strongly by the bird's own song when the syllables are in the normal sequence than when the identical song components are played out of order or in reverse. This high degree of selectivity in individual neurons provides a possible mechanism for specific recognition of song. Because the bird's own song is learned during development, this song selectivity must also be learned. In fact, studies in young birds have shown that these neurons acquire their specificity during sensorimotor learning.
Lesion studies have shown that the anterior fore-brain pathway containing MAN and X (see Figure 4) plays an important role in song learning but is not an essential part of the motor pathway for song in the adult. Lesions of MAN or X have no apparent effect on adult song production, but destruction of either of these areas in young birds results in markedly abnormal song (Bottjer and Johnson, 1997). There are song-selective auditory neurons, similar to those in HVc, in every nucleus in this loop—X, DLM, and MAN. Like the neurons in HVc, these auditory neurons acquire their song selectivity in parallel with song acquisition. If the syrinx is selectively dennervated prior to the sensorimotor phase of song learning, male zebra finches in many cases are unable to match their vocal output to the tutor's song (Solis and Doupe, 2000). In such birds, many neurons in area X exhibited a dual selectivity and responded equally well to the bird's own song and to the tutor song. The degree of selectivity for these stimuli as compared to conspecific song or reversed song was considerably less than in normal adults (Solis and Doupe, 2000).
One possible function of this song-selective auditory pathway is to act as a correction signal provided by auditory feedback for the learning of song and the maintenance of learned song. There is evidence that the delayed auditory feedback can cause a gradual deterioration of adult zebra finch song (Leonardo and Konishi, 1999). Deafening adult male zebra finches also results in a deterioration of song (Nordeen and Nordeen, 1992). However, lesioning a nucleus in the anterior forebrain pathway such as lMAN prevents the deterioration in song resulting from deafening (Brainard and Doupe, 2000). These findings suggest that an active process is required for the maintenance of song and that the anterior forebrain pathway is essential to this process.
The song-selective auditory loop from HVc to the anterior forebrain eventually projects back into the motor pathway through its connection to RA (see Figure 4). This convergence of auditory and motor inputs makes RA a possible site for the auditory guidance of vocal motor development during learning. The NMDA subclass of glutamate receptors is thought to play a role in some forms of synaptic plasticity. NMDA receptor-mediated EPSCs (NMDAEPSCs) become fast during song development, a transition posited to limit learning. However, manipulations of the sensitive period for song learning by isolating nestling zebra finches delayed NMDAEPSCs but did not prevent the birds from learning (Livingston, White, and Mooney, 2000). Thus song learning did not require slow NMDA-EPSCs at synapses critical for song development.
The Development of the Song System, Hormonal Effects, and Sex Differences in Brain and Behavior
It is a striking feature of the song system that it continues to develop after hatching, during song learning. Administration of 3H-thymidine can be used to label neurons undergoing their last cell division, or "birthdate." Such birthdating of song nuclei shows that MAN and RA are "born" before hatching, but that there is significant neurogenesis in HVc and X in the first several months after hatching (Alvarez- Buylla and Kirn, 1997). There is also naturally occurring cell death during postnatal development. In male zebra finches, many MAN neurons die around five weeks after hatching. Synaptic connectivity continues to develop at these late stages. The motor projection from HVc reaches its target nucleus RA by postnatal day fifteen, but then "waits" outside RA for about ten days before growing in and completing the circuit (Konishi and Akutagawa, 1985). Interestingly, male zebra finches first begin to sing at the time of in- growth of HVc axons into RA. Connections from HVc to MAN via X and DLM are present and functional by day fifteen, but topographic features of the projection from lMAN to RA occur at days twenty to twenty- five during the early stages of vocal learning. Timing of this projection is delayed if juvenile birds are deprived of normal conspecific auditory experience (Iyengar and Bottjer, 2002).
Bird song can vary among the sexes. Typically in temperate zone species, male birds sing for courtship and territorial defense, while female birds sing much less or not at all. In the tropics the pattern is quite different: males and females often stay together on territories all year round, and both sexes will sing to defend these territories. The behavioral dimorphism between males and females has a striking correlate in the sexual dimorphism of the song system itself. Initial studies of species the exhibit extreme differences in song behavior: For example, zebra finches and canaries revealed marked male-biased differences between males and females (Nottebohm and Arnold, 1976). Nottebohm and Arnold's discovery provided an opportunity to explore sex differences in the brain in a truly comparative sense. Comparative studies have been employed to understand the function of these sex differences in the brain (see Figure 5). In some songbird species, females sing rarely or not at all, and the brain nuclei that control song are many times larger in volume in males than in females. In other species, males and females sing approximately equally, and the brain nuclei that control song are approximately equal between the sexes. Recently statistical methods have been employed control for phylogenetic effects while comparing the coevolution of traits. This analysis indicates that the evolution of sex differences in song has coevolved with the evolution of sex differences in singing behavior in songbird species (Figure 5; MacDougall-Shackleton and Ball, 1999). It is unclear whether these morphological differences related to variation in song are just related to differences in production or if differences in song learning also occur. Sex differences in volume in nuclei such as HVc and RA are associated with differences in cell size and cell number. Other attributes of the phenotype of cells in these nuclei are different in males and females, such as the number of cells expressing androgen receptors.
Steroid hormones influence both singing and the song system. Singing is much increased when androgen levels are high, for instance during the breeding season in the spring. In several songbird species, there is also a seasonal variation in the size of the song nuclei (Tramontin and Brenowitz, 2000). In canaries, where researchers first described this trait, HVc and RA enlarge by approximately 50 percent in the spring (Nottebohm, 1981). These seasonal changes in volume involve changes in cell size and cell number (Tramontin and Brenowitz, 2000). These seasonal morphological changes were initially thought to be related to seasonal changes in song learning but current data support the notion that the changes are more closely related to seasonal changes in song performance (Tramontin and Brenowitz, 2000). In some species, such as canaries and white-crowned sparrows, adult females will respond to the administration of testosterone by beginning to sing and rapidly going through the sensorimotor phase of learning. These injections also induce marked growth of the song nuclei. The effects of testosterone in stimulating these cellular changes in HVc are mediated at least in part via the upregulation of brain-derived neurotrophic factor, or BDNF (Rasika, Alvarez-Buylla, and Nottebohm, 1999). Interestingly, there is also evidence that BDNF is released in HVc in response to singing itself. Thus testosterone can promote morphological changes in HVc by acting directly on cells in that nucleus or by acting elsewhere in the brain (such as the preoptic area) to induce increased singing behavior that results in increased BDNF in HVc (Ball, Riters, and Balthazart, 2002).
The influence of sex steroids on the development of the song system has been extensively studied in zebra finches, where the differences between the male and female song systems are especially pronounced (see Figure 5). Female zebra finches have very small and shrunken song nuclei and, unlike canaries, do not respond with song to testosterone administration in adulthood. If given estrogen early in life, however, female zebra finch chicks develop masculinized song nuclei (Schlinger, 1998). Based on many studies of zebra finches, researchers are clear that this differentiation process that occurs early in ontogeny is not the result of sex differences in gonadal steroid hormone action as is the case in the mammalian brain and in other aspects of sexually dimorphic behaviors in birds (Schlinger, 1998). Rather, it is either the result of estrogen synthesized by the brain acting early in ontogeny to masculinize the system (Holloway and Clayton, 2001) or of sex differences in gene expression in the brain that is triggered independently of the gonad.
Another unusual feature of the songbird brain and avian brains in general is that neurogenesis continues to occur in portions of the periventricular zone in adult birds, and these newly generated neurons migrate out into the forebrain and are incorporated into the neural circuitry. Some of these neurons in HVc project to RA (Alvarez-Buylla and Kirn, 1997). Researchers are not clear, however, what significance this phenomenon has for song learning. The new neurons occur throughout the forebrain, in females as well as males. They are found in one-time learners such as zebra finches as well as in open-ended learners like canaries, and even in nonsongbirds. Nonetheless, this phenomenon suggests that adult birds retain a remarkable ability to generate new neurons as well as a preservation of the cues for axon guidance and neuronal specification in their brains.
Vocal learning early in development during the sensory phase is associated with prominent cellular and synaptic changes. There is a neural reorganization that includes massive synaptogenesis associated with the incorporation of new neurons into the vocal pathways. Behavioral evidence clearly implicates NMDA receptor activation in specific song nuclei as being required for song learning (Basham, Nordeen, and Nordeen, 1996). However, scientists have yet to identify the precise cellular events that occur developmentally that mediate song learning rather than the maturation of the song system.
Bird song is a complex motor behavior that is learned by matching vocal output to an auditory memory. This memory has an innate component but is also modified by experience early in ontogeny. In some species, only songs learned early in life are produced in adulthood. In other species, learning continues throughout adult life. Birds tend to learn more songs than will be used throughout adult life, and these are selected based on social interactions among conspecifics in the area they settle.
A specialized neural circuit has evolved in association with the occurrence of song learning. This circuit contains nuclei primarily involved in motor production or in the auditory feedback needed for the learning and maintenance of song. Neurons within this circuit appear to be feature detectors that exhibit highly selective response to conspecific song. The selectivity of these neurons develops in parallel with song learning. The morphology of the song system varies between males and females in a systematic fashion among different species that reflects species-variability in song behavior. Steroid hormones regulate these sex differences as well as the striking seasonal plasticity in adulthood. Songbirds exhibit adult neurogenesis that contributes to the unusual adult plasticity. Scientists have described cellular changes in synaptogenesis and neuronal incorporation that correlate with song learning. This system will continue to be a valuable model for the investigation of the neurobiology of species-typical learning.
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Revised byGregory F.Ball