Responses to Song Playback Differ in Sleeping versus Anesthetized Songbirds.

Vocal learning in songbirds is mediated by a highly localized system of interconnected forebrain regions, including recurrent loops that traverse the cortex, basal ganglia, and thalamus. This brain-behavior system provides a powerful model for elucidating mechanisms of vocal learning, with implications for learning speech in human infants, as well as for advancing our understanding of skill learning in general. A long history of experiments in this area has tested neural responses to playback of different song stimuli in anesthetized birds at different stages of vocal development. These studies have demonstrated selectivity for different song types that provide neural signatures of learning. In contrast to the ease of obtaining responses to song playback in anesthetized birds, song-evoked responses in awake birds are greatly reduced or absent, indicating that behavioral state is an important determinant of neural responsivity. Song-evoked responses can be elicited during sleep as well as anesthesia, and the selectivity of responses to song playback in adult birds is highly similar between anesthetized and sleeping states, encouraging the idea that anesthesia and sleep are similar. In contrast to that idea, we report evidence that cortical responses to song playback in juvenile zebra finches (Taeniopygia guttata) differ greatly between sleep and urethane anesthesia. This finding indicates that behavioral states differ in sleep versus anesthesia and raises questions about relationships between developmental changes in sleep activity, selectivity for different song types, and the neural substrate for vocal learning.

Developmentally regulated pathways for motor skill learning in songbirds.

Vocal learning in songbirds is mediated by cortico-basal ganglia circuits that govern diverse functions during different stages of development. We investigated developmental changes in axonal projections to and from motor cortical regions that underlie learned vocal behavior in juvenile zebra finches (Taeniopygia guttata). Neurons in LMAN-core project to RA, a motor cortical region that drives vocal output; these RA-projecting neurons send a transient collateral projection to AId, a region adjacent to RA, during early vocal development. Both RA and AId project to a region of dorsal thalamus (DLM), which forms a feedback pathway to cortico-basal ganglia circuitry. These projections provide pathways conveying efference copy and a means by which information about vocal motor output could be reintegrated into cortico-basal ganglia circuitry, potentially aiding in the refinement of juvenile vocalizations during learning. We used tract-tracing techniques to label the projections of LMAN-core to AId and of RA to DLM in juvenile songbirds. The volume and density of terminal label in the LMAN-core→AId projection declined substantially during early stages of sensorimotor learning. In contrast, the RA→DLM projection showed no developmental change. The retraction of LMAN-core→AId axon collaterals indicates a loss of efference copy to AId and suggests that projections that are present only during early stages of sensorimotor learning mediate unique, temporally restricted processes of goal-directed learning. Conversely, the persistence of the RA→DLM projection may serve to convey motor information forward to the thalamus to facilitate song production during both learning and maintenance of vocalizations.

Multidimensional Tuning in Motor Cortical Neurons during Active Behavior.

A region within songbird cortex, dorsal intermediate arcopallium (AId), is functionally analogous to motor cortex in mammals and has been implicated in song learning during development. Non-vocal factors such as visual and social cues are known to mediate song learning and performance, yet previous chronic-recording studies of regions important for song behavior have focused exclusively on neural activity in relation to song production. Thus, we have little understanding of the range of non-vocal information that single neurons may encode. We made chronic recordings in AId of freely behaving juvenile zebra finches and evaluated neural activity during diverse motor behaviors throughout entire recording sessions, including song production as well as hopping, pecking, preening, fluff-ups, beak interactions, scratching, and stretching. These movements are part of natural behavioral repertoires and are important components of both song learning and courtship behavior. A large population of AId neurons showed significant modulation of activity during singing. In addition, single neurons demonstrated heterogeneous response patterns during multiple movements (including excitation during one movement type and suppression during another), and some neurons showed differential activity depending on the context in which movements occurred. Moreover, we found evidence of neurons that did not respond during discrete movements but were nonetheless modulated during active behavioral states compared with quiescence. Our results suggest that AId neurons process both vocal and non-vocal information, highlighting the importance of considering the variety of multimodal factors that can contribute to vocal motor learning during development.

Response properties of single neurons in higher level auditory cortex of adult songbirds.

The caudomedial nidopallium (NCM) is a higher level region of auditory cortex in songbirds that has been implicated in encoding learned vocalizations and mediating perception of complex sounds. We made cell-attached recordings in awake adult male zebra finches ( Taeniopygia guttata) to characterize responses of single NCM neurons to playback of tones and songs. Neurons fell into two broad classes: narrow fast-spiking cells and broad sparsely firing cells. Virtually all narrow-spiking cells responded to playback of pure tones, compared with approximately half of broad-spiking cells. In addition, narrow-spiking cells tended to have lower thresholds and faster, less variable spike onset latencies than did broad-spiking cells, as well as higher firing rates. Tonal responses of narrow-spiking cells also showed broader ranges for both frequency and amplitude compared with broad-spiking neurons and were more apt to have V-shaped tuning curves compared with broad-spiking neurons, which tended to have complex (discontinuous), columnar, or O-shaped frequency response areas. In response to playback of conspecific songs, narrow-spiking neurons showed high firing rates and low levels of selectivity whereas broad-spiking neurons responded sparsely and selectively. Broad-spiking neurons in which tones failed to evoke a response showed greater song selectivity compared with those with a clear tuning curve. These results are consistent with the idea that narrow-spiking neurons represent putative fast-spiking interneurons, which may provide a source of intrinsic inhibition that contributes to the more selective tuning in broad-spiking cells. NEW & NOTEWORTHY The response properties of neurons in higher level regions of auditory cortex in songbirds are of fundamental interest because processing in such regions is essential for vocal learning and plasticity and for auditory perception of complex sounds. Within a region of secondary auditory cortex, neurons with narrow spikes exhibited high firing rates to playback of both tones and multiple conspecific songs, whereas broad-spiking neurons responded sparsely and selectively to both tones and songs.

Differential developmental changes in cortical representations of auditory-vocal stimuli in songbirds.

Procedural skill learning requires iterative comparisons between feedback of self-generated motor output and a goal sensorimotor pattern. In juvenile songbirds, neural representations of both self-generated behaviors (each bird's own immature song) and the goal motor pattern (each bird's adult tutor song) are essential for vocal learning, yet little is known about how these behaviorally relevant stimuli are encoded. We made extracellular recordings during song playback in anesthetized juvenile and adult zebra finches ( Taeniopygia guttata) in adjacent cortical regions RA (robust nucleus of the arcopallium), AId (dorsal intermediate arcopallium), and RA cup, each of which is well situated to integrate auditory-vocal information: RA is a motor cortical region that drives vocal output, AId is an adjoining cortical region whose projections converge with basal ganglia loops for song learning in the dorsal thalamus, and RA cup surrounds RA and receives inputs from primary and secondary auditory cortex. We found strong developmental differences in neural selectivity within RA, but not in AId or RA cup. Juvenile RA neurons were broadly responsive to multiple songs but preferred juvenile over adult vocal sounds; in addition, spiking responses lacked consistent temporal patterning. By adulthood, RA neurons responded most strongly to each bird's own song with precisely timed spiking activity. In contrast, we observed a complete lack of song responsivity in both juvenile and adult AId, even though this region receives song-responsive inputs. A surprisingly large proportion of sites in RA cup of both juveniles and adults did not respond to song playback, and responsive sites showed little evidence of song selectivity. NEW & NOTEWORTHY Motor skill learning entails changes in selectivity for behaviorally relevant stimuli across cortical regions, yet the neural representation of these stimuli remains understudied. We investigated how information important for vocal learning in zebra finches is represented in regions analogous to infragranular layers of motor and auditory cortices during vs. after the developmentally regulated learning period. The results provide insight into how neurons in higher level stages of cortical processing represent stimuli important for motor skill learning.

Neural activity in cortico-basal ganglia circuits of juvenile songbirds encodes performance during goal-directed learning.

Cortico-basal ganglia circuits are thought to mediate goal-directed learning by a process of outcome evaluation to gradually select appropriate motor actions. We investigated spiking activity in core and shell subregions of the cortical nucleus LMAN during development as juvenile zebra finches are actively engaged in evaluating feedback of self-generated behavior in relation to their memorized tutor song (the goal). Spiking patterns of single neurons in both core and shell subregions during singing correlated with acoustic similarity to tutor syllables, suggesting a process of outcome evaluation. Both core and shell neurons encoded tutor similarity via either increases or decreases in firing rate, although only shell neurons showed a significant association at the population level. Tutor similarity predicted firing rates most strongly during early stages of learning, and shell but not core neurons showed decreases in response variability across development, suggesting that the activity of shell neurons reflects the progression of learning.

Cortical inter-hemispheric circuits for multimodal vocal learning in songbirds.

Vocal learning in songbirds and humans is strongly influenced by social interactions based on sensory inputs from several modalities. Songbird vocal learning is mediated by cortico-basal ganglia circuits that include the SHELL region of lateral magnocellular nucleus of the anterior nidopallium (LMAN), but little is known concerning neural pathways that could integrate multimodal sensory information with SHELL circuitry. In addition, cortical pathways that mediate the precise coordination between hemispheres required for song production have been little studied. In order to identify candidate mechanisms for multimodal sensory integration and bilateral coordination for vocal learning in zebra finches, we investigated the anatomical organization of two regions that receive input from SHELL: the dorsal caudolateral nidopallium (dNCLSHELL ) and a region within the ventral arcopallium (Av). Anterograde and retrograde tracing experiments revealed a topographically organized inter-hemispheric circuit: SHELL and dNCLSHELL , as well as adjacent nidopallial areas, send axonal projections to ipsilateral Av; Av in turn projects to contralateral SHELL, dNCLSHELL , and regions of nidopallium adjacent to each. Av on each side also projects directly to contralateral Av. dNCLSHELL and Av each integrate inputs from ipsilateral SHELL with inputs from sensory regions in surrounding nidopallium, suggesting that they function to integrate multimodal sensory information with song-related responses within LMAN-SHELL during vocal learning. Av projections share this integrated information from the ipsilateral hemisphere with contralateral sensory and song-learning regions. Our results suggest that the inter-hemispheric pathway through Av may function to integrate multimodal sensory feedback with vocal-learning circuitry and coordinate bilateral vocal behavior.

Development of neural responsivity to vocal sounds in higher level auditory cortex of songbirds.

Like humans, songbirds learn vocal sounds from "tutors" during a sensitive period of development. Vocal learning in songbirds therefore provides a powerful model system for investigating neural mechanisms by which memories of learned vocal sounds are stored. This study examined whether NCM (caudo-medial nidopallium), a region of higher level auditory cortex in songbirds, serves as a locus where a neural memory of tutor sounds is acquired during early stages of vocal learning. NCM neurons respond well to complex auditory stimuli, and evoked activity in many NCM neurons habituates such that the response to a stimulus that is heard repeatedly decreases to approximately one-half its original level (stimulus-specific adaptation). The rate of neural habituation serves as an index of familiarity, being low for familiar sounds, but high for novel sounds. We found that response strength across different song stimuli was higher in NCM neurons of adult zebra finches than in juveniles, and that only adult NCM responded selectively to tutor song. The rate of habituation across both tutor song and novel conspecific songs was lower in adult than in juvenile NCM, indicating higher familiarity and a more persistent response to song stimuli in adults. In juvenile birds that have memorized tutor vocal sounds, neural habituation was higher for tutor song than for a familiar conspecific song. This unexpected result suggests that the response to tutor song in NCM at this age may be subject to top-down influences that maintain the tutor song as a salient stimulus, despite its high level of familiarity.

Neural representation of a target auditory memory in a cortico-basal ganglia pathway.

Vocal learning in songbirds, like speech acquisition in humans, entails a period of sensorimotor integration during which vocalizations are evaluated via auditory feedback and progressively refined to achieve an imitation of memorized vocal sounds. This process requires the brain to compare feedback of current vocal behavior to a memory of target vocal sounds. We report the discovery of two distinct populations of neurons in a cortico-basal ganglia circuit of juvenile songbirds (zebra finches, Taeniopygia guttata) during vocal learning: (1) one in which neurons are selectively tuned to memorized sounds and (2) another in which neurons are selectively tuned to self-produced vocalizations. These results suggest that neurons tuned to learned vocal sounds encode a memory of those target sounds, whereas neurons tuned to self-produced vocalizations encode a representation of current vocal sounds. The presence of neurons tuned to memorized sounds is limited to early stages of sensorimotor integration: after learning, the incidence of neurons encoding memorized vocal sounds was greatly diminished. In contrast to this circuit, neurons known to drive vocal behavior through a parallel cortico-basal ganglia pathway show little selective tuning until late in learning. One interpretation of these data is that representations of current and target vocal sounds in the shell circuit are used to compare ongoing patterns of vocal feedback to memorized sounds, whereas the parallel core circuit has a motor-related role in learning. Such a functional subdivision is similar to mammalian cortico-basal ganglia pathways in which associative-limbic circuits mediate goal-directed responses, whereas sensorimotor circuits support motor aspects of learning.

Afferents from vocal motor and respiratory effectors are recruited during vocal production in juvenile songbirds.

Learned behaviors require coordination of diverse sensory inputs with motivational and motor systems. Although mechanisms underlying vocal learning in songbirds have focused primarily on auditory inputs, it is likely that sensory inputs from vocal effectors also provide essential feedback. We investigated the role of somatosensory and respiratory inputs from vocal effectors of juvenile zebra finches (Taeniopygia guttata) during the stage of sensorimotor integration when they are learning to imitate a previously memorized tutor song. We report that song production induced expression of the immediate early gene product Fos in trigeminal regions that receive hypoglossal afferents from the tongue and syrinx (the main vocal organ). Furthermore, unilateral lesion of hypoglossal afferents greatly diminished singing-induced Fos expression on the side ipsilateral to the lesion, but not on the intact control side. In addition, unilateral lesion of the vagus reduced Fos expression in the ipsilateral nucleus of the solitary tract in singing birds. Lesion of the hypoglossal nerve to the syrinx greatly disrupted vocal behavior, whereas lesion of the hypoglossal nerve to the tongue exerted no obvious disruption and lesions of the vagus caused some alterations to song behavior. These results provide the first functional evidence that somatosensory and respiratory feedback from peripheral effectors is activated during vocal production and conveyed to brainstem regions. Such feedback is likely to play an important role in vocal learning during sensorimotor integration in juvenile birds and in maintaining stereotyped vocal behavior in adults.

Morphology of axonal projections from the high vocal center to vocal motor cortex in songbirds.

Only birds that learn complex vocalizations have telencephalic brain regions that control vocal learning and production, including HVC (high vocal center), a cortical nucleus that encodes vocal motor output in adult songbirds. HVC projects to RA (robust nucleus of the arcopallium), a nucleus in motor cortex that in turn projects topographically onto hindbrain neurons innervating vocal muscles. Individual neurons projecting from HVC to RA (HVC(RA) ) fire sparsely to drive RA activity during song production. To advance understanding of how individual HVC neurons encode production of learned vocalizations, we reconstructed single HVC axons innervating RA in adult male zebra finches. Individual HVC(RA) axons were not topographically organized within RA: 1) axon arbors of HVC cell bodies located near each other sent branches to different subregions of RA, and 2) branches of single HVC axons terminated in different locations within RA. HVC(RA) axons also had a simple, sparse morphology, suggesting that a single HVC neuron activates a limited population of postsynaptic RA neurons. These morphological data are consistent with previous work showing that single HVC(RA) neurons burst sparsely for a brief period of time during the production of a song, indicating that ensembles of HVC(RA) neurons fire simultaneously to drive small temporal segments of song behavior. We also examined the morphology of axons projecting from HVC to RA cup, a region surrounding RA that receives input from auditory cortex. Axons projecting to RA cup also sent some branches into RA, suggesting direct integration between the sensory and motor circuits for song control.

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 experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches.

Experience-dependent changes in neural connectivity underlie developmental learning and result in life-long changes in behavior. In songbirds axons from the cortical region LMAN(core) (core region of lateral magnocellular nucleus of anterior nidopallium) convey the output of a basal ganglia circuit necessary for song learning to vocal motor cortex [robust nucleus of the arcopallium (RA)]. This axonal projection undergoes remodeling during the sensitive period for learning to achieve topographic organization. To examine how auditory experience instructs the development of connectivity in this pathway, we compared the morphology of individual LMAN(core)→RA axon arbors in normal juvenile songbirds to those raised in white noise. The spatial extent of axon arbors decreased during the first week of vocal learning, even in the absence of normal auditory experience. During the second week of vocal learning axon arbors of normal birds showed a loss of branches and varicosities; in contrast, experience-deprived birds showed no reduction in branches or varicosities and maintained some arbors in the wrong topographic location. Thus both experience-independent and experience-dependent processes are necessary to establish topographic organization in juvenile birds, which may allow birds to modify their vocal output in a directed manner and match their vocalizations to a tutor song. Many LMAN(core) axons of juvenile birds, but not adults, extended branches into dorsal arcopallium (Ad), a region adjacent to RA that is part of a parallel basal ganglia pathway also necessary for vocal learning. This transient projection provides a point of integration between the two basal ganglia pathways, suggesting that these branches convey corollary discharge signals as birds are actively engaged in learning.

Conjunction of vocal production and perception regulates expression of the immediate early gene ZENK in a novel cortical region of songbirds.

The cortical nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium) provides the output of a basal ganglia pathway that is necessary for acquisition of learned vocal behavior during development in songbirds. LMAN is composed of two subregions, a core and a surrounding shell, that give rise to independent pathways that traverse the forebrain in parallel. The LMAN(shell) pathway forms a recurrent loop that includes a cortical region, the dorsal region of the caudolateral nidopallium (dNCL), hitherto unknown to be involved with learned vocal behavior. Here we show that vocal production strongly induces the IEG product ZENK in dNCL of zebra finches. Hearing tutor song while singing is more effective at inducing expression in dNCL of juvenile birds during the auditory-motor integration stage of vocal learning than is hearing conspecific song. In contrast, hearing conspecific song is relatively more effective at inducing expression in adult birds, regardless of whether they are producing song. Furthermore, ZENK+ neurons in dNCL include projection neurons that are part of the LMAN(shell) recurrent loop and a high proportion of dNCL projection neurons express ZENK in singing juvenile birds that hear tutor song. Thus juvenile birds that are actively refining their vocal pattern to imitate a tutor song show high levels of ZENK induction in dNCL neurons when they are singing while hearing the song of their tutor and low levels when they hear a novel conspecific. This pattern indicates that dNCL is a novel brain region involved with vocal learning and that its function is developmentally regulated.

Parallel pathways for vocal learning in basal ganglia of songbirds.

The cortical nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium) provides the output of a basal ganglia pathway that is necessary for vocal learning in juvenile songbirds. The shell subregion of LMAN (LMAN(shell)) gives rise to recurrent loops that may subserve specific learning-related functions. We found that lesions in the LMAN(shell) pathway caused no immediate disruption of vocal behavior, but prevented the development of stable vocal sequences and the ability to imitate vocal sounds.

Silent synapses in a thalamo-cortical circuit necessary for song learning in zebra finches.

Developmental changes in synaptic properties may act to limit neural and behavioral plasticity associated with sensitive periods. This study characterized synaptic maturation in a glutamatergic thalamo-cortical pathway that is necessary for vocal learning in songbirds. Lesions of the projection from medial dorsolateral nucleus of the thalamus (DLM) to the cortical nucleus lateral magnocellular nucleus of the anterior nidopallium (LMAN) greatly disrupt song behavior in juvenile birds during early stages of vocal learning. However, such lesions lose the ability to disrupt vocal behavior in normal birds at 60-70 days of age, around the time that selective auditory tuning for each bird's own song (BOS) emerges in LMAN neurons. This pattern has suggested that LMAN is involved in processing song-related information and evaluating the degree to which vocal motor output matches the tutor song to be learned. Analysis of reversed excitatory postsynaptic currents at DLM-->LMAN synapses in in vitro slice preparations revealed a pronounced N-methyl-D-aspartate receptor (NMDAR)-mediated component in both juvenile and adult cells with no developmental decrease in the relative contribution of NMDARs to synaptic transmission. However, the synaptic failure rate at DLM-->LMAN synapses in juvenile males during the sensitive period for song learning was significantly lower at depolarized potentials than at hyperpolarized potentials. In contrast, the failure rate at DLM-->LMAN synapses did not differ at hyper- versus depolarized holding potentials in adult males that had completed the acquisition of a stereotyped song. This pattern indicates that juvenile cells have a higher incidence of silent (NMDAR-only) synapses, which are postsynaptically silent at hyperpolarized potentials due to the voltage-dependent gating of NMDARs. Thus the decreased involvement of the LMAN pathway in vocal behavior is mirrored by a decline in the incidence of silent synapses but not by changes in the relative number of NMDA and AMPA receptors at DLM-->LMAN synapses. These findings suggest that a developmental decrease in silent synapses within LMAN may represent a neural correlate of behavioral plasticity during song learning.

Timing and prediction the code from basal ganglia to thalamus.

When is an inhibitory synapse not inhibitory? In this issue of Neuron, Person and Perkel demonstrate that thalamic neurons can translate extrinsic GABAergic input from the basal ganglia into highly precise patterns of sustained spiking in a circuit that is essential for vocal learning in songbirds. Postinhibitory rebound serves as a mechanism that preserves precise spike timing information, enabling reliable propagation of activity throughout this pathway. The results have broad implications for basic mechanisms of functional processing in both thalamus and basal ganglia and serve to increase our understanding of how acoustic units of vocal sounds are transformed into motor gestures during the sensitive period for song learning.

Neurogenesis within the juvenile zebra finch telencephalic ventricular zone: a map of proliferative activity.

Localized regions of increased cellular proliferation within the ventricular zone (VZ) of juvenile male songbirds may contain progenitor cells that give rise to song-control neurons and, thereby, contribute to the construction of brain areas important for song learning. The purpose of this study was to examine levels of cell division throughout the telencephalic VZ of juvenile birds. A single pulse of [(3)H]thymidine was administered to 30-day male and female zebra finches, and the birds were killed 2 hours later. The VZ was divided into segments throughout the entire anterior-posterior and dorsal-ventral neuraxes, and levels of thymidine labeling were measured within each subdivision. By subdividing the VZ into segments, we were able to construct a "map" of proliferation throughout the telencephalic VZ, thereby allowing us to compare levels of mitotic activity within corresponding locations of the VZ between males and females. Our map revealed two major findings: (1) proliferation in both juvenile males and females was spatially differentiated throughout the VZ, suggesting that mitotic activity is differentially regulated across the neuraxis; (2) sex differences in proliferation were present in 30-day-old birds, but were highly restricted. The most robust sexual dimorphism occurred within the ventral aspect of the VZ at rostral levels of the song-control nucleus Area X, with males demonstrating an increased number of dividing cells compared with females. This result raises the possibility that Area X neurons in males are derived from committed progenitors within the adjacent VZ in close proximity to this nucleus.

Developmental regulation of basal ganglia circuitry during the sensitive period for vocal learning in songbirds.

A hallmark of sensitive periods of development is an enhanced capacity for learning, such that experience exerts a profound effect on the brain resulting in the establishment of behaviors and underlying neural circuitry that can last a lifetime. Songbirds, like humans, have a sensitive period for vocal learning: they acquire the sounds used for vocal communication during a restricted period of development. In principle, any organism that undertakes vocal learning is faced with the same challenge: to form some representation of target vocal sounds based on auditory experience, and then to translate that auditory target into a motor program that reproduces the sound. Both birds and humans achieve this translation by using auditory (and other) feedback resulting from incipient vocalizations ("babbling" in humans, "subsong" in birds) to adjust motor commands until vocal output produces a good copy of the target sounds. Similarities between vocal learning in birds and humans suggest that many aspects of the learning process have evolved to meet demands imposed by vocal communication. Thus songbirds provide a valuable animal model in which to study the physiological basis of learned vocal communication and the nature of sensitive periods in general. In this article, I describe aspects of both behavioral and neural frameworks that currently inform our thinking about mechanisms underlying vocal learning and behavior in songbirds, and highlight ideas that may need re-examination.

Limits on reacquisition of song in adult zebra finches exposed to white noise.

Zebra finches (Taeniopygia guttata) learn a specific song pattern during a sensitive period of development, after which song changes little or not at all. However, recent studies have demonstrated substantial behavioral plasticity in song behavior during adulthood under a range of conditions. The current experiment examined song behavior of adult zebra finches temporarily deprived of auditory feedback by chronic exposure to loud white noise (WN). Long-term exposure to continuous WN resulted in disruption of song similar to that observed after deafening. When auditory feedback was restored by discontinuing WN, birds were either tutored using tape-recorded playback or housed with adult conspecific tutors. No evidence of learning new tutor syllables was observed, and recovery of pre-WN song patterns was very limited after restoration of hearing. However, many birds did reacquire some aspects of their pretreatment song, suggesting an adult form of learning that may retain some of the initial aspects of sensorimotor acquisition of song in which vocalizations are shaped to match a stored template representation. The failure to learn novel song elements and the modest degree of recovery observed overall suggest a limit on plasticity in adult birds that have acquired species-typical song patterns and may reflect an important species difference between zebra finches and Bengalese finches.