Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei

Young male canaries become sexually mature in late winter, 8-12 months after hatching. During the months between hatching and sexual maturity they develop adult song. The successive stages in the development of adult song are subsong, plastic song, and stable or full song. Once stable song is achieved it lasts for the duration of the breeding season. After the end of the breeding season there is a recurrence of song instability during summer and early fall. This plastic song is followed, once more, by stable song. New song syllables are added to the song of adult male canaries and some of the earlier syllables disappear. The song repertoire sung at 2 years of age is substantially larger, and different, from that sung during the first breeding season, when the birds were 1 year old. A comparable change occurs between the second and third breeding seasons. Most of the syllables acquired by adult males are formed during the summer-fall period of song instability. Developmental and seasonal changes in song are accompanied by anatomical changes in two forebrain nuclei known to be involved in song control, the hyperstriatum ventralis, pars caudalis (HVc), and the robust nucleus of the archistriatum (RA). HVc and RA grow during the subsong and plastic song periods of song development. These nuclei reach adult size by the time stable adult song is first produced, and retain this size during the breeding season. However, the size of HVc and RA diminishes by late summer, when it becomes comparable to that of a 3- to 4-month-old bird. This reduction in size is temporary and has been corrected by the following breeding season. It is suggested that these seasonal changes in volume reflect circuit changes which are under hormonal control, and that these changes are related to processes of learning and, possibly, forgetting. Despite earlier reports of left hemispheric dominance in canary song production, we failed to find any evidence of right-left systematic differences in the size of HVc and RA during development or in adulthood. Various hypotheses relating song learning to changes in the underlying anatomy are offered.     

Dissociation between extension of the sensitive period for avian vocal learning and dendritic spine loss in the song nucleus lMAN

Several instances of early learning coincide with significant rearrangements of neural connections in regions contributing to these behaviors. In fact developmentally restricted learning may be constrained temporally by the opportunity for experience to selectively maintain appropriate synapses amidst the elimination of exuberant connections. Consistent with this notion, during the normal sensitive period for vocal learning in zebra finches (Taenopygia guttata), there is a decline in the density of dendritic spines within a region essential for song development, the lateral magnocellular nucleus of the anterior nidopallium (lMAN). Moreover, in birds isolated from conspecific song shortly after hatching, both the closure of the sensitive period for vocal learning and the pruning of spines from lMAN neurons is delayed. Here, we employed a more subtle form of deprivation to delay the close of the sensitive period for song learning, and found that late song learning occurred without obvious alterations in the pruning of dendritic spines on lMAN neurons. At posthatch day (PHD) 65 (beyond the end of the normal sensitive period for song memorization in zebra finches), birds isolated from song beginning on PHD30 did not differ from normally reared birds in measures of dendritic spine density on Golgi-Cox stained lMAN neurons. Moreover, tutor exposure from PHD65 to 90 did not increase spine elimination in these isolates (who memorized new song material) relative to controls (who did not). Thus, we conclude that the extent of normally occurring lMAN spine loss is not sufficient to account for the timing of the sensitive period for zebra finch song learning.     

Left-side dominance for song discrimination in Bengalese finches (Lonchura striata var. domestica)

Male Bengalese finches are left-side dominant for the motor control of song in the sensorimotor nucleus (the high vocal center, or HVc) of the telencephalon. We examined whether perceptual discrimination of songs might also be lateralized in this species. Twelve male Bengalese finches were trained by operant conditioning to discriminate between a Bengalese finch song and a zebra finch song. Before training, the left HVc was lesioned in four birds and the right HVc was lesioned in four other birds. The remaining four birds were used as controls without surgery. Birds with a left HVc lesion required significantly more time to learn to discriminate between the two songs than did birds with a right HVc lesion or intact control birds. These results suggest that the left HVc is not only dominant for the motor control of song, but also for the perceptual discrimination of song. Accepted after revision: 11 September 2001 Electronic Publication     

Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch

Area X, a large sexually dimorphic nucleus in the avian ventral forebrain, is part of a highly discrete system of interconnected nuclei that have been implicated in either song learning or adult song production. Previously, this nucleus has been included in the song system because of its substantial connections with other vocal control nuclei, and because its volume is positively correlated with the capacity for song. In order to directly assess the role of Area X in song behavior, this nucleus was bilaterally lesioned in both juvenile and adult zebra finches, using ibotenic acid. We report here that lesioning Area X disrupts normal song development in juvenile birds, but does not affect the production of stereotyped song by adult birds. Although juvenile-lesioned birds were consistently judged as being in earlier stages of vocal development than age-matched controls, they continued to produce normal song-like vocalizations. Thus, unlike the lateral magnocellular nucleus of the anterior neostriatum, another avian forebrain nucleus implicated in song learning, Area X does not seem to be necessary for sustaining production of juvenile song. Rather, the behavioral results suggest Area X is important for either the acquisition of a song model or the improvement of song through vocal practice.     

Influence of social conditions in song sharing in the adult canary

In songbirds, experience of social and environmental cues during a discrete period after birth may dramatically influence song learning. In the canary, the ability to learn new songs is assumed to persist throughout life. The aim of the present study was to investigate whether social context could guide changes in adult song. Three groups of canaries were kept in different social and temporal conditions. Results showed that the multiple hierarchical levels of the canary song structure were affected by social environment: songs of males housed together for 2 years were more similar than those of males that spent the same time in individual cages in regard to acoustic parameters, syllable repertoire and repertoire of sequences of two-syllable types. However, social housing did not result in the emergence of a group-specific vocal signature within songs. In conclusion, these results suggested that under the influence of social factors, a copying process could allow adult canaries to adjust, at least in part, their songs to those of other individuals.     

Sexual dimorphism of auditory activity in the zebra finch song system

While the tracheosyringeal motor neurons of anesthetized male zebra finches fire in response to acoustic stimuli, the same motor neurons in females show no such response. Females masculinized by estradiol implants on Days 1 or 2 after hatching may develop auditory responses in their tracheosyringeal motor neurons; the presence of the response is directly related to the degree of masculinization of the estradiol-treated females' telencephalic song centers. In male zebra finches, neurons in HVc (Hyperstriatum Ventrale pars caudalis) respond to sound, and the HVc is necessary for the tracheosyringeal auditory response. Multiunit auditory activity was demonstrated in the HVc of female zebra finches. A single 20-microA pulse delivered to the male HVc elicits a large volley in the tracheosyringeal nerve; microstimulating the female HVc does not evoke a response in the motor nerve. This failure of both auditory and HVc stimulation to elicit a response in the female tracheosyringeal nerve is attributed to the lack of a functional HVc-nucleus Robustus Archistriatalis projection in females. If, as has been suggested, the tracheosyringeal auditory response may be important for the processing of song, female zebra finches might not process song in the same manner as do males.     

Altered daylength affects dendritic structure in a song-related brain region in red-winged blackbirds.

Substantial neural and behavioral plasticity occurs in the avian song system in adulthood. Changes in the volume of one of the song control nuclei, robustus archistriatalis (RA), have been associated with seasonal changes in singing behavior in adult canaries (Serinus canarius) and red-winged blackbirds (Agelaius phoeniceus). The present work assessed the effects of changed daylength on dendritic morphology in RA in adult male red-winged blackbirds. Brains from hand-reared red-winged blackbirds maintained on long days or long days followed by short days were stained with a Golgi-Cox procedure. Dendritic morphology and spine density of type IV neurons from nucleus RA were compared between long and short day birds. Neurons from short day birds have smaller dendritic fields than neurons from long day birds, with the difference greatest for distal dendrites. In addition, the density of dendritic spines is significantly smaller for neurons from short day birds. Together, these changes result in the loss of approximately 40% of the spines on this neuron class. In previous work in adult female canaries, external testosterone administration has been shown to be associated with increases in dendritic field size and synapse number. The similarity of the neuronal changes in RA that are associated with the two sorts of manipulations suggest that some consequences of altered daylength are mediated by changes in the levels of gonadal steroids.     

Effects of lesions of the central nucleus of the anterior archistriatum on contact call and warble song production in the budgerigar (Melopsittacus undulatus)

We studied the effects of both unilateral and bilateral lesions of the central nucleus of the anterior archistriatum (AAc) on the production of contact calls and warble song in adult male and female budgerigars. Birds were sorted into three experimental groups based on the percentage of AAc destroyed and whether lesions were unilateral or bilateral. The experimental groups were Unilateral Lesion (N = 8), Partial Bilateral Lesion (N = 5), and Bilateral Lesion birds (N = 12). Each group contained both sexes. Unilateral lesions had no demonstrable effects on contact call or warble song production. Bilateral lesions resulted in immediate and permanent disruption of all learned temporal and spectral characteristics of contact calls, although call initiation was not dependent on the AAc. Partial bilateral lesion effects varied with lesion size and location. At least 20-30% sparing of the AAc, including sparing portions of both the dorsal (AAcd) and ventral (AAcv) subdivisions on the same side of the brain, is necessary for production of prelesion contact call patterns. Warble song was absent in birds with complete bilateral destruction. Two birds with large yet incomplete lesions of the AAc sang after surgery, although the warble song of these birds was extremely impoverished and contained only a few of the typical warble song elements. Lesion results indicate that the AAc mediates the production of learned vocal features in male and female budgerigars, with each hemisphere capable of supporting a normal vocal repertoire.     

Enlargement of Neuronal Somata in the LMAN Coincides with the Onset of Sensorimotor Learning for Song

The lateral magnocellular nucleus of the anterior neostriatum (LMAN) in the zebra finch (Taeniopygia guttata) has been shown to play a developmentally restricted role that is essential during song-learning processes. Dendritic spine frequencies and synapse numbers in LMAN have been reported to decline in males during early vocal motor learning and thereafter, but not in females, who do not sing. Nissl staining has shown the LMAN volume to be very similar in both sexes, however. To gain more insight into the development of sex-specific differences in LMAN, the size of neuronal somata and cell nuclei were analyzed in 1-μm semithin sections. Cell somata and nuclei were similar in males and females during the initial phases of sensory memory formation for song, but during early vocal motor learning cell size increased in males and decreased in females. Sex differences in neuronal somata size were present at 50 days and remained throughout life. This sex difference may be indicative of a difference in protein biosynthesis in LMAN, arising as a consequence of vocal learning in males.     

Behavioral consequences of song learning: Discrimination of song types by male white-crowned sparrows

The functional significance of learned population differences in male song in the white-crowned sparrow was explored in natural populations using playback tests. Laboratory results have shown that learning of the population-specific song seems to take place in early life and is strongly dependent upon the nature of the auditory experience at that time. However, the varied results of recent studies make it difficult to reach a confident conclusion about the ecological functions of song learning. The present research took advantage of naturally occurring variation in the differences between songs of adjacent populations to determine a function relating degree of difference in song to intensity of territorial singing elicited. Applying a typological evaluation of syllable structure to the four segments of the song allowed a crude quantitative ranking of the differences between local songs and playback stimuli. These results, together with those of other studies, suggest a unimodal aggressive response function of males to songs of other males. A maximum response to songs slightly different from the local song environment suggests that male exclusion based upon acquired song components may contribute to the maintenance of discrete and stable song dialects.     

Dopamine regulation of human speech and bird song: a critical review

To understand the neural basis of human speech control, extensive research has been done using a variety of methodologies in a range of experimental models. Nevertheless, several critical questions about learned vocal motor control still remain open. One of them is the mechanism(s) by which neurotransmitters, such as dopamine, modulate speech and song production. In this review, we bring together the two fields of investigations of dopamine action on voice control in humans and songbirds, who share similar behavioral and neural mechanisms for speech and song production. While human studies investigating the role of dopamine in speech control are limited to reports in neurological patients, research on dopaminergic modulation of bird song control has recently expanded our views on how this system might be organized. We discuss the parallels between bird song and human speech from the perspective of dopaminergic control as well as outline important differences between these species.     

Social metrics of song learning

Five metrics of song learning are described for brown-headed cowbirds (Molothrus ater). The intent of these metrics is to capture not only the behavior of the song learner but the social context in which song learning occurs. Playback procedures, observations of mating, and acoustic and functional assessment of song content are combined to yield measures of song potency, functional validity, social dynamics, vocal flexibility, and social reactivity. Taken as a whole, the results revealed by these metrics indicate that males learn to be effective singers by attending to the social consequences of their behavior.     

Song repertoire development in male cowbirds (Molothrus ater): its relation to female assessment of song potency

Two studies were conducted to investigate the relation between the male cowbird's (Molothrus ater ater) development of a song repertoire and the female cowbird's assessment of song potency. Male development was assayed by vocal copying and female assessment by copulatory responsiveness to song playback. The results demonstrate that males do not copy most often the particular songs that females respond to most often. Whereas rank orderings of potency were highly correlated across two independent samples of playback females, male and female rank orderings were not significantly correlated. The data highlight the potential significance of social interactions between and across the sexes for repertoire development.     

Learning lyrics: To sing or not to sing?

According to common practice and oral tradition, learning verbal materials through song should facilitate word recall. In the present study, we provide evidence against this belief. In Experiment 1, 36 university students, half of them musicians, learned an unfamiliar song in three conditions. In the sung-sung condition, the song to be learned was sung, and the response was sung too. In the sung-spoken condition, the response was spoken. In the divided-spoken condition, the presented lyrics (accompanied by music) and the response were both spoken. Superior word recall in the sung-sung condition was predicted. However, fewer words were recalled when singing than when speaking. Furthermore, the mode of presentation, whether sung or spoken, had no influence on lyric recall, in either short- or long-term recall. In Experiment 2, singing was assessed with and without words. Altogether, the results indicate that the text and the melody of a song have separate representations in memory, making singing a dual task to perform, at least in the first steps of learning. Interestingly, musical training had little impact on performance, suggesting that vocal learning is a basic and widespread skill.     

Factors influencing song development in the white-crowned sparrow (Zonotrichia leucophrys)

Nestling white-crowned sparrows (Zonotrichia leucophrys nuttalli) were hand-reared in sound-isolation chambers under a variety of conditions. The songs of total isolates were compared with songs of birds tutored with song, and the number of inputs sufficient for a bird to produce a normal song was explored. The flexibility of the song learning system was investigated with a range of tape-recorded tutor songs: alien dialects, alien subspecies, alien species, alternating alien dialects, and an aberrant song. Adult songs were obtained for 40 males and 7 testosterone-injected females. All of the tutor songs could be learned. Also, some birds learned elements of an alien species' song. Birds tutored with two songs copied one or the other, were bilingual, or sang a hybrid of the two. No bird presented with fewer than 120 songs learned the tutor song; 2 birds tutored with 252 songs copied the tutor song. It is concluded that the song learning system is quite flexible, hat the results obtained with tape-tutors are very different from those with social tutors, and that there may be an interaction between total number of song inputs and the number presented on a single day. Some implications of these data for physiological mechanisms and the possible functional significance of the acquisition system are discussed.     

Common cues to emotion in the dynamic facial expressions of speech and song

Speech and song are universal forms of vocalization that may share aspects of emotional expression. Research has focused on parallels in acoustic features, overlooking facial cues to emotion. In three experiments, we compared moving facial expressions in speech and song. In Experiment 1, vocalists spoke and sang statements each with five emotions. Vocalists exhibited emotion-dependent movements of the eyebrows and lip corners that transcended speech–song differences. Vocalists’ jaw movements were coupled to their acoustic intensity, exhibiting differences across emotion and speech–song. Vocalists’ emotional movements extended beyond vocal sound to include large sustained expressions, suggesting a communicative function. In Experiment 2, viewers judged silent videos of vocalists’ facial expressions prior to, during, and following vocalization. Emotional intentions were identified accurately for movements during and after vocalization, suggesting that these movements support the acoustic message. Experiment 3 compared emotional identification in voice-only, face-only, and face-and-voice recordings. Emotion judgements for voice-only singing were poorly identified, yet were accurate for all other conditions, confirming that facial expressions conveyed emotion more accurately than the voice in song, yet were equivalent in speech. Collectively, these findings highlight broad commonalities in the facial cues to emotion in speech and song, yet highlight differences in perception and acoustic-motor production.     

The origins of vocal learning: New sounds, new circuits, new cells

We do not know how vocal learning came to be, but it is such a salient trait in human evolution that many have tried to imagine it. In primates this is difficult because we are the only species known to possess this skill. Songbirds provide a richer and independent set of data. I use comparative data and ask broad questions: How does vocal learning emerge during ontogeny? In what contexts? What are its benefits? How did it evolve from unlearned vocal signals? How was brain anatomy altered to enable vocal learning? What is the relation of vocal learning to adult neurogenesis? No one has described yet a circuit or set of circuits that can master vocal learning, but this knowledge may soon be within reach. Moreover, as we uncover how birds encode their learned song, we may also come closer to understanding how we encode our thoughts.     

Morphological changes in dendritic spines of Purkinje cells associated with motor learning

Experience-dependent changes of spine structure and number may contribute to long-term memory storage. Although several studies demonstrated structural spine plasticity following associative learning, there is limited evidence associating motor learning with alteration of spine morphology. Here, we investigated this issue in the cerebellar Purkinje cells using high voltage electron microscopy (HVEM). Adult rats were trained in an obstacle course, demanding significant motor coordination to complete. Control animals either traversed an obstacle-free runway or remained sedentary. Quantitative analysis of spine morphology showed that the density and length of dendritic spines along the distal dendrites of Purkinje cells were significantly increased in the rats that learned complex motor skills compared to active or inactive controls. Classification of spines into shape categories indicated that the increased spine density and length after motor learning was mainly attributable to an increase in thin spines. These findings suggest that motor learning induces structural spine plasticity in the cerebellar Purkinje neurons, which may play a crucial role in acquiring complex motor skills.     

Timbre control in zebra finch (Taeniopygia guttata) song syllables

Zebra finch (Taeniopygia guttata) song syllables often include harmonically related frequency components. These harmonics may be suppressed, and this differential emphasis varies between the syllables in a song and between individual birds' songs. These patterns of harmonic suppression are timbre. Individual syllables' patterns of harmonic suppression are constant with adult males' songs. Young males that imitate the songs of older males also imitate their patterns of harmonic suppression. Syringeal denervation distorts these patterns, which suggests that they are produced through active control of the vocal organ. The selective suppression and emphasis of some harmonics creates a great number of possible timbre variants for any one syllable. These add signal diversity to the limited array of frequency modulations and range of fundamental frequencies found in zebra finch song. Analyses of bird song that disregard timbre may overlook a feature that is important in vocal communication.     

Blockade of NMDA Receptors in the Anterior Forebrain Impairs Sensory Acquisition in the Zebra Finch (Poephila guttata)

Juvenile zebra finches (Poephila guttata) learn song in two stages: during sensory acquisition, they memorize the song of an adult tutor, and during sensorimotor learning, they alter their vocalizations to match the stored song model. Like many other forms of neural plasticity and memory formation, vocal learning in zebra finches is impaired by pharmacological blockade of NMDA receptors, but the relevant NMDA receptors have not yet been localized. During song development, one neural region that has been implicated specifically in song learning, the lMAN, exhibits an increased density of NMDA receptors as well as decreased binding affinity for the NMDA antagonist MK-801. To test the hypothesis that sensory acquisition requires activation of NMDA receptors in or near the lMAN we infused the NMDA receptor antagonist amino-5-phosphonopentanoic acid (AP5; 2.5 μg in 0.1 μl) directly into the anterior forebrain. Birds receiving AP5 infusions prior to each of 10 tutoring sessions copied significantly less of their tutor's song than did sham-operated birds, saline-infused birds, birds that received AP5 infusions on nontutoring days, or birds that received AP5 infusions into the cerebellum. Furthermore, infusions of AP5 in the anterior forebrain did not impair young birds’ ability to discriminate zebra finch from canary song. These findings are consistent with the hypothesis that NMDA receptor activation in the anterior forebrain is necessary for the memorization of song material during avian vocal learning. This is also the first report that song-related regions of the anterior forebrain contribute to sensory acquisition specifically.