Learning In Songbirds Research Articles

Birdsong.

Vocalizations used by birds for territory defense, mate attraction, or both are often referred to as a given species' song. Birdsong refers to the often complex vocalizations produced most frequently by males of species that are members of the songbird order (passeriformes). Unlike most species-typical vocalizations produced by nonhuman animals, some songbird vocalizations are learned. Studies of birdsong learning, production, and perception address issues of fundamental interest to psychologists and others interested in behavior and its physiological underpinnings and provide the basis for this review. This article highlights recent advances in knowledge as illustrations of the utility of birdsong as an arena for significant new developments in experimental psychology and behavioral neuroscience.

Circuits, hormones, and learning: vocal behavior in songbirds.

Species-typical vocal patterns subserve species identification and communication for individual organisms. Only a few groups of organisms learn the sounds used for vocal communication, including songbirds, humans, and cetaceans. Vocal learning in songbirds has come to serve as a model system for the study of brain-behavior relationships and neural mechanisms of learning and memory. Songbirds learn specific vocal patterns during a sensitive period of development via a complex assortment of neurobehavioral mechanisms. In many species of songbirds, the production of vocal behavior by adult males is used to defend territories and attract females, and both males and females must perceive vocal patterns and respond to them. In both juveniles and adults, specific types of auditory experience are necessary for initial song learning as well as the maintenance of stable song patterns. External sources of experience such as acoustic cues must be integrated with internal regulatory factors such as hormones, neurotransmitters, and cytokines for vocal patterns to be learned and produced. Thus, vocal behavior in songbirds is a culturally acquired trait that is regulated by multiple intrinsic as well as extrinsic factors. Here, we focus on functional relationships between circuitry and behavior in male songbirds. In that context, we consider in particular the influence of sex hormones on vocal behavior and its underlying circuitry, as well as the regulatory and functional mechanisms suggested by morphologic changes in the neural substrate for song control. We describe new data on the architecture of the song system that suggests strong similarities between the songbird vocal control system and neural circuits for memory, cognition, and use-dependent plasticity in the mammalian brain.

Functional organization of forebrain pathways for song production and perception.

This article reviews the organization of the forebrain nuclei of the avian song system. Particular emphasis is placed on recent physiologic recordings from awake behaving adult birds while they sing, call, and listen to broadcasts of acoustic stimuli. The neurons in the descending motor pathway (HVc and RA) are organized in a hierarchical arrangement of temporal units of song production, with HVc neurons representing syllables and RA neurons representing notes. The nuclei Uva and NIf, which are afferent to HVc, may help organize syllables into larger units of vocalization. HVc and RA are also active during production of all calls. The patterns of activity associated with calls differ between learned calls and those that are innately specified, and give insight into the interactions between the forebrain and midbrain during calling, as well as into the evolutionary origins of the song system. Neurons in Area X, the first part of the anterior forebrain pathway leading from HVc to RA, are also active during singing. Many HVc neurons are also auditory, exhibiting selectivity for learned acoustic parameters of the individual bird's own song (BOS). Similar auditory responses are also observed in RA and Area X in anesthetized birds. In contrast to HVc, however, auditory responses in RA are very weak or absent in awake birds under our experimental paradigm, but are uncovered when birds are anesthetized. Thus, the roles of both pathways beyond HVc in adult birds is under review. In particular, theories hypothesizing a role for the descending motor pathway (RA and below) in adult song perception do not appear to obtain. The data also suggest that the anterior forebrain pathway has a greater motor role than previously considered. We suggest that a major role of the anterior forebrain pathway is to resolve the timing mismatch between motor program readout and sensory feedback, thereby facilitating motor programming during birdsong learning. Pathways afferent to HVc may participate more in sensory acquisition and sensorimotor learning during song development than is commonly assumed.

Localized Changes in Immediate-Early Gene Regulation during Sensory and Motor Learning in Zebra Finches

A complex neural system controls birdsong learning, but its organization is not understood, nor is it known why learning only occurs during a critical period in adolescence. Here, we analyzed developmental regulation in zebra finches of zenk, an immediate-early gene (IEG) implicated in memory consolidation. Basal expression was elevated within auditory telencephalon (specifically, within the caudomedial neostriatum [NCM]) during song acquisition. Expression could be further induced by song playbacks 30 days after hatching but not at 20 days nor in juveniles reared in severe isolation. Singing itself induced zenk in song production nuclei, including Area X, even in adults. Within a compartment of the robust nucleus of the archistriatum (RA), however, this response dwindled as singing matured. These results suggest that the onset of sensory memory storage may be regulated in part at NCM, and motor plasticity may be regulated at RA.

The timing of song memorization differs in males and females: a new assay for avian vocal learning

We describe a new assay for measuring the acquisition phase of song learning in birds and compare it with the standard method of comparing a pupil's imitation to his tutor's song. Juvenile male and female white-crowned sparrows,Zonotrichia leucophrysgive call notes in response to playback of species-typical song. After 10-day periods of tape tutoring conducted in the first 50 days of life, subjects gave significantly more calls in response to tutor songs than to novel songs. An identical procedure conducted at a later age yielded a different result. Birds did not distinguish tutor from novel songs in winter, after the sensitive phase for song acquisition. Males gave significantly more calls to those tutor songs that they subsequently sang the next spring than to tutor songs they did not reproduce. Assuming that the call assay correlates with long-term storage of songs in females as it does in males, these results also indicate that the sensitive phase for song acquisition is shorter in females than in males of this species.

Anterior Forebrain Neurons Develop Selectivity by an Intermediate Stage of Birdsong Learning

Auditory neurons of the anterior forebrain (AF) in adult zebra finches are highly selective for the bird's own song (BOS): they respond more to BOS than to songs of other zebra finches (conspecifics) and to BOS played in reverse. In contrast, juvenile AF neurons are not selective at 30 d of age, responding equally well to all song stimuli. Both BOS and tutor song experience are required by juveniles for normal song learning and may produce the selective properties of adult neurons. Because such selectivity could subserve song learning, it is important to determine when it arises. Birds were therefore studied at an intermediate stage of learning, after substantial experience of both tutor song and their own developing (plastic) song. Extracellular single neuron recordings in 60-d-old zebra finches revealed that AF neurons had significant song and order selectivity for both tutor song and BOS (the bird's plastic song). The degree of BOS selectivity was less than that found in adults, as indicated in part by 60 d neurons that were sensitive to the local order within syllables but not yet to the global order of syllables within a song. When responses to BOS and tutor song were compared, most neurons preferred BOS, some preferred tutor song, and others responded equally to both stimuli. The latter type of neuron was not simply immature, because many of these neurons responded significantly more to BOS and tutor song than to conspecific and reverse songs. The selectivity of AF neurons at 60 d is markedly different from the unselective properties of neurons at 30 d and may function in vocal learning at this stage. Moreover, the selectivity for both BOS and tutor song raises the possibility that both aspects of the birds' sensory experience during learning are reflected in properties of AF neurons.

Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development

Auditory experience is critical for vocal learning in songbirds as in humans. Therefore, in a search for neural mechanisms for song learning and recognition, the auditory response properties of neurons in the anterior forebrain (AF) pathway of the songbird brain were investigated. This pathway plays an essential but poorly understood role during the period of song development when auditory feedback is most crucial. Single-unit recordings demonstrated that both the lateral magnocellular nucleus of the anterior neostriatum (LMAN) and Area X (X) contain auditory neurons in adult male finches. These neurons are strongly selective for both spectral and temporal properties of song; they respond more robustly to the bird's own song (BOS) than to songs of conspecific individuals, and they respond less well to the BOS if it is played in reverse. In addition, X neurons are more broadly responsive than LMAN neurons, suggesting that responses to song become progressively more refined along this pathway. Both X and LMAN of young male finches early in the process of song learning (30-45 d old) also contain song-responsive auditory neurons, but these juvenile neurons lack the song and order selectivity present in adult birds. The spectral and temporal selectivity of the adult AF auditory neurons therefore arises during development in neurons that are initially broadly song-responsive. These neurons provide one of the clearest examples of experience-dependent acquisition of complex stimulus selectivity. Moreover, the auditory properties of the AF circuit suggest that one of its functions may be to mediate the auditory learning and feedback so essential to song development.

Early deafening affects PKC activity during bird song learning

Early deafening affects PKC activity during bird song learning

1312 Early deafening affects PKC activity during bird song learning

1312 Early deafening affects PKC activity during bird song learning

Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains.

This study examined the distribution of the neuropeptides somatostatin (SS) and calcitonin gene-related peptide (CGRP) in forebrain and midbrain song-control nuclei of male versus female brains in adult zebra finches (Poephila guttata) using immunohistochemical techniques. Vocal learning in songbirds is controlled by an interconnected, highly-localized system of brain nuclei. Male zebra finches produce learned vocalizations, and females do not. This behavioral sexual dimorphism is reflected in a substantial difference in the size of these song-control nuclei: males have larger nuclei containing a greater number of neurons than do females. Interestingly, previous studies describing neurochemical aspects of the song-control system in other songbird species have not reported any obvious sex differences. However, the results of this study showed that the level of neuropeptide staining was substantially greater in telencephalic song-control nuclei of male brains compared to female brains in zebra finches. In some brain regions females lacked any apparent staining, whereas male brains were intensely labeled. In other cases the number of neurons and/or intensity of labeling were diminished in females relative to males. The telencephalic pattern of somatostatin labeling revealed a large number of SS-labeled somata in the magnocellular nucleus of the anterior neostriatum species that occupy habitats with different hydrodynamic conditions. (MAN), the high vocal center (HVC) and the robust nucleus of the archistriatum (RA) of males, whereas female song-control nuclei contained many fewer or no labeled cells in these regions. Area X of the striatum appeared to contain a slightly higher level of somatostatin immunoreactivity than surrounding striatum in males, but the region corresponding to Area X in females could not be distinguished from the rest of striatum. The telencephalic pattern of CGRP staining was less extensive than that seen for SS. In male brains the magnocellular core region of lateral MAN contained many darkly labeled neurons, and RA was stained by a dense field of anterograde terminal label. Well labeled somata were also seen in medial MAN of males, but HVC was devoid of immunoreactivity. Area X in male brains contained a light field of terminal immunoreactivity. The pattern of labeling seen in males indicates that CGRP acts selectively as a neuromodulator along the efferent projection from lateral MAN to RA and Area X but not in the HVC-to-RA pathway. No telencephalic song-control nuclei in female brains contained CGRP staining. Although some diencephalic and midbrain nuclei contained well-labeled somata or fibers with either or both neuropeptides, there was little or no evidence of a sex difference in neuropeptide expression in these regions. This latter finding suggests that the greater anatomical specialization seen in cortical regions of songbirds compared to those regions in non-oscine species is accompanied by a greater neurochemical differentiation, whereas thalamic and midbrain regions may be more conserved across sex as well as species. These findings indicate that male neurons produce high levels of somatostatin and calcitonin gene-related peptide in major telencephalic vocal-control regions in zebra finches, whereas female neurons produce less or none at all. These dramatic neurochemical sex differences may be directly related to production of learned vocalizations in males, as well as to other aspects of song behavior and courtship.

Discontinuous and incremental processes in the song learning of birds: evidence for a primer effect

Studies on the song learning in birds revealed a puzzling property of the acquisition system: Stimulus memorization becomes effective after remarkably few exposures, but nevertheless shows a relationship to the frequency of exposure to learning stimuli. This raises questions on the amount of learning that will occur during a given exposure to song. To examine this issue, we tutored handraised fledgling nightingales (Luscinia megarhynchos) with song strings, in which the serial succession of species-typical master songs was altered upon subsequent exposures. The sequencing of imitations obtained from the birds' adult singing revealed the following results: (1) A single exposure was sufficient for subjects to acquire serial information on song-type sequencing. (2) The first exposure to a master string played a key role for this accomplishment. (3) Nevertheless, the acquisition of serial information improved with increasing exposure frequency of master strings. (4) The acquisition of song patterns was not impaired by a non-regular presentation of master song-types. With respect to the particular salience of the first exposure for sequence memorization, we termed the phenomenon ‘primer effect’. The findings suggest that stimulus acquisition during perceptual song learning is mediated by a discontinuous process. Once acquired, information is then consolidated gradually, i.e. through an incremental process.

Objective analysis of song learning in birds: Toward automated techniques.

It is demonstrated that indigo buntings sing bouts of ‘‘adult plastic’’ songs (APS) distinct from stereotyped songs (SS). Some distinguishing characteristics of APS include syllables of variable morphology and syllables not present in SS. The hypothesis that APS may play a role in adult song learning is tested by monitoring socially paired males housed together. Some yearlings changed their SS to more closely match their tutors’ SS, by replacing syllables or inserting new syllables. New syllables were developed in APS through transformation and combination of morphologically similar existing syllables, and syllables were transferred from APS into SS. To address the limitations of manual scoring of spectrographs, dynamic time warping (DTW) for template‐based automated analysis of continuous recordings of birdsongs was evaluated. With laboratory recordings, the DTW algorithm employed identified syllables and syllable boundaries of SS and calls of indigo bunting and zebra finch with greater than 97% accuracy. APS constituents were identified with approximately 84% accuracy. Under these restricted recording conditions, DTW has general applicability to objective analysis of birdsongs, and dramatically decreases the effort required. Application of hybrid hidden Markov models may improve the performance for variable vocalizations such as APS, and under noisy conditions of field recordings.

Song displays, song dialects, and lek mating systems in hummingbirds.

Males of some hummingbirds, including Colibri (violet‐ears), congregate and display from traditional areas, leks, to attract mates. Hummingbirds use a vocal display. Males on a lek share the same song, i.e., nearest neighbors share song; males on distant, acoustically isolated, leks have different songs, i.e., there are dialects. Dialects have been used as evidence for song learning in birds, and, although song learning is usually ascribed to oscines and parrots, hummingbirds share vocal organ (syrinx) structures with them consistent with song learning ability. Digital spectrogram cross correlation was used to objectively determine degree of song similarity; this statistic was used in cluster analysis to describe relationships between birds and with the Mantel method to test hypotheses about associations. Further, males of a lek deliver their song cooperatively, i.e., without interference. The resultant is a lek signal that, from a distance, sounds as one song. If, as in other cooperative lekking systems,...

Regressive development in neuronal structure during song learning in birds

We investigated the development of spiny neurons in the lateral magnocellular nucleus of the anterior neostriatum before, during, and after song learning in male zebra finches (Taeniopygia guttata). The frequency of dendritic spines, dendritic field size, and branching characteristics were quantified at different ages in Golgi-stained tissue using a three-dimensional computerized tracing system. During development, overall spine frequencies increase between 3 and 5 weeks and decrease thereafter. In particular, spine frequencies of middle segments decrease significantly by 14% between 5 and 7 weeks posthatching (p = 0.017). A further reduction of 48% occurs between 7 weeks and adulthood (p < 0.001), resulting in a spine reduction of 56% on middle segments between 35 days of age and adulthood. In addition to the reduction of spine frequencies, we find regressive events also on some of the neuronal parameters that we have quantified. In general, dendrites of adult animals terminate closer to the cell body than those of 7-, 5-, or 3-week-old birds. Whereas no changes in segment length of first- and second-order dendrites have been identified, third-order dendrites end 19% closer to the cell body in adults than in younger birds (p < 0.024). Second-order dendrites in adult animals branch less frequently than in 3-week-old animals (35%, p = 0.017). There is also a trend of a smaller number of tertiary branches in adulthood compared with 3-week-old birds (41%, p = 0.060). The morphological changes may be related to the function of this nucleus and the sensitive phase for song acquisition.

Vocal learning in Budgerigars (Melopsittacus undulatus) using food reward

Budgerigars (parakeets) are small, highly social, Australian parrots capable of vocal learning throughout adulthood. These birds readily produce short (200 ms), whistled, frequency‐modulated contact calls when separated from one another. In this experiment, birds were trained twice daily in 10 min sessions to produce or modify contact‐call‐like vocalizations using food reward. Calls were analyzed in real time using serial FFTs and each production was compared to a digitally stored ‘‘template.’’ Call productions which exceeded a predetermined criterion of similarity were rewarded, while those below criterion were not. Results show that budgerigars can learn to modify the intensity and spectro‐temporal pattern of their species‐typical calls within several days. Aside from human language, bird vocalizations have provided the only other clear example of learning in the acquisition and maintenance of a vocal repertoire. While song learning in birds has led to a number of important insights into the neurobiolog...

Social malleability in cowbirds (Molothrus ater artemisiae): Species and mate recognition in the first 2 years of life.

In a longitudinal study, the authors housed wild-caught juvenile male cowbirds (Molothrus ater artemisiae) with female cowbirds or canaries (Serinus canaria) from August until May. The males were then exposed to 3 social contexts. Males housed with canaries directed more vocalizations to canaries than to female cowbirds. Males housed with female cowbirds vocalized most to other males. The data revealed plasticity at a rudimentary level of reproductive behavior, selective responding to members of one's own species. Song potency, as assayed by playback, did not predict vocal use. To test adult malleability, the authors studied the males for a 2nd year. Half were housed with conspecific females and experienced males and half with only females. The manipUlation eradicated any signs of the males' 1st-year experiences. The data suggest malleability in species and mate recognition in cowbirds. Considerable evidence indicates that male cowbirds' vo­ cal repertoires are socially malleable. The timing and extent of exposure to adult male models affects the content of two vocal signals, the song and the flight whistle (Dufty, 1985; King & West, 1990; King, West, & Eastzer, 1980; O'Loghlen & Rothstein, 1993). Moreover, in some parts of the species' range, female cowbirds, which do not sing, can shape the content of the males' vocal repertoires through visual responses (West & King, 1988). In this report, we pose a broader question about male cowbirds' vocal capac­ ities: How does a juvenile male's access to social stimula­ tion affect his ability to use vocal signals effectively during the breeding season? To this end, we housed young males either with conspecific females or with canaries during their 1st year and then measured patterns of vocal behavior in the context of mate assortment during the breeding season. We followed this experiment with a second one in which we looked for evidence of plasticity in vocal and courtship skills in the same males' 2nd year. Although abundant evidence exists on the role of learning in songbirds' acquisition of vocal signals, few such studies include assessments of how males actually use their vocal­ izations in species-typical circumstances. Studies of blue

鳥の歌学習の脳内神経機構 鳥歌学習臨界期の脳可塑性を制御する物質を求めて

鳥の歌学習の脳内神経機構 鳥歌学習臨界期の脳可塑性を制御する物質を求めて

Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds

Song and brain structure are compared amongst 41 species of oscine birds by using the method of independent evolutionary contrasts. We find a significant correlation between the relative volume of the song control centre, the high vocal centre (HVC), and the number of song types typically found in the repertoire. Relative HVC volume is not correlated with the number of different syllable types per song bout. The relative volume of a second song nucleus, area X, is not significantly correlated with either measure. Relative HVC volume is uncorrelated with relative volume of the hippocampus, a brain area involved in other forms of memory. This is the first evidence for repeated independent evolution of an association between complexity of learned song and the relative volume of one of the song control nuclei though to be involved in song learning.

Where Is the Comparison in Comparative Cognition? Alternative Research Programs

Contemporary research on comparative cognition reflects two distinct programs. The purpose of the anthropocentric program is to discover whether nonhuman species process information in the same way as humans do. The ecological program analyzes ecologically significant aspects of cognition and compares them in closely and distantly related species. Research on memory for stored food in birds provides a detailed example of this latter program. Other examples include research on bird song learning and foraging and ecological analyses of human cognition.

Does Chaffinch Fringilla coelebs song vary with the habitat in which it is sung?

The acoustic adaptation hypothesis suggests that song learning in birds is advantageous because it enables song to become adapted to the habitat in which it is sung. A comparison was made among song types recorded from male Chaffinches Fringilla coelebs at a variety of sites in open scrub and in coniferous plantations, as well as in mature pine forest. Although some significant differences were found among habitats, these were few and there was no systematic relationship with features of the environment. This study does not therefore support the acoustic adaptation hypothesis.