Design of a robotic zebra finch for experimental studies on developmental song learning.

Birdsong learning has been consolidated as the model system of choice for exploring the biological substrates of vocal learning. In the zebra finch (Taeniopygia guttata), only males sing and they develop their song during a sensitive period in early life. Different experimental procedures have been used in the laboratory to train a young finch to learn a song. So far, the best method to achieve a faithful imitation is to keep a young bird singly with an adult male. Here, we present the different characteristics of a robotic zebra finch that was developed with the goal to be used as a song tutor. The robot is morphologically similar to a life-sized finch: it can produce movements and sounds contingently to the behaviours of a live bird. We present preliminary results on song imitation, and other possible applications beyond the scope of developmental song learning.

Traffic noise disrupts vocal development and suppresses immune function.

Noise pollution has been linked to learning and language deficits in children, but the causal mechanisms connecting noise to cognitive deficiencies remain unclear because experimental models are lacking. Here, we investigated the effects of noise on birdsong learning, the primary animal model for vocal learning and speech development in humans. We found that traffic noise exposure retarded vocal development and led to learning inaccuracies. In addition, noise suppressed immune function during the sensitive learning period, indicating that it is a potent stressor for birds, which is likely to compromise their cognitive functions. Our results provide important insights into the consequences of noise pollution and pave the way for future studies using birdsong as an experimental model for the investigation of noise-induced learning impairments.

Auditory perception of self and others in zebra finches: evidence from an operant discrimination task.

Vocal communication is essential for social interactions in many animal species. For this purpose, an animal has to perceive vocal signals of conspecifics and is often also required to discriminate conspecifics. The capacity to discriminate conspecifics is particularly important in social species in which individuals interact repeatedly. In addition, auditory perception of self plays an important role for vocal learners. A vocal learner has to memorise vocalisations of conspecifics and to subsequently modify its own vocalisations in order to match the memorised vocalisations. Here, we investigated auditory perception of self and others in zebra finches (Taeniopygia guttata), a highly gregarious songbird species and vocal learner. We used laboratory colonies in which founder males had been previously trained to produce the same song type. This resulted in artificial dialects in the song of founders and their offspring. We investigated whether those birds would be able to discriminate between familiar and unfamiliar conspecifics based on song. Furthermore, we examined whether they would classify their own song as familiar or unfamiliar. We found that birds were able to discriminate between songs of familiar versus unfamiliar conspecifics, despite the fact that all songs were imitations of the same song type. This suggests that such discrimination is possible even based on songs with a high acoustic similarity. None of the subjects classified their own song as unfamiliar. Three out of eight males classified their own song as familiar. Thus zebra finches might recognise their own song. Further experiments are needed to confirm such self-recognition.

Mechanisms of recognition in birds and social Hymenoptera: from detection to information processing.

In this opinion piece, we briefly review our knowledge of the mechanisms underlying auditory individual recognition in birds and chemical nest-mate recognition in social Hymenoptera. We argue that even though detection and perception of recognition cues are well studied in social Hymenoptera, the neural mechanisms remain a black box. We compare our knowledge of these insect systems with that of the well-studied avian 'song control system'. We suggest that future studies on recognition should focus on the hypothesis of a distributed template instead of trying to locate the seat of the template as recent results do not seem to point in that direction. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Individual vocal recognition in zebra finches relies on song syllable structure rather than song syllable order.

Many species are able to vocally recognize individual conspecifics and this capacity seems widespread in oscine songbirds. The exact acoustic features used for such recognition are often not clear. In the zebra finch (Taeniopygia guttata), the song motif is composed of a few syllables repeated in a fixed sequential order and song bouts include several repetitions of the motif. Here, we used an operant discrimination task, the GO/NOGO procedure, to show that zebra finches are capable of individual vocal recognition even if the bird has to distinguish males that all produce an imitation of the same song model. Furthermore, we studied whether such individual vocal recognition was based on spectro-temporal details of song syllables, i.e. the local fine structure of the song, or on the sequential order in which song syllables are arranged in the song bout. To this end, we trained male and female zebra finches to discriminate songs of one male conspecific from those of four others. After learning this baseline discrimination, subjects were exposed to a novel set of stimuli originating from the same individuals, in order to test for their capability to generalise. Subjects correctly classified those novel stimuli, illustrating their ability for individual vocal recognition. Then they were exposed to hybrid stimuli combining the syllable sequences of one individual with the spectro-temporal features of another. Behavioural responses of subjects to hybrid stimuli suggest that they rely on spectro-temporal details of syllables and might pay less attention to syllable sequences for individual vocal recognition.

Consistency of female preference for male song in the domestic canary using two measures: Operant conditioning and vocal response.

Variation of female preferences is often reported in the literature and could be related to an artefact derived from multiple different methods used. Thus, there is a need to evaluate the influence of different methods when assessing female preferences. The present study aims to compare female preferences obtained from an operant conditioning test and from female vocal responses to male song in the domestic canary (Serinus canaria). In an operant conditioning test, females had the possibility to choose between two keys; a peck on one key elicited a supposed very attractive canary song while a peck on the other key elicited a less attractive song. Meanwhile, female vocal responses were recorded. Our results revealed that female canaries preferred to peck on the key eliciting the attractive song and that they emitted more copulation calls in response to the attractive song compared to the less attractive song. This study shows the congruence of these two methods and further suggests that they are reliable to study female preferences in laboratory conditions.

The perception of self in birds.

The perception of self is an important topic in several disciplines such as ethology, behavioral ecology, psychology, developmental and cognitive neuroscience. Self-perception is investigated by experimentally exposing different species of animals to self-stimuli such as their own image, smell or vocalizations. Here we review more than one hundred studies using these methods in birds, a taxonomic group that exhibits a rich diversity regarding ecology and behavior. Exposure to self-image is the main method for studying self-recognition, while exposing birds to their own smell is generally used for the investigation of homing or odor-based kin discrimination. Self-produced vocalizations - especially in oscine songbirds - are used as stimuli for understanding the mechanisms of vocal coding/decoding both at the neural and at the behavioral levels. With this review, we highlight the necessity to study the perception of self in animals cross-modally and to consider the role of experience and development, aspects that can be easily monitored in captive populations of birds.

Horizontal transmission of the father's song in the zebra finch (Taeniopygia guttata).

As is the case for human speech, birdsong is transmitted across generations by imitative learning. Although transfer of song patterns from adults to juveniles typically occurs via vertical or oblique transmission, there is also evidence of horizontal transmission between juveniles of the same generation. Here, we show that a young male zebra finch (Taeniopygia guttata) that has been exposed to its father during the sensitive period for song learning can lead a brother, that has never heard the paternal song, to imitate some sounds of the father. Moreover, song similarity between the two brothers was higher than the similarity measured between the paternal song and the song of the brother that had a week-long exposure to the father. We speculate that the phenomenon of within-generation song learning among juveniles may be more widespread than previously thought and that when a juvenile evaluates potential models for imitative learning, a sibling may be as salient as an adult.

Representation of early sensory experience in the adult auditory midbrain: implications for vocal learning.

Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird's own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning.

Heterospecific exposure affects the development of secondary sexual traits in male zebra finches (Taeniopygia guttata).

In many animal species, social signals can affect the reproductive physiology and behaviour of conspecifics. In a few species that exhibit vocal learning, exposure to conspecific and sometimes heterospecific sounds can also influence their vocal development. Here we show that heterospecific exposure can affect the development of secondary sexual traits of male zebra finches (Taeniopygia guttata). In a first experiment, we trained young males with a passive playback of domesticated canary (Serinus canaria) song. Song playback enhanced the sexual development of the birds: they started to sing during the presentation of a video clip of a female earlier during development and exhibited secondary sexual plumage ornaments faster than males of the control group kept in silence. Two out of five birds exhibited clear evidence of imitation of canary song. In a second experiment, we raised young male finches with young male canaries in pairs until adulthood. Again, the live contact with a heterospecific companion affected the development of plumage ornaments in finches. We also observed some evidences of vocal convergence, both for calls and song. Moreover, young males of both species could recognize the call of their heterospecific companion when adults. These results suggest that heterospecific exposure can affect both the sexual and the vocal development of the zebra finch and can have long lasting effects. This article is part of a Special Issue entitled: insert SI title.

Comparisons of different methods to train a young zebra finch (Taeniopygia guttata) to learn a song.

Like humans, oscine songbirds exhibit vocal learning. They learn their song by imitating conspecifics, mainly adults. Among them, the zebra finch (Taeniopygia guttata) has been widely used as a model species to study the behavioral, cellular and molecular substrates of vocal learning. Various methods using taped song playback have been used in the laboratory to train young male finches to learn a song. Since different protocols have been applied by different research groups, the efficiency of the studies cannot be directly compared. The purpose of our study was to address this problem. Young finches were raised by their mother alone from day post hatching (dph) 10 and singly isolated from dph 35. One week later, exposure to a song model began, either using a live tutor or taped playback (passive or self-elicited). At dph 100, the birds were transferred to a common aviary. We observed that one-to-one live tutoring is the best method to get a fairly complete imitation. Using self-elicited playback we observed high inter-individual variability; while some finches learned well (including good copying of the song model), others exhibited poor copying. Passive playback resulted in poor imitation of the model. We also observed that finches exhibited vocal changes after dph 100 and that the range of these changes was negatively related to their imitation of the song model. Taken together, these results suggest that social aspects are predominant in the success outcome of song learning in the zebra finch.

Melatonin affects the temporal pattern of vocal signatures in birds.

In humans and other animals, melatonin is involved in the control of circadian biological rhythms. Here, we show that melatonin affects the temporal pattern of behavioral sequences in a noncircadian manner. The zebra finch (Taeniopygia guttata) song and the crow of the Japanese quail (Coturnix japonica) are courtship vocalizations composed of a stereotyped sequence of syllables. The zebra finch song is learned from conspecifics during infancy, whereas the Japanese quail crow develops normally without auditory input. We recorded and analyzed the complete vocal activity of adult birds of both species kept in social isolation for several weeks. In both species, we observed a shortening of signal duration following the transfer from a light-dark (LD) cycle to constant light (LL), a condition known to abolish melatonin production and to disrupt circadian rhythmicity. This effect was reversible because signal duration increased when the photoperiod was returned to the previous LD schedule. We then tested whether this effect was directly related to melatonin by removal of the pineal gland, which is the main production site of circulating melatonin. A shortening of the song duration was observed following pinealectomy in LD. Likewise, melatonin treatment induced changes in the temporal structure of the song. In a song learning experiment, young pinealectomized finches and young finches raised in LL failed to copy the temporal pattern of their tutor's song. Taken together, these results suggest that melatonin is involved in the control of motor timing of noncircadian behavioral sequences through an evolutionary conserved neuroendocrine pathway.

Interspecific hybridization as a tool to understand vocal divergence: the example of crowing in quail (Genus Coturnix).

Understanding the mechanisms that lead organisms to be separated into distinct species remains a challenge in evolutionary biology. Interspecific hybridization, which results from incomplete reproductive isolation, is a useful tool to investigate such mechanisms. In birds, interspecific hybridization is relatively frequent, despite the fact that closed species exhibit morphological and behavioural differences. Evolution of behaviour is difficult to investigate on a large timescale since it does not 'fossilize'. Here I propose that calls of hybrid non-songbirds that develop without the influence of learning may help in understanding the gradual process that leads to vocal divergence during speciation. I recorded crows produced by the European quail (Coturnix c. coturnix), the domestic Japanese quail (Coturnix c. japonica) and their hybrids (F1, F2 and backcrosses). Most crowing patterns were intermediate to those of the parental species; some were similar to one or the other parental species, or not present in either parental species. I also observed vocal changes in hybrid crows during the breeding season and from one year to the other. This vocal variability resembles those observed during the ontogeny of the crow in quails. It is likely that similar mechanisms involved in vocal changes during ontogeny might have driven vocal divergence in the species of Palearctic quails. I suggest that hybrid crows might have resembled those produced by intermediary forms of quails during speciation.

The genetic basis of zebra finch vocalizations.

Animal vocalizations play an important role in individual recognition, kin recognition, species recognition, and sexual selection. Despite much work in these fields done on birds virtually nothing is known about the heritability of vocal traits in birds. Here, we study a captive population of more than 800 zebra finches (Taeniopygia guttata) with regard to the quantitative genetics of call and song characteristics. We find very high heritabilities in nonlearned female call traits and considerably lower heritabilities in male call and song traits, which are learned from a tutor and hence show much greater environmental variance than innate vocalizations. In both sexes, we found significant heritabilities in several traits such as mean frequency and measures of timbre, which reflect morphological characteristics of the vocal tract. These traits also showed significant genetic correlations with body size, as well as positive genetic correlations between the sexes, supporting a scenario of honest signaling of body size through genetic pleiotropy ("index signal"). In contrast to such morphology-related voice characteristics, classical song features such as repertoire size or song length showed very low heritabilities. Hence, these traits that are often suspected to be sexually selected would hardly respond to current directional selection.

Dynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica).

Species-specific behaviours gradually emerge, via incomplete patterns, to the final complete adult form. A classical example is birdsong, a learned behaviour ideally suited for studying the neural and molecular substrates of vocal learning. Young songbirds gradually transform primitive unstructured vocalizations (subsong, akin to human babbling) into complex, stereotyped sequences of syllables that constitute adult song. In comparison with birdsong, territorial and mating calls of vocal non-learner species are thought to exhibit little change during development. We revisited this issue using the crowing behaviour of domestic Japanese quail (Coturnix coturnix japonica). Crowing activity was continuously recorded in young males maintained in social isolation from the age of three weeks to four months. We observed developmental changes in crow structure, both the temporal and the spectral levels. Speed and trajectories of these developmental changes exhibited an unexpected high inter-individual variability. Mechanisms used by quails to transform sounds during ontogeny resemble those described in oscines during the sensorimotor phase of song learning. Studies on vocal non-learners could shed light on the specificity and evolution of vocal learning.

How sleep affects the developmental learning of bird song.

Sleep affects learning and development in humans and other animals, but the role of sleep in developmental learning has never been examined. Here we show the effects of night-sleep on song development in the zebra finch by recording and analysing the entire song ontogeny. During periods of rapid learning we observed a pronounced deterioration in song structure after night-sleep. The song regained structure after intense morning singing. Daily improvement in similarity to the tutored song occurred during the late phase of this morning recovery; little further improvement occurred thereafter. Furthermore, birds that showed stronger post-sleep deterioration during development achieved a better final imitation. The effect diminished with age. Our experiments showed that these oscillations were not a result of sleep inertia or lack of practice, indicating the possible involvement of an active process, perhaps neural song-replay during sleep. We suggest that these oscillations correspond to competing demands of plasticity and consolidation during learning, creating repeated opportunities to reshape previously learned motor skills.

Classification of hybrid crows in quail using artificial neural networks.

In galliforms, calls are strongly determined genetically and no influence of learning has ever been demonstrated. Hybridization is a useful tool for investigating patterns of heritability. The vocal repertoire of the European quail (Coturnix c. coturnix) and of the Japanese quail (C. c. japonica) are similar except for their crows. The European quail possesses two forms of crows and the Japanese quail only one form. We produced hybrids from the following crosses; F(1), F(2) and backcrosses. Visual analysis of spectrograms showed that hybrid crows presented all intermediaries between the three forms of crows produced by the two subspecies. According to the level of analysis of a crow, visual classifications of spectrograms probably include some subjectivity. Artificial Neural Networks (ANN) are now widely used as a powerful classification technique in behavioural sciences. We trained an ANN to recognize the three crows of the two subspecies. Then we analysed its classification of hybrid crows. The ANN revealed important inter-individual variability between the crows of the F(1) and the F(2) crosses. Birds issued from backcrosses produced crows similar to those of the European quail to which they were backcrossed. This study confirms that ANN is a useful tool to classify spectrograms rapidly.