Song Patterns Research Articles

Acoustic pattern variations in the female-directed birdsongs of a colony of laboratory-bred zebra finches

The acoustic profile of the zebra finch song is characterized by a series of identical repeating units, each comprising a distinctive sequence of acoustic elements, called syllables. Here, we perform an analysis of song pattern deviations caused by variabilities in the production of song syllables. Zebra finches produce four different kinds of syllable variabilities–syllable deletions, single or double syllable insertions, syllable alterations, and syllable repetitions. All these variabilities, with the exception of repetitions, are present in songs of more than two-thirds of the normal adult birds; repetitions are present in less than one-fifth of birds. The frequency of occurrence of these variabilities is independent of the amount of singing, suggesting that they are unlikely to result simply from singing-induced physiological changes such as fatigue. Their frequencies in tutor-deprived birds are not significantly different from those in normal birds, indicating that they are unlikely to be acquired due to deficiencies in tutor-dependent learning. The types, patterns of occurrence and relative frequencies of these song syllable variabilities might reveal insights into the functioning of the song motor control pathway.

Control of cricket stridulation by a command neuron: efficacy depends on the behavioral state.

Crickets use different song patterns for acoustic communication. The stridulatory pattern-generating networks are housed within the thoracic ganglia but are controlled by the brain. This descending control of stridulation was identified by intracellular recordings and stainings of brain neurons. Its impact on the generation of calling song was analyzed both in resting and stridulating crickets and during cercal wind stimulation, which impaired the stridulatory movements and caused transient silencing reactions. A descending interneuron in the brain serves as a command neuron for calling-song stridulation. The neuron has a dorsal soma position, anterior dendritic processes, and an axon that descends in the contralateral connective. The neuron is present in each side of the CNS. It is not activated in resting crickets. Intracellular depolarization of the interneuron so that its spike frequency is increased to 60-80 spikes/s reliably elicits calling-song stridulation. The spike frequency is modulated slightly in the chirp cycle with the maximum activity in phase with each chirp. There is a high positive correlation between the chirp repetition rate and the interneuron's spike frequency. Only a very weak correlation, however, exists between the syllable repetition rate and the interneuron activity. The effectiveness of the command neuron depends on the activity state of the cricket. In resting crickets, experimentally evoked short bursts of action potentials elicit only incomplete calling-song chirps. In crickets that previously had stridulated during the experiment, short elicitation of interneuron activity can trigger sustained calling songs during which the interneuron exhibits a spike frequency of approximately 30 spikes/s. During sustained calling songs, the command neuron activity is necessary to maintain the stridulatory behavior. Inhibition of the interneuron stops stridulation. A transient increase in the spike frequency of the interneuron speeds up the chirp rate and thereby resets the timing of the chirp pattern generator. The interneuron also is excited by cercal wind stimulation. Cercal wind stimulation can impair the pattern of chirp and syllable generation, but these changes are not reflected in the discharge pattern of the command neuron. During wind-evoked silencing reactions, the activity of the calling-song command neuron remains unchanged, but under these conditions, its activity is no longer sufficient to maintain stridulation. Therefore stridulation can be suppressed by cercal inputs from the terminal ganglia without directly inhibiting the descending command activity.

ACOUSTIC COMMUNICATION DISTANCES OF A GOMPHOCERINE GRASSHOPPER

ABSTRACT I studied in the laboratory and in the field the communication distance of the gomphocerine grasshopper Chorthippus biguttulus, which lives close to the ground in stony, short grass habitats. Using sound measurements and behavioural tests, I examined the frequency dependent attenuation and temporal degradation of the song pattern. Sound measurements (2–40 kHz) in the field revealed that excess attenuation increases with increasing frequency. Close to the ground, excess attenuation reaches 18 dB/m. On the basis of (i) excess attenuations, (ii) tympanic receptor threshold curves and (iii) song spectra, perception distances of female tympanic receptors for male songs and vice versa were calculated. Behavioural tests revealed that, especially in short and stony grass vegetation, the typical habitat of Ch. biguttulus, the temporal song pattern is strongly degraded. Thus, in the laboratory and in tall grass vegetation, sound attenuation was found to limit the communication distance. In contrast, in short grass vegetation, degradation of the temporal pattern was found to limit the communication distance of males listening to female songs. I argue that the exploitation of fast amplitude modulations for song recognition restricts the acoustic communication of grasshoppers to short distances (1–2.2 m). In this respect it seems adaptive to stridulate at low intensities.

A NEW SENSE OF THE COMPLEXITIES OF BIRD SONG

SINGING BIRDS are so familiar to most of us that the astounding complexity of their feats is often overlooked. Two articles in this issue of The Auk serve to remind us how little we understand or even recognize this complexity. The Nightingale Wren (Microcerculus philomela) of Central American forests, as Leger and his colleagues (2000) make clear, needs no special pleading to qualify as a source of wonder. This species produces one of the longest regularly repeated patterns of all bird songs. Most tropical ornithologists have assumed that these birds simply produce random sequences of notes. It turns out, however, that we have just not paid enough attention, because they actually produce a stereotyped sequence of haunting tones that can last nearly 15 seconds before repeating. A Nightingale Wren does not sing its entire song each time, but instead often interrupts its pattern. Apparently, these interruptions do not tend to occur at particular places in the sequence. Such weak links in a prolonged sequence of notes might indicate that the sequence was organized in chunks in the bird’s brain in much the same way that human songs are arranged in stanzas (Hultsch and Todt 1989). By singing songs that can end in many ways and by shifting the pattern in pitch, Nightingale Wrens turn their single pattern into a large repertoire of sorts. Despite their length, the songs of Nightin-

Neurochemical control of cricket stridulation revealed by pharmacological microinjections into the brain.

Neuroactive substances were administered into the frontal protocerebrum of tethered male Gryllus bimaculatus by pressure injections from microcapillaries. All three types of species-specific song pattern (calling song, rivalry song and courtship song) could be elicited by injection of acetylcholine and cholinergic agonists. Injection of nicotine led to short bouts of calling song that occurred after a short latency. In contrast, muscarine elicited long-lasting stridulation that took longer to develop. The pharmacologically induced song patterns showed transitions from rivalry song to calling song and from calling song to courtship song, which also occur during natural behaviour. Stridulation induced by a cholinergic agonist could be immediately blocked by microinjection of (&ggr;)-aminobutyric acid (GABA) into the same neuropile sites. Administration of picrotoxin in resting crickets led to enhanced motor activity that incorporated the three different song patterns. We propose that, in the brain of the cricket, acetylcholine and GABA are putative transmitters involved in the control of stridulation. Histological analysis located the stimulation sites to an area between the pedunculus and the (&agr;)-lobe of the mushroom body in which the command neurons for calling song have dendritic arborizations.

Auditory–visual stimulus pairing enhances perceptual learning in a songbird

In many oscine birds, song learning is affected by social variables, for example the behaviour of a tutor. This implies that both auditory and visual perceptual systems should be involved in the acquisition process. To examine whether and how particular visual stimuli can affect song acquisition, we tested the impact of a tutoring design in which the presentation of auditory stimuli (i.e. species-specific master songs) was paired with a well-defined nonauditory stimulus (i.e. stroboscope light flashes: Strobe regime). The subjects were male hand-reared nightingales, Luscinia megarhynchos . For controls, males were exposed to tutoring without a light stimulus (Control regime). The males’ singing recorded 9 months later showed that the Strobe regime had enhanced the acquisition of song patterns. During this treatment birds had acquired more songs than during the Control regime; the observed increase in repertoire size was from 20 to 30% in most cases. Furthermore, the copy quality of imitations acquired during the Strobe regime was better than that of imitations developed from the Control regime, and this was due to a significant increase in the number of ‘perfect’ song copies. We conclude that these effects were mediated by an intrinsic component (e.g. attention or arousal) which specifically responded to the Strobe regime. Our findings also show that mechanisms of song learning are well prepared to process information from cross-modal perception. Thus, more detailed enquiries into stimulus complexes that are usually referred to as social variables are promising.

Decrystallization of adult birdsong by perturbation of auditory feedback.

Young birds learn to sing by using auditory feedback to compare their own vocalizations to a memorized or innate song pattern; if they are deafened as juveniles, they will not develop normal songs. The completion of song development is called crystallization. After this stage, song shows little variation in its temporal or spectral properties. However, the mechanisms underlying this stability are largely unknown. Here we present evidence that auditory feedback is actively used in adulthood to maintain the stability of song structure. We found that perturbing auditory feedback during singing in adult zebra finches caused their song to deteriorate slowly. This 'decrystallization' consisted of a marked loss of the spectral and temporal stereotypy seen in crystallized song, including stuttering, creation, deletion and distortion of song syllables. After normal feedback was restored, these deviations gradually disappeared and the original song was recovered. Thus, adult birds that do not learn new songs nevertheless retain a significant amount of plasticity in the brain.

The neuromuscular control of birdsong.

Birdsong requires complex learned motor skills involving the coordination of respiratory, vocal organ and craniomandibular muscle groups. Recent studies have added to our understanding of how these vocal subsystems function and interact during song production. The respiratory rhythm determines the temporal pattern of song. Sound is produced during expiration and each syllable is typically followed by a small inspiration, except at the highest syllable repetition rates when a pattern of pulsatile expiration is used. Both expiration and inspiration are active processes. The oscine vocal organ, the syrinx, contains two separate sound sources at the cranial end of each bronchus, each with independent motor control. Dorsal syringeal muscles regulate the timing of phonation by adducting the sound-generating labia into the air stream. Ventral syringeal muscles have an important role in determining the fundamental frequency of the sound. Different species use the two sides of their vocal organ in different ways to achieve the particular acoustic properties of their song. Reversible paralysis of the vocal organ during song learning in young birds reveals that motor practice is particularly important in late plastic song around the time of song crystallization in order for normal adult song to develop. Even in adult crystallized song, expiratory muscles use sensory feedback to make compensatory adjustments to perturbations of respiratory pressure. The stereotyped beak movements that accompany song appear to have a role in suppressing harmonics, particularly at low frequencies.

DUET SONGS OF THE SIAMANG, HYLOBATES SYNDACTYLUS: II. TESTING THE PAIR-BONDING HYPOTHESIS DURING A PARTNER EXCHANGE

AbstractIt has repeatedly been suggested for several duetting bird and primate species that duetting might act as a reinforcement of the pair bond. Until now, it has apparently not been demonstrated that the premises underlying the pair-bonding hypothesis are met by any duetting species. Siamangs (Hylobates syndactylus) are monogamous apes which produce long and complex duet songs. This study analyses the changes in duet structure in two pairs of siamangs during a forced partner exchange. The duet songs of the siamangs underwent many notable changes during partner exchange. Of 33 different variants of the great call sequence, 29% in one pair and 21% in the other were restricted to the first stage just after the partner exchange. Some of these changes were certainly due to individualistic traits of the new partner, and for some other changes, this possibility cannot be reliably excluded. At least two changes, however, can only be interpreted in terms of a learning effort by which one partner adapts its duetting behaviour to that of its new mate. The two newly formed pairs of this report appear to be the first documented cases to fulfil the requirements underlying Wickler's (1980) pair-bonding hypothesis: The animals under study were showing a stable song pattern with pair-specific traits. After the partner exchange, new pair-specific traits occurred, some of them obviously achieved through a partner-directed effort of one or both individual(s). Moreover, the pair-bonding hypothesis appears to be one of the few biological functions suggested so far which could explain a high degree of duet-complexity as adaptive. However, the loudness of the siamang song alone suggests that other functions are also involved. These are most probably related to territorial advertisement, pair bond advertisement and (possibly) mate attraction.

The Role of Auditory Feedback in the Maintenance of Song in Adult Male Bengalese Finches Lonchura striata var. domestica

Abstract Young songbirds use auditory feedback to match their own vocalizations with a memorized tutor's song in order to develop their songs normally. After learning, songs of adult birds are stereotyped and remain stable. Recent studies showed that auditory feedback is necessary for maintaining the stability of adult bird song in some species including Bengalese finches. We deprived adult male Bengalese finches of auditory input by removing their cochleae and acoustically analyzed the songs of the deafened birds. After the operation, song patterns altered within a week and remained unstable for approximately a month. The post-operative songs were finally stabilized within 60 days after the operation, although their patterns were different from those of the pre-operative songs. Compared with the pre-operative songs, syllables with higher fundamental frequencies decreased and those with lower fundamental frequencies increased in the stabilized post-operative songs of all the birds examined. These results ...

Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows ( Zonotrichia leucophrys)

The anterior forebrain pathway of the avian song system is involved in juvenile song learning, but its function in adult song behavior is not known. This report uses lesions to study the role of a particular forebrain nucleus, lMAN, in the seasonal regeneration of song in adult white-crowned sparrows ( Zonotrichia leucophrys oriantha). White-crowned sparrows, even when acoustically isolated as juveniles, crystallize a single song which they maintain throughout adulthood. The lateral portion of the magnocellular nucleus of the anterior neostriatum (lMAN) was lesioned bilaterally in adult males maintained on short days (8 h of light). Daylength was increased to 16 h following the surgeries, and all birds were recorded in the post-lesion singing season. Lesioned birds showed a large decrease in song note frequency following the lesions, significantly larger than did intact, age-matched controls. Further changes were seen in the post-lesion songs of seven of 11 successfully lesioned males. These changes included variability in song pattern, loss of frequency control and addition of new notes, some of which had been practiced during juvenile song development. These changes seemed especially large in birds that had either been acoustically isolated or had not fully copied a tape-tutor song during juvenile song development. These results are the first to indicate that the motor memories for song elements that had been practiced and discarded early in life are retained, and they suggest that lMAN affects seasonal song expression by selectively reinforcing a particular song pattern.

Robots, crickets and ants: models of neural control of chemotaxis and phonotaxis

Neural control in animals can be investigated using robot models. Two simple behaviours are focused on: pheromone trail following in ants and sound source localization in crickets. Our models address the real sensorimotor constraints and physiological underpinnings of these behaviours. Using alcohol gas sensors on a robot it is shown that a simple neural architecture can reproduce a range of trail-following behaviours that qualitatively resemble the results reported for ants. Building a more detailed auditory sensor based on the cricket ear it is shown that preference for song frequency and pattern does not require a recognition mechanism, using real cricket song as stimuli. Finally the spiking neuron models that enable us to examine exactly how these robust forms of motor control can emerge from small networks of neurons are introduced.

EVOLUTION OF COURTSHIP SONG AND REPRODUCTIVE ISOLATION IN THE DROSOPHILA WILLISTONI SPECIES COMPLEX: DO SEXUAL SIGNALS DIVERGE THE MOST QUICKLY?

Reproductive isolation increases with genetic distance between species. Although sexual selection may drive divergence of sexual signals and traits, causing rapid evolution of sexual isolation, quantitative data supporting this idea are rare. We examine the rates of divergence of a species-specific courtship signal, sexual isolation, and postmating isolation in the Drosophila willistoni group. Both types of isolation increase with genetic distance and postmating isolation is the most strongly correlated with genetic divergence, suggesting this has the least variable divergence rate. Song divergence is not correlated with genetic divergence. Homoplasy in song pattern results in poorly resolved phylogenies that are different from molecular phylogenies. Song evolves more quickly than sexual isolation, which evolves more quickly than postmating isolation.

Recognition of Neighbors' Song in a Species with Large and Complex Song Repertoires: The Thrush Nightingale

To investigate aspects of neighbor recognition in a migratory bird with large and complex song repertoires we conducted playback experiments in the field with male territorial Thrush Nightingales Luscinia luscinia as subjects. Males sing with immediate variety and neighbors can share a considerable part of their repertoire of song components and song types. Subjects responded significantly more to their neighbors' song broadcast from the unshared (opposite) territorial boundary than to playback of the same song broadcast from the shared territorial boundary. Thus, this study did not detect constraints on neighbor recognition imposed for instance by large and complex song repertoires, high singing versatility, or sharing of song patterns. Because Thrush Nightingales sing shared patterns in different ways, either by constructing different song types out of the shared pool of elements or by singing shared song types in different sequential order, they could attend to song components and their syntactical arrangement, full songs, or their sequential delivery for neighbor recognition. Which mechanism they use might depend on the similarity of the song and singing style of a singer compared to other familiar conspecifics.

Temporal rhythms in the signals of insects

The signals generated by acoustic insects exhibit temporal patterns on several time scales. Annual or seasonal rhythms provide information about temporal changes in insect population size. Knowledge of such changes might be useful in ecological monitoring programs. Circadian or daily rhythms commonly seen in insect signaling are generated by endogenous ‘‘clocks’’ that are reset by environmental cues. Understanding these daily patterns is also important for monitoring insect populations. Within insect populations, the signals of neighbors sometimes show temporal patterns of synchrony or alternation with timing on the order of seconds. The phase relationships among individuals are maintained by acoustic resetting, whereby an individual’s temporal rhythm will change depending on the phase that neighboring signals are received. On still smaller time scales, temporal patterns of insect songs are diverse and generally differ among species. These small-scale patterns are often essential components of mating signals and are used in mate recognition and mate choice.

Sexual selection and natural selection in bird speciation

The role of sexual selection in speciation is investigated, addressing two main issues. First, how do sexually selected traits become species recognition traits? Theory and empirical evidence suggest that female preferences often do not evolve as a correlated response to evolution of male traits. This implies that, contrary to runaway (Fisherian) models of sexual selection, premating isolation will not arise as an automatic side effect of divergence between populations in sexually selected traits. I evaluate premating isolating mechanisms in one group, the birds. In this group premating isolation is often a consequence of sexual imprinting, whereby young birds learn features of their parents and use these features in mate choice. Song, morphology and plumage are known recognition cues. I conclude that perhaps the main role for sexual selection in speciation is in generating differences between populations in traits. Sexual imprinting then leads to these traits being used as species recognition mechanisms. The second issue addressed in this paper is the role of sexual selection in adaptive radiation, again concentrating on birds. Ecological differences between species include large differences in size, which may in themselves be sufficient for species recognition, and differences in habitat, which seem to evolve frequently and at all stages of an adaptive radiation. Differences in habitat often cause song and plumage patterns to evolve as a result of sexual selection for efficient communication. Therefore sexual selection is likely to have an important role in generating premating isolating mechanisms throughout an adaptive radiation. It is also possible that sexual selection, by creating more allopatric species, creates more opportunity for ecological divergence to occur. The limited available evidence does not support this idea. A role for sexual selection in accelerating ecological diversification has yet to be demonstrated.

Localization of androgen receptor mRNA-containing cells in avian respiratory-vocal nuclei: Anin situ hybridization study

Song development and song pattern formation in oscine songbirds are influenced by steroid hormones such as estrogens and androgens, and the control of vocal pattern generation is mediated via a network of interconnected vocal and respiratory nuclei. The main components of the respiratory part of the network are the expiratory and inspiratory premotor nuclei, known as retroambigualis (RAm) and the rostral ventral respiratory group (rVRG), respectively. These respiratory components play an integral role in song production either by providing the expiratory pulses of air required for each and every song syllable, or by controlling inspiration between syllables in the form of minibreaths, and between phrases for major replenishments of air. Here we analyze the distribution of androgen receptors (AR) and estrogen receptors (ER) in the midbrain and hindbrain of male and female zebra finches, and male canaries and green finches, using in situ hybridization with cRNA probes of the zebra finch AR and ER. ERmRNA was not expressed in any of the respiratory-vocal nuclei of the midbrain or hindbrain, but ARmRNA was expressed in the tracheosyringeal motor nucleus (nXIIts) and in RAm and rVRG. The size of the ARmRNA defined RAm and rVRG was similar in male and female zebra finches, but the size of ARmRNA defined nXIIts was slightly sexual dimorphic. Previously undescribed areas of ARmRNA expression outside the respiratory-vocal network in the brain stem were the nucleus semilunaris and layers 10-12 of the optic tectum. AR-mRNA expression in the respiratory-vocal nuclei of adult male songbirds, adult female zebra finches, and juvenile zebra finches suggests that the temporal pattern of learned and unlearned vocalizations is sensitive to androgen-dependent mechanisms mediated by RAm and rVRG.

Neural pathways for the control of birdsong production

As in humans, song production in birds involves the intricate coordination of at least three major groups of muscles: namely, those of the syrinx, the respiratory apparatus, and the upper vocal tract, including the jaw. The pathway in songbirds that controls the syrinx originates in the telencephalon and projects via the occipitomesencephalic tract directly upon vocal motoneurons in the medulla. Activity in this pathway configures the syrinx into phonatory positions for the production of species typical vocalizations. Another component of this pathway mediates control of respiration during vocalization, since it projects upon both expiratory and inspiratory groups of premotor neurons in the ventrolateral medulla, as well as upon several other nuclei en route. This pathway appears to be primarily involved with the control of the temporal pattern of song, but is also importantly involved in the control of vocal intensity, mediated via air sac pressure. There are extensive interconnections between the vocal and respiratory pathways, especially at brain-stem levels, and it may be these that ensure the necessary temporal coordination of syringeal and respiratory activity. The pathway mediating control of the jaw appears to be different from those mediating control of the syrinx and respiratory muscles. It originates in a different part of the archistriatum and projects upon premotor neurons in the medulla that appear to be separate from those projecting upon the syringeal motor nucleus. The separateness of this pathway may reflect the imperfect correlation of jaw movements with the dynamic and acoustic features of song. The brainstem pathways mediating control of vocalization and respiration in songbirds have distinct similarities to those in mammals such as cats and monkeys. However, songbirds, like humans, but unlike most other non-songbirds, have developed a telencephalic vocal control system for the production of learned vocalizations.

Three models of song learning: Evidence from behavior

Research on avian song learning has traditionally been based on an instructional model, as exemplified by the sensorimotor model of song development. Several large-scale, species-wide field studies of learned birdsongs have revealed that variation is narrowly restricted to certain aspects of song structure. Other aspects are sufficiently stereotyped and so widely shared by species' members that they qualify as species-specific universals. The limitations on natural song variation are difficult to reconcile with a fully open, instructive model of song learning. An alternative model based on memorization by selection postulates a system of innate neural templates that facilitate the recognition and rapid memorization of conspecific song patterns. Behavioral evidence compatible with this model includes learning preferences, rapid conspecific song learning, and widespread ocurrence of species-specific song universals that are recognized innately but fail to develop in songs of social isolates. A third model combines instruction, in the memorization phase, with selection during song production. An overproduced repertoire of plastic songs previously memorized by instruction is winnowed by selection imposed during social interactions at the time of adult song crystallization. Selection during production is well established as a factor in the song development of several species, in the form of action-based learning. The possible role of selective processes in song memorization merits further neurobiological investigation.

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.