Avian vocalisations: the female perspective.

Research on avian vocalisations has traditionally focused on male song produced by oscine passerines. However, accumulating evidence indicates that complex vocalisations can readily evolve outside the traditional contexts of mate attraction and territory defence by male birds, and yet the previous bias towards male song has shaped - and continues to shape - our understanding of avian communication as a whole. Accordingly, in this review we seek to address this imbalance by synthesising studies on female vocalisations from across signalling contexts throughout the Aves, and discuss the implications of recent empirical advances for our understanding of vocalisations in both sexes. This review reveals great structural and functional diversity among female vocalisations and highlights the important roles that vocalisations can play in mediating female-specific behaviours. However, fundamental gaps remain. While there are now several case studies that identify the function of female vocalisations, few quantify the associated fitness benefits. Additionally, very little is known about the role of vocal learning in the development of female vocalisations. Thus, there remains a pressing need to examine the function and development of all forms of vocalisations in female birds. In the light of what we now know about the functions and mechanisms of female vocalisations, we suggest that conventional male-biased definitions of songs and calls are inadequate for furthering our understanding of avian vocal communication more generally. Therefore, we propose two simple alternatives, both emancipated from the sex of the singer. The first distinguishes song from calls functionally as a sexually selected vocal signal, whilst the second distinguishes them mechanistically in terms of their underlying neurological processes. It is clear that more investigations are needed into the ultimate and proximate causes of female vocalisations; however, these are essential if we are to develop a holistic epistemology of avian vocal communication in both sexes, across ecological contexts and taxonomic divides.

Local Axonal Conduction Shapes the Spatiotemporal Properties of Neural Sequences.

Sequential activation of neurons has been observed during various behavioral and cognitive processes, but the underlying circuit mechanisms remain poorly understood. Here, we investigate premotor sequences in HVC (proper name) of the adult zebra finch forebrain that are central to the performance of the temporally precise courtship song. We use high-density silicon probes to measure song-related population activity, and we compare these observations with predictions from a range of network models. Our results support a circuit architecture in which heterogeneous delays between sequentially active neurons shape the spatiotemporal patterns of HVC premotor neuron activity. We gauge the impact of several delay sources, and we find the primary contributor to be slow conduction through axonal collaterals within HVC, which typically adds between 1 and 7.5 ms for each link within the sequence. Thus, local axonal "delay lines" can play an important role in determining the dynamical repertoire of neural circuits.

Effect of Birdsong Soundscape on Perceived Restorativeness in an Urban Park.

Natural soundscapes have beneficial effects on the perceived restorativeness of an environment. This study examines the effect of birdsong, a common natural soundscape, on perceived restorativeness in Harbin Sun Island Park in China. Eight sites were selected and a series of questionnaire surveys on perceived restorativeness soundscape scale (PRSS) of four birdsong types were conducted during summer and winter. Two-hundred and forty respondents participated in this survey. Analysis of the survey results shows that different types of birdsong have different perceived restorativeness effects in different seasons. Crow birdsong has the worst effect on the perceived restorativeness in both summer and winter. Moreover, sound comfort and preference are significantly associated with the perceived restorativeness. The perceived restorativeness soundscape is best when birdsong is at a height of 4 m rather than 0.5 m or 2 m. The demographic/social factors of age, education, and stress level are all correlated with perceived restorativeness. There are suggestions for urban park design, especially with constructed natural elements. Creating a suitable habitat for multiple species of birds will improve perceived restorativeness. Moreover, appropriate activities should be provided in city parks to ensure restorativeness environments, especially for subjects with high levels of education and stress.

Does the Presence of Birdsongs Improve Perceived Levels of Mental Restoration from Park Use? Experiments on Parkways of Harbin Sun Island in China.

Green spaces in cities and urban parks serve as central areas for mental restoration and relieving pressure, and attention to soundscapes for their mental health benefits has become more prevalent. Birdsongs are perceived to enhance the restorative benefits of urban parks. This study examines Harbin Sun Island Park, the main bird habitat in the city of Harbin with numerous types of landscapes. We used space syntax to select the appropriate path space as a carrier and the pixel grid method to quantify path space shapes. A correlation analysis of field data was also used to explore the perceived restorative effects of birdsongs heard in urban parks using scales detailing the perceived restorative effects of various visual and auditory stimuli. The results show that soundscapes can significantly improve perceived recovery benefits, and that hearing birdsongs can significantly improve the perceived restorative benefits of wetland paths; the sky index of a tour path showed a significantly negative correlation with each feature (i.e., the four featured dimensions of "charm", "escape", "ductility" and "compatibility" included in the recovery scale), and the soft/hard ratio showed a significantly negative correlation with each studied feature. When the sky index ranged from 13-36%, tree coverage of the vertical coverage range was 30.28-38.6%, and when the soft/hard ratio ranged from 5-21, the perceived recovery benefit was strongest.

Stable Sequential Activity Underlying the Maintenance of a Precisely Executed Skilled Behavior.

A vast array of motor skills can be maintained throughout life. Do these behaviors require stability of individual neuron tuning or can the output of a given circuit remain constant despite fluctuations in single cells? This question is difficult to address due to the variability inherent in most motor actions studied in the laboratory. A notable exception, however, is the courtship song of the adult zebra finch, which is a learned, highly precise motor act mediated by orderly dynamics within premotor neurons of the forebrain. By longitudinally tracking the activity of excitatory projection neurons during singing using two-photon calcium imaging, we find that both the number and the precise timing of song-related spiking events remain nearly identical over the span of several weeks to months. These findings demonstrate that learned, complex behaviors can be stabilized by maintaining precise and invariant tuning at the level of single neurons.

Learning Biases Underlie "Universals" in Avian Vocal Sequencing.

Biological predispositions in vocal learning have been proposed to underlie commonalities in vocal sequences, including for speech and birdsong, but cultural propagation could also account for such commonalities [1-4]. Songbirds such as the zebra finch learn the sequencing of their acoustic elements ("syllables") during development [5-8]. Zebra finches are not constrained to learn a specific sequence of syllables, but significant consistencies in the positioning and sequencing of syllables have been observed between individuals within populations and between populations [8-10]. To reveal biological predispositions in vocal sequence learning, we individually tutored juvenile zebra finches with randomized and unbiased sequences of syllables and analyzed the extent to which birds produced common sequences. In support of biological predispositions, birds tutored with randomized sequences produced songs with striking similarities. Birds preferentially started and ended their song sequence with particular syllables, consistently positioned shorter and higher frequency syllables in the middle of their song, and sequenced their syllables such that pitch alternated across adjacent syllables. These patterns are reminiscent of those observed in normally tutored birds, suggesting that birds "creolize" aberrant sequence inputs to produce normal sequence outputs. Similar patterns were also observed for syllables that were not used for tutoring (i.e., unlearned syllables), suggesting that motor biases could contribute to sequence learning biases. Furthermore, zebra finches spontaneously produced acoustic patterns that are commonly observed in speech and music, suggesting that sensorimotor processes that are shared across a wide range of vertebrates could underlie these patterns in humans.

Positive effect of dietary lutein and cholesterol on the undirected song activity of an opportunistic breeder.

Song is a sexually selected trait that is thought to be an honest signal of the health condition of an individual in many bird species. For species that breed opportunistically, the quantity of food may be a determinant of singing activity. However, it is not yet known whether the quality of food plays an important role in this respect. The aim of the present study was to experimentally investigate the role of two calorie-free nutrients (lutein and cholesterol) in determining the expression of a sexually selected behavior (song rate) and other behaviors (locomotor activity, self-maintenance activity, eating and resting) in male zebra finches (Taeniopygia guttata). We predicted that males supplemented with lutein and cholesterol would sing at higher rates than controls because both lutein and cholesterol have important health-related physiological functions in birds and birdsong mirrors individual condition. To control for testosterone secretion that may upregulate birdsong, birds were exposed to a decreasing photoperiod. Our results showed that control males down-regulated testosterone in response to a decreasing photoperiod, while birds treated with lutein or cholesterol maintained a constant singing activity. Both lutein- and cholesterol-supplemented groups sang more than control groups by the end of the experiment, indicating that the quality of food can affect undirected song irrespective of circulating testosterone concentrations. None of the other measured behaviors were affected by the treatment, suggesting that, when individuals have full availability of food, sexually selected song traits are more sensitive to the effect of food quality than other behavioral traits. Overall the results support our prediction that undirected song produced by male zebra finches signals access to high-quality food.

Mirrored patterns of lateralized neuronal activation reflect old and new memories in the avian auditory cortex.

In monolingual humans, language-related brain activation shows a distinct lateralized pattern, in which the left hemisphere is often dominant. Studies are not as conclusive regarding the localization of the underlying neural substrate for language in sequential language learners. Lateralization of the neural substrate for first and second language depends on a number of factors including proficiency and early experience with each language. Similar to humans learning speech, songbirds learn their vocalizations from a conspecific tutor early in development. Here, we show mirrored patterns of lateralization in the avian analog of the mammalian auditory cortex (the caudomedial nidopallium [NCM]) in sequentially tutored zebra finches (Taeniopygia guttata​) in response to their first tutor song, learned early in development, and their second tutor song, learned later in development. The greater the retention of song from their first tutor, the more right-dominant the birds were when exposed to that song; the more birds learned from their second tutor, the more left-dominant they were when exposed to that song. Thus, the avian auditory cortex may preserve lateralized neuronal traces of old and new tutor song memories, which are dependent on proficiency of song learning. There is striking resemblance in humans: early-formed language representations are maintained in the brain even if exposure to that language is discontinued. The switching of hemispheric dominance related to the acquisition of early auditory memories and subsequent encoding of more recent memories may be an evolutionary adaptation in vocal learners necessary for the behavioral flexibility to acquire novel vocalizations, such as a second language.

Shared neural substrates for song discrimination in parental and parasitic songbirds.

In many social animals, early exposure to conspecific stimuli is critical for the development of accurate species recognition. Obligate brood parasitic songbirds, however, forego parental care and young are raised by heterospecific hosts in the absence of conspecific stimuli. Having evolved from non-parasitic, parental ancestors, how brood parasites recognize their own species remains unclear. In parental songbirds (e.g. zebra finch Taeniopygia guttata), the primary and secondary auditory forebrain areas are known to be critical in the differential processing of conspecific vs. heterospecific songs. Here we demonstrate that the same auditory brain regions underlie song discrimination in adult brood parasitic pin-tailed whydahs (Vidua macroura), a close relative of the zebra finch lineage. Similar to zebra finches, whydahs showed stronger behavioral responses during conspecific vs. heterospecific song and tone pips as well as increased neural responses within the auditory forebrain, as measured by both functional magnetic resonance imaging (fMRI) and immediate early gene (IEG) expression. Given parallel behavioral and neuroanatomical patterns of song discrimination, our results suggest that the evolutionary transition to brood parasitism from parental songbirds likely involved an "evolutionary tinkering" of existing proximate mechanisms, rather than the wholesale reworking of the neural substrates of species recognition.

Exposure to a novel stimulus environment alters patterns of lateralization in avian auditory cortex.

Perceptual filters formed early in development provide an initial means of parsing the incoming auditory stream. However, these filters may not remain fixed, and may be updated by subsequent auditory input, such that, even in an adult organism, the auditory system undergoes plastic changes to achieve a more efficient representation of the recent auditory environment. Songbirds are an excellent model system for experimental studies of auditory phenomena due to many parallels between song learning in birds and language acquisition in humans. In the present study, we explored the effects of passive immersion in a novel heterospecific auditory environment on neural responses in caudo-medial neostriatum (NCM), a songbird auditory area similar to the secondary auditory cortex in mammals. In zebra finches, a well-studied species of songbirds, NCM responds selectively to conspecific songs and contains a neuronal memory for tutor and other familiar conspecific songs. Adult male zebra finches were randomly assigned to either a conspecific or heterospecific auditory environment. After 2, 4 or 9 days of exposure, subjects were presented with heterospecific and conspecific songs during awake electrophysiological recording. The neural response strength and rate of adaptation to the testing stimuli were recorded bilaterally. Controls exposed to conspecific environment sounds exhibited the normal pattern of hemispheric lateralization with higher absolute response strength and faster adaptation in the right hemisphere. The pattern of lateralization was fully reversed in birds exposed to heterospecific environment for 4 or 9 days and partially reversed in birds exposed to heterospecific environment for 2 days. Our results show that brief passive exposure to a novel category of sounds was sufficient to induce a gradual reorganization of the left and right secondary auditory cortices. These changes may reflect modification of perceptual filters to form a more efficient representation of auditory space.

Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches.

Songbirds use auditory feedback to learn and maintain their songs, but how feedback interacts with vocal motor circuitry remains unclear. A potential site for this interaction is the song premotor nucleus HVC, which receives auditory input and contains neurons (HVCX cells) that innervate an anterior forebrain pathway (AFP) important to feedback-dependent vocal plasticity. Although the singing-related output of HVCX cells is unaltered by distorted auditory feedback (DAF), deafening gradually weakens synapses on HVCX cells, raising the possibility that they integrate feedback only at subthreshold levels during singing. Using intracellular recordings in singing zebra finches, we found that DAF failed to perturb singing-related synaptic activity of HVCX cells, although many of these cells responded to auditory stimuli in non-singing states. Moreover, in vivo multiphoton imaging revealed that deafening-induced changes to HVCX synapses require intact AFP output. These findings support a model in which the AFP accesses feedback independent of HVC. DOI: http://dx.doi.org/10.7554/eLife.01833.001.

Timing vocal behaviour: experimental evidence for song overlap avoidance in Eurasian wrens.

Timing during vocal interactions can play a significant role in terms of audibility as signal overlap may lead to masking of acoustic details for both of the interacting animals as well as for third-party eavesdroppers. Here we investigated timing aspects experimentally in Eurasian wrens (Troglodytes troglodytes) using non-interactive playback. We applied a randomized overlay method incorporating the temporal pattern of singing by the focal bird to establish a null model and to test observed patterns of overlap against this null model. We used different stimulus song rates but temporal response patterns always resulted in significantly lower levels of overlap than expected by chance. The male wrens avoided overlapping by timing their song starts predominately right after the end of stimulus songs, but they did not avoid being overlapped by the stimulus songs. The territorial males typically raised their song rates during and after playback with a tendency to shorten between-song intervals while keeping song durations unchanged. Higher song rates of the playback stimuli increased the extent to which responders were being overlapped by the stimulus songs. Our data provide experimental evidence for a timing ability in Eurasian wrens by which they reduce mutual interference during vocal interactions.

Escalation of aggressive vocal signals: a sequential playback study.

Rival conspecifics often produce stereotyped sequences of signals as agonistic interactions escalate. Successive signals in sequence are thought to convey increasingly pronounced levels of aggressive motivation. Here, we propose and test a model of aggressive escalation in black-throated blue warblers, presenting subjects with two sequential and increasingly elevated levels of threat. From a speaker outside the territorial boundary, we initiated an interaction (low-threat level), and from a second speaker inside the territory, accompanied by a taxidermic mount, we subsequently simulated a territorial intrusion (escalated threat level). Our two main predictions were that signalling behaviours in response to low-threat boundary playback would predict signalling responses to the escalated within-territory threat, and that these latter signalling behaviours would in turn reliably predict attack. We find clear support for both predictions: (i) specific song types (type II songs) produced early in the simulated interaction, in response to boundary playback, predicted later use of low-amplitude 'soft' song, in response to within-territory playback; and (ii) soft song, in turn, predicted attack of the mount. Unexpectedly, use of the early-stage signal (type II song) itself did not predict attack, despite its apparent role in aggressive escalation. This raises the intriguing question of whether type II song can actually be considered a reliable aggressive signal. Overall, our results provide new empirical insights into how songbirds may use progressive vocal signalling to convey increasing levels of threat.