Daily singing of adult songbirds functions to maintain song performance independently of auditory feedback and age.

Many songbirds learn to produce songs through vocal practice in early life and continue to sing daily throughout their lifetime. While it is well-known that adult songbirds sing as part of their mating rituals, the functions of singing behavior outside of reproductive contexts remain unclear. Here, we investigated this issue in adult male zebra finches by suppressing their daily singing for two weeks and examining the effects on song performance. We found that singing suppression decreased the pitch, amplitude, and duration of songs, and that those song features substantially recovered through subsequent free singing. These reversible song changes were not dependent on auditory feedback or the age of the birds, contrasting with the adult song plasticity that has been reported previously. These results demonstrate that adult song structure is not stable without daily singing, and suggest that adult songbirds maintain song performance by preventing song changes through physical act of daily singing throughout their life. Such daily singing likely functions as vocal training to maintain the song production system in optimal conditions for song performance in reproductive contexts, similar to how human singers and athletes practice daily to maintain their performance.

The ecology of zebra finch song and its implications for vocal communication in multi-level societies.

Acoustic signalling is crucial in affecting movements and in social interactions. In species with dynamic social structures, such as multi-level societies, acoustic signals can provide a key mechanism allowing individuals to identify and find or avoid each other and to exchange information. Yet, if the spacing between individuals regularly exceeds the maximum signalling range, the relation between movements and signals becomes more complex. As the best-studied songbird in captivity, the zebra finch (Taeniopygia castanotis) is a species with individually distinct songs that are audible over just a few metres and a widely ranging dynamic multi-level social organization in the wild, raising questions on the actual role of its song in social cohesion and coordination. Here, we provide an overview of birdsong in social organizations (networks) and use the ecology of the zebra finch and male song to discuss how singing can facilitate social cohesion and coordination in species where the signal range is very short. We raise the question of the extent to which zebra finches are a representative species to understand the function of song in communication, and we broaden current views on the function of birdsong and its individual signature. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Conserved regulatory switches for the transition from natal down to juvenile feather in birds.

The transition from natal downs for heat conservation to juvenile feathers for simple flight is a remarkable environmental adaptation process in avian evolution. However, the underlying epigenetic mechanism for this primary feather transition is mostly unknown. Here we conducted time-ordered gene co-expression network construction, epigenetic analysis, and functional perturbations in developing feather follicles to elucidate four downy-juvenile feather transition events. We report that extracellular matrix reorganization leads to peripheral pulp formation, which mediates epithelial-mesenchymal interactions for branching morphogenesis. α-SMA (ACTA2) compartmentalizes dermal papilla stem cells for feather renewal cycling. LEF1 works as a key hub of Wnt signaling to build rachis and converts radial downy to bilateral symmetry. Novel usage of scale keratins strengthens feather sheath with SOX14 as the epigenetic regulator. We show that this primary feather transition is largely conserved in chicken (precocial) and zebra finch (altricial) and discuss the possibility that this evolutionary adaptation process started in feathered dinosaurs.

A novel skin cancer detection model using modified finch deep CNN classifier model.

Skin cancer is one of the most life-threatening diseases caused by the abnormal growth of the skin cells, when exposed to ultraviolet radiation. Early detection seems to be more crucial for reducing aberrant cell proliferation because the mortality rate is rapidly rising. Although multiple researches are available based on the skin cancer detection, there still exists challenges in improving the accuracy, reducing the computational time and so on. In this research, a novel skin cancer detection is performed using a modified falcon finch deep Convolutional neural network classifier (Modified Falcon finch deep CNN) that efficiently detects the disease with higher efficiency. The usage of modified falcon finch deep CNN classifier effectively analyzed the information relevant to the skin cancer and the errors are also minimized. The inclusion of the falcon finch optimization in the deep CNN classifier is necessary for efficient parameter tuning. This tuning enhanced the robustness and boosted the convergence of the classifier that detects the skin cancer in less stipulated time. The modified falcon finch deep CNN classifier achieved accuracy, sensitivity, and specificity values of 93.59%, 92.14%, and 95.22% regarding k-fold and 96.52%, 96.69%, and 96.54% regarding training percentage, proving more effective than literary works.

Captivity affects mitochondrial aerobic respiration and carotenoid metabolism in the house finch (Haemorhous mexicanus).

In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation can be an honest signal of individual quality. However, the physiological basis for associations between organism function and the metabolism of red ornamental carotenoids from yellow dietary carotenoids remains uncertain. A recent hypothesis posits that carotenoid metabolism depends on mitochondrial performance, with diminished red coloration resulting from altered mitochondrial aerobic respiration. To test for an association between mitochondrial respiration and red carotenoids, we held wild-caught, molting male house finches in either small bird cages or large flight cages to create environmental challenges during the period when red ornamental coloration is produced. We predicted that small cages would present a less favorable environment than large flight cages and that captivity itself would decrease both mitochondrial performance and the abundance of red carotenoids compared with free-living birds. We found that captive-held birds circulated fewer red carotenoids, showed increased mitochondrial respiratory rates, and had lower complex II respiratory control ratios - a metric associated with mitochondrial efficiency - compared with free-living birds, though we did not detect a difference in the effects of small cages versus large cages. Among captive individuals, the birds that circulated the highest concentrations of red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrate. These data support the hypothesis that the metabolism of red carotenoid pigments is linked to mitochondrial aerobic respiration in the house finch, but the mechanisms for this association remain to be established.

Window into the songbird brain reveals superdiffusive migration of adult-born neurons.

In a recent study, Shvedov and colleagues used live two-photon imaging in transgenic zebra finches to reveal migration patterns of neuroblasts through the complex environment of the postembryonic brain. This study highlights the value of ubiquitin C/green fluorescent protein (UBC-GFP) transgenic zebra finches in studying adult neurogenesis and advances our understanding of dispersed long-distance neuronal migration in the adult brain, shedding light on this understudied phenomenon.

Auditory discrimination learning and acoustic cue weighing in female zebra finches with localized FoxP1 knockdowns.

Rare disruptions of the transcription factor FOXP1 are implicated in a human neurodevelopmental disorder characterized by autism and/or intellectual disability with prominent problems in speech and language abilities. Avian orthologues of this transcription factor are evolutionarily conserved and highly expressed in specific regions of songbird brains, including areas associated with vocal production learning and auditory perception. Here, we investigated possible contributions of FoxP1 to song discrimination and auditory perception in juvenile and adult female zebra finches. They received lentiviral knockdowns of FoxP1 in one of two brain areas involved in auditory stimulus processing, HVC (proper name) or CMM (caudomedial mesopallium). Ninety-six females, distributed over different experimental and control groups were trained to discriminate between two stimulus songs in an operant Go/Nogo paradigm and subsequently tested with an array of stimuli. This made it possible to assess how well they recognized and categorized altered versions of training stimuli and whether localized FoxP1 knockdowns affected the role of different features during discrimination and categorization of song. Although FoxP1 expression was significantly reduced by the knockdowns, neither discrimination of the stimulus songs nor categorization of songs modified in pitch, sequential order of syllables or by reversed playback were affected. Subsequently, we analyzed the full dataset to assess the impact of the different stimulus manipulations for cue weighing in song discrimination. Our findings show that zebra finches rely on multiple parameters for song discrimination, but with relatively more prominent roles for spectral parameters and syllable sequencing as cues for song discrimination.NEW & NOTEWORTHY In humans, mutations of the transcription factor FoxP1 are implicated in speech and language problems. In songbirds, FoxP1 has been linked to male song learning and female preference strength. We found that FoxP1 knockdowns in female HVC and caudomedial mesopallium (CMM) did not alter song discrimination or categorization based on spectral and temporal information. However, this large dataset allowed to validate different cue weights for spectral over temporal information for song recognition.

Urbanization alters the song propagation of two human-commensal songbird species.

Urban expansion has increased pollution, including both physical (e.g., exhaust, litter) and sensory (e.g., anthropogenic noise) components. Urban avian species tend to increase the frequency and/or amplitude of songs to reduce masking by low-frequency noise. Nevertheless, song propagation to the receiver can also be constrained by the environment. We know relatively little about how this propagation may be altered across species that (1) vary in song complexity and (2) inhabit areas along an urbanization gradient. We investigated differences in song amplitude, attenuation, and active space, or the maximum distance a receiver can detect a signal, in two human-commensal species: the house sparrow (Passer domesticus) and house finch (Haemorhous mexicanus). We described urbanization both discretely and quantitatively to investigate the habitat characteristics most responsible for propagation changes. We found mixed support for our hypothesis of urban-specific degradation of songs. Urban songs propagated with higher amplitude; however, urban song fidelity was species-specific and showed lowered active space for urban house finch songs. Taken together, our results suggest that urban environments may constrain the propagation of vocal signals in species-specific manners. Ultimately, this has implications for the ability of urban birds to communicate with potential mates or kin.

Goal-directed and flexible modulation of syllable sequence within birdsong.

Songs constitute a complex system of vocal signals for inter-individual communication in songbirds. Here, we elucidate the flexibility which songbirds exhibit in the organizing and sequencing of syllables within their songs. Utilizing a newly devised song decoder for quasi-real-time annotation, we execute an operant conditioning paradigm, with rewards contingent upon specific syllable syntax. Our analysis reveals that birds possess the capacity to modify the contents of their songs, adjust the repetition length of particular syllables and employing specific motifs. Notably, birds altered their syllable sequence in a goal-directed manner to obtain rewards. We demonstrate that such modulation occurs within a distinct song segment, with adjustments made within 10 minutes after cue presentation. Additionally, we identify the involvement of the parietal-basal ganglia pathway in orchestrating these flexible modulations of syllable sequences. Our findings unveil an unappreciated aspect of songbird communication, drawing parallels with human speech.

The role of cerebellum in learned vocal communication in adult songbirds.

Injury, tumors, ischemia, and lesions in the cerebellum show the involvement of this region in human speech. The association of the cerebellum with learned birdsong has only been identified recently. Cerebellar dysfunction in young songbirds causes learning disabilities, but its role in adult songbirds has not been established. The aim of this study was to investigate the role of the deep cerebellar nuclei (DCN) in adult birdsong. We created bilateral excitotoxic lesions in the DCN of adult male zebra finches (Taeniopygia guttata) and recorded their songs for up to 4 months. Using magnetic resonance imaging (MRI) and immunohistochemistry, we validated the lesion efficacy. We found that the song duration significantly increased from 14 weeks post-op; the increase in duration was caused by a greater number of introductory notes as well as a greater number of syllables sung after the introductory notes. On the other hand, the motif duration decreased from 8 weeks after DCN lesions were induced, which was due to faster singing of syllables, not changes in inter-syllable interval length. DCN lesions also caused a decrease in the fundamental frequency of syllables. In summary, we showed that DCN lesions influence the temporal and acoustic features of birdsong. These results suggest that the cerebellum influences singing in adult songbirds.

A sound beginning of life starts before birth.

Long-term impact from prenatal noise exposure in birds should raise general concern.

Babbling opens the sensory phase for imitative vocal learning.

Zebra finches, a species of songbirds, learn to sing by creating an auditory template through the memorization of model songs (sensory learning phase) and subsequently translating these perceptual memories into motor skills (sensorimotor learning phase). It has been traditionally believed that babbling in juvenile birds initiates the sensorimotor phase while the sensory phase of song learning precedes the onset of babbling. However, our findings challenge this notion by demonstrating that testosterone-induced premature babbling actually triggers the onset of the sensory learning phase instead. We reveal that juvenile birds must engage in babbling and self-listening to acquire the tutor song as the template. Notably, the sensory learning of the template in songbirds requires motor vocal activity, reflecting the observation that prelinguistic babbling in humans plays a crucial role in auditory learning for language acquisition.

Pre- and postnatal noise directly impairs avian development, with fitness consequences.

Noise pollution is expanding at an unprecedented rate and is increasingly associated with impaired reproduction and development across taxa. However, whether noise sound waves are intrinsically harmful for developing young-or merely disturb parents-and the fitness consequences of early exposure remain unknown. Here, by only manipulating the offspring, we show that sole exposure to noise in early life in zebra finches has fitness consequences and causes embryonic death during exposure. Exposure to pre- and postnatal traffic noise cumulatively impaired nestling growth and physiology and aggravated telomere shortening across life stages until adulthood. Consistent with a long-term somatic impact, early life noise exposure, especially prenatally, decreased individual offspring production throughout adulthood. Our findings suggest that the effects of noise pollution are more pervasive than previously realized.

Language-like efficiency and structure in house finch song.

Communication needs to be complex enough to be functional while minimizing learning and production costs. Recent work suggests that the vocalizations and gestures of some songbirds, cetaceans and great apes may conform to linguistic laws that reflect this trade-off between efficiency and complexity. In studies of non-human communication, though, clustering signals into types cannot be done a priori, and decisions about the appropriate grain of analysis may affect statistical signals in the data. The aim of this study was to assess the evidence for language-like efficiency and structure in house finch (Haemorhous mexicanus) song across three levels of granularity in syllable clustering. The results show strong evidence for Zipf's rank-frequency law, Zipf's law of abbreviation and Menzerath's law. Additional analyses show that house finch songs have small-world structure, thought to reflect systematic structure in syntax, and the mutual information decay of sequences is consistent with a combination of Markovian and hierarchical processes. These statistical patterns are robust across three levels of granularity in syllable clustering, pointing to a limited form of scale invariance. In sum, it appears that house finch song has been shaped by pressure for efficiency, possibly to offset the costs of female preferences for complexity.

Male and female syringeal muscles exhibit superfast shortening velocities in zebra finches.

Vocalisations play a key role in the communication behaviour of many vertebrates. Vocal production requires extremely precise motor control, which is executed by superfast vocal muscles that can operate at cycle frequencies over 100 Hz and up to 250 Hz. The mechanical performance of these muscles has been quantified with isometric performance and the workloop technique, but owing to methodological limitations we lack a key muscle property characterising muscle performance, the force-velocity relationship. Here, we quantified the force-velocity relationship in zebra finch superfast syringeal muscles using the isovelocity technique and tested whether the maximal shortening velocity is different between males and females. We show that syringeal muscles exhibit high maximal shortening velocities of 25L0 s-1 at 30°C. Using Q10-based extrapolation, we estimate they can reach 37-42L0 s-1 on average at body temperature, exceeding other vocal and non-avian skeletal muscles. The increased speed does not adequately compensate for reduced force, which results in low power output. This further highlights the importance of high-frequency operation in these muscles. Furthermore, we show that isometric properties positively correlate with maximal shortening velocities. Although male and female muscles differ in isometric force development rates, maximal shortening velocity is not sex dependent. We also show that cyclical methods to measure force-length properties used in laryngeal studies give the same result as conventional stepwise methodologies, suggesting either approach is appropriate. We argue that vocal behaviour may be affected by the high thermal dependence of superfast vocal muscle performance.

Impact of filgotinib on pain control in the phase 3 FINCH studies.

OBJECTIVE: This post hoc analysis of the FINCH 1-3 (NCT02889796, NCT02873936 and NCT02886728) studies assessed specific effects of filgotinib on pain control and their relationship with other aspects of efficacy in patients with rheumatoid arthritis (RA). METHODS: Assessments included: residual pain responses of ≤10 and ≤20 mm on a 100 mm visual analogue scale (VAS); the proportion of patients who achieved VAS pain responses in addition to remission or low disease activity by Disease Activity Score-28 with C-reactive protein (DAS28-CRP) or Clinical Disease Activity Index (CDAI) criteria. RESULTS: Across studies, filgotinib reduced pain from week 2, with responses sustained throughout the studies. In FINCH 1, at week 24, 35.8%, 25.0%, 24.6% and 11.6% of patients in the filgotinib 200 mg, filgotinib 100 mg, adalimumab and placebo arms (each plus methotrexate) achieved VAS pain ≤20 mm in addition to DAS28-CRP remission; 26.3%, 17.9%, 17.2% and 7.6% achieved VAS pain ≤10 mm in addition to DAS28-CRP remission. A similar pattern was seen for CDAI remission. Time during which VAS pain was ≤10 or ≤20 mm was longest with filgotinib 200 mg and comparable between adalimumab and filgotinib 100 mg. Similar findings were reported for filgotinib in FINCH 2 and 3. CONCLUSION: In all RA populations studied, pain improvements occurred from week 2 and were sustained over time. In FINCH 1, filgotinib 100 mg provided similar pain amelioration to adalimumab, whereas filgotinib 200 mg resulted in greater pain improvement and higher proportion of patients with residual pain ≤10 or ≤20 mm and meeting DAS28-CRP remission criteria.

The hidden fitness of the male zebra finch courtship song.

Vocal learning in songbirds is thought to have evolved through sexual selection, with female preference driving males to develop large and varied song repertoires1-3. However, many songbird species learn only a single song in their lifetime4. How sexual selection drives the evolution of single-song repertoires is not known. Here, by applying dimensionality-reduction techniques to the singing behaviour of zebra finches (Taeniopygia guttata), we show that syllable spread in low-dimensional feature space explains how single songs function as honest indicators of fitness. We find that this Gestalt measure of behaviour captures the spectrotemporal distinctiveness of song syllables in zebra finches; that females strongly prefer songs that occupy more latent space; and that matching path lengths in low-dimensional space is difficult for young males. Our findings clarify how simple vocal repertoires may have evolved in songbirds and indicate divergent strategies for how sexual selection can shape vocal learning.

Constant light and pinealectomy disrupt daily rhythm in song production and negatively impact reproductive performance in zebra finches.

We assessed the circadian clock control of singing and reproductive performance in zebra finches. Experiment 1 examined changes in body mass, testis size, and plasma corticosterone and testosterone levels in male birds exposed to constant light (LL, 100 lx) and constant darkness (DD, 0.5 lx), with controls on 12L:12D (L = 100 lx, D = 0.5 lx). There was a significant increase in the body mass and testis size under LL and a decrease in testis size under the DD. Using a similar design, experiment 2 assessed the persistence of the circadian rhythm in singing along with activity-rest pattern in cohort I birds that were entrained to 12L:12D and subsequently released in DD or LL, and in cohort II birds that were entrained to 12L:12D and following pinealectomy were released in DD. Both activity and singing patterns were synchronized with the light phase under 12L:12D, free-ran with a circadian period under DD, and were arrhythmic under the LL. There was an overall decreased and increased effect on singing under DD and LL, respectively, albeit with differences in various song parameters. The pinealectomy disrupted both activity and singing rhythms but did not affect singing or the overall song features. Pinealectomized bird pairs also exhibited a significant reduction in their nest-building and breeding efforts, resulting in a compromised reproductive performance. These results suggest a circadian clock control of singing and more importantly demonstrate a role of the pineal clock in breeding behaviors, leading to a compromised reproductive performance in diurnal zebra finches.

Tracing the development of learned song preferences in the female zebra finch brain with functional magnetic resonance imaging.

In sexually dimorphic zebra finches (Taeniopygia guttata), only males learn to sing their father's song, whereas females learn to recognize the songs of their father or mate but cannot sing themselves. Memory of learned songs is behaviorally expressed in females by preferring familiar songs over unfamiliar ones. Auditory association regions such as the caudomedial mesopallium (CMM; or caudal mesopallium) have been shown to be key nodes in a network that supports preferences for learned songs in adult females. However, much less is known about how song preferences develop during the sensitive period of learning in juvenile female zebra finches. In this study, we used blood-oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to trace the development of a memory-based preference for the father's song in female zebra finches. Using BOLD fMRI, we found that only in adult female zebra finches with a preference for learned song over novel conspecific song, neural selectivity for the father's song was localized in the thalamus (dorsolateral nucleus of the medial thalamus; part of the anterior forebrain pathway, AFP) and in CMM. These brain regions also showed a selective response in juvenile female zebra finches, although activation was less prominent. These data reveal that neural responses in CMM, and perhaps also in the AFP, are shaped during development to support behavioral preferences for learned songs.

Abnormal Feather Phenotype Associated with a Fatal Stress Response and Unusual Tolerance to Human Contact in the Zebra Finch (Taeniopygia castanotis).

The zebra finch (Taeniopygia castanotis) is a songbird sold in the pet trade and commonly used in research. In this report, we describe a set of partially overlapping traits shared by 3 birds in 2 broods from the same nest box that included atypical morphologic, developmental, and behavioral characteristics. The most obvious feature of this novel phenotype was feathers exhibiting a clumped appearance, which was accompanied by slow growth, delayed expression of adult plumage traits, and tameness, which we define as a lack of escape response upon handling without behavioral indicators of stress such as rapid breathing. Surprisingly, these birds also displayed a fatal response to nonhuman stressors. In one brood, a male expressed all of these characteristics, 2 females were wild-type, and a male sibling expressed only a hyperactive stress response but was otherwise normal. This indicates that the stress response could be inherited independently of the other abnormalities found in the male nest mate. In a second brood, a male bearing the abnormal feather phenotype behaved similarly to the male in the first brood, supporting the possibility that tameness is genetically associated with the unusual feather phenotype. The 2 other male and 2 female nest mates from this brood were behaviorally and visually normal, although the females developed slowly. Although similar traits have appeared in the aviary previously, such as slow development and small size, these are the first cases documented in detail. This correlated suite of traits suggests a linkage among altered feather growth, developmental rate, and brain and/or physiologic traits influencing normal fear and stress responses in the zebra finch. Awareness and study of the mechanism(s) linking these traits by examination of underlying genetic or environmental factors will allow a better understanding of the relationship between physical and behavioral traits in domesticated laboratory animals.