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.

Adult neurogenesis is necessary for functional regeneration of a forebrain neural circuit.

In adult songbirds, new neurons are born in large numbers in the proliferative ventricular zone in the telencephalon and migrate to the adjacent song control region HVC (acronym used as proper name) [A. Reiner et al., J. Comp. Neurol. 473, 377-414 (2004)]. Many of these new neurons send long axonal projections to the robust nucleus of the arcopallium (RA). The HVC-RA circuit is essential for producing stereotyped learned song. The function of adult neurogenesis in this circuit has not been clear. A previous study suggested that it is important for the production of well-structured songs [R. E. Cohen, M. Macedo-Lima, K. E. Miller, E. A. Brenowitz, J. Neurosci. 36, 8947-8956 (2016)]. We tested this hypothesis by infusing the neuroblast migration inhibitor cyclopamine into HVC of male Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) to block seasonal regeneration of the HVC-RA circuit. Decreasing the number of new neurons in HVC prevented both the increase in spontaneous electrical activity of RA neurons and the improved structure of songs that would normally occur as sparrows enter breeding condition. These results show that the incorporation of new neurons into the adult HVC is necessary for the recovery of both electrical activity and song behavior in breeding birds and demonstrate the value of the bird song system as a model for investigating adult neurogenesis at the level of long projection neural circuits.

An Aggressive Interaction Rapidly Increases Brain Androgens in a Male Songbird during the Non-breeding Season.

Aggression is a crucial behavior that impacts access to limited resources in different environmental contexts. Androgens synthesized by the gonads promote aggression during the breeding season. However, aggression can be expressed during the non-breeding season, despite low androgen synthesis by the gonads. The brain can also synthesize steroids ("neurosteroids"), including androgens, which might promote aggression during the non-breeding season. Male song sparrows, Melospiza melodia, are territorial year-round and allow the study of seasonal changes in the steroid modulation of aggression. Here, we quantified steroids following a simulated territorial intrusion (STI) for 10 min in wild adult male song sparrows during the breeding and non-breeding seasons. Using liquid chromatography-tandem mass spectrometry (LC-MS/MS), we examined 11 steroids: pregnenolone, progesterone, corticosterone, dehydroepiandrosterone, androstenedione, testosterone, 5α-dihydrotestosterone, 17ß-estradiol, 17α-estradiol, estriol, and estrone. Steroids were measured in blood and 10 microdissected brain regions that regulate social behavior. In both seasons, STI increased corticosterone in the blood and brain. In the breeding season, STI had no rapid effects on androgens or estrogens. Intriguingly, in the non-breeding season, STI increased testosterone and androstenedione in several behaviorally relevant regions, but not in the blood, where androgens remained non-detectable. Also in the non-breeding season, STI increased progesterone in the blood and specific brain regions. Overall, rapid socially modulated changes in brain steroid levels are more prominent during the non-breeding season. Brain steroid levels vary with season and social context in a region-specific manner and suggest a role for neuroandrogens in aggression during the non-breeding season.

Drosophila females have an acoustic preference for symmetric males.

SignificanceTheoretically, symmetry in bilateral animals is subject to sexual selection, since it can serve as a proxy for genetic quality of competing mates during mate choice. Here, we report female preference for symmetric males in Drosophila, using a mate-choice paradigm where males with environmentally or genetically induced wing asymmetry were competed. Analysis of courtship songs revealed that males with asymmetric wings produced songs with asymmetric features that served as acoustic cues, facilitating this female preference. Females experimentally evolved in the absence of mate choice lost this preference for symmetry, suggesting that it is maintained by sexual selection.

A neural circuit for vocal production responds to viscerosensory input in the songbird.

Motor performance is monitored continuously by specialized brain circuits and used adaptively to modify behavior on a moment-to-moment basis and over longer time periods. During vocal behaviors, such as singing in songbirds, internal evaluation of motor performance relies on sensory input from the auditory and vocal-respiratory systems. Sensory input from the auditory system to the motor system, often referred to as auditory feedback, has been well studied in singing zebra finches (Taeniopygia guttata), but little is known about how and where nonauditory sensory feedback is evaluated. Here we show that brief perturbations in air sac pressure cause short-latency neural responses in the higher-order song control nucleus HVC (used as proper name), an area necessary for song learning and song production. Air sacs were briefly pressurized through a cannula in anesthetized or sedated adult male zebra finches, and neural responses were recorded in both nucleus parambigualis (PAm), a brainstem inspiratory center, and HVC, a cortical premotor nucleus. These findings show that song control nuclei in the avian song system are sensitive to perturbations directly targeted to vocal-respiratory, or viscerosensory, afferents and support a role for multimodal sensory feedback integration in modifying and controlling vocal control circuits.NEW & NOTEWORTHY This study presents the first evidence of sensory input from the vocal-respiratory periphery directly activating neurons in a motor circuit for vocal production in songbirds. It was previously thought that this circuit relies exclusively on sensory input from the auditory system, but we provide groundbreaking evidence for nonauditory sensory input reaching the higher-order premotor nucleus HVC, expanding our understanding of what sensory feedback may be available for vocal control.

Limited Song Mixing Without Genomic Gene Flow in a Contact Zone Between Two Songbird Species.

Song is considered to play an important role in the maintenance of prezygotic reproductive isolation between closely related songbird species. Therefore, song mixing in a contact zone between closely related species is often considered as evidence of hybridization. The Sichuan Leaf Warbler Phylloscopus forresti and the Gansu Leaf Warbler Phylloscopus kansuensis, which diverged 2 million years ago, have formed a contact zone in the south of the Gansu Province of China, where mixed songs have been observed. In this study, we investigated the potential causes and consequences of song mixing by integrating bioacoustic, morphological, mitochondrial, and genomic data with field ecological observations. We found that the two species display no apparent morphological differences, whereas their songs differ dramatically. We demonstrated that ∼11% of the males in the contact zone sang mixed songs. Two males singing mixed song were genotyped, and both were found to be P. kansuensis. Despite the presence of mixed singers, population genomic analyses detected no signs of recent gene flow between the two species, although two possible cases of mitochondrial introgression were identified. We conclude that the rather limited song mixing does not lead to, or result from, hybridization, and hence does not result in the breakdown of reproductive barriers between these cryptic species.

Steroid-dependent plasticity in the song control system: Perineuronal nets and HVC neurogenesis.

The vocal control nucleus HVC in songbirds has emerged as a widespread model system to study adult brain plasticity in response to changes in the hormonal and social environment. I review here studies completed in my laboratory during the last decade that concern two aspects of this plasticity: changes in aggregations of extracellular matrix components surrounding the soma of inhibitory parvalbumin-positive neurons called perineuronal nets (PNN) and the production/incorporation of new neurons. Both features are modulated by the season, age, sex and endocrine status of the birds in correlation with changes in song structure and stability. Causal studies have also investigated the role of PNN and of new neurons in the control of song. Dissolving PNN with chondroitinase sulfate, a specific enzyme applied directly on HVC or depletion of new neurons by focalized X-ray irradiation both affected song structure but the amplitude of changes was limited and deserves further investigations.

Body size shapes song in honeyeaters.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

Chickadees sing different songs in sympatry versus allopatry.

Character displacement theory predicts that closely-related co-occurring species should diverge in relevant traits to reduce costly interspecific interactions such as competition or hybridization. While many studies document character shifts in sympatry, few provide corresponding evidence that these shifts are driven by the costs of co-occurrence. Black-capped (Poecile atricapillus) and mountain chickadees (P. gambeli) are closely-related, ecologically similar, and broadly distributed songbirds with both allopatric and sympatric populations. In sympatry, both species appear to suffer costs of their co-occurrence: 1) both species are in worse body condition compared to allopatry and 2) hybridization sometimes yields sterile offspring. Here, we explored character displacement in the songs of black-capped and mountain chickadees by characterizing variation in male songs from sympatric and allopatric populations. We found that mountain chickadees sing differently in sympatry versus allopatry. Specifically, they produced more notes per song, were more likely to include an extra introductory note, and produced a smaller glissando in their first notes compared to all other populations. Combined with previous research on social dominance and maladaptive hybridization between black-capped and mountain chickadees, we posit that differences in sympatric mountain chickadee song are population-wide shifts to reduce aggression from dominant black-capped chickadees and/or prevent maladaptive hybridization.

A late burst of colour evolution in a radiation of songbirds (Passeriformes: Parulidae) suggests secondary contact drives signal divergence.

Evolutionary radiations provide important insights into species diversification, which is especially true of adaptive radiations. New World wood warblers (Parulidae) are a family of small, insectivorous, forest-dwelling passerine birds, often considered an exemplar of adaptive radiation due to their rapid diversification followed by a slowdown. However, they deviate from the expectations of an adaptive radiation scenario due to the lack of conspicuous morphological and ecological differentiation. We fitted several macroevolutionary models to trait data in 105 species of wood warblers. We tested whether morphological traits underwent an early burst of evolution (suggesting adaptation to new ecological niches in adaptive radiations) and whether song and colour underwent a diversity-dependent acceleration of trait evolutionary rate (consistent with reproductive interference driving signal evolution). Morphology and song evolved gradually under stabilizing selection, suggesting niche conservatism, with morphology possibly acting as a constraint on song evolution. In contrast, many feather colour traits underwent a diversity-dependent burst of evolution occurring late in the clade's history. We suggest that a two-step process has led to the remarkable diversification of wood warblers. First, their early diversification probably proceeded by allopatric speciation. Second, feather colour divergence likely occurred during secondary contact after range expansion. This diversification of signalling traits might have facilitated species coexistence, in combination with behavioural niche partitioning. Wood warblers seem to present characteristics of both adaptive and non-adaptive radiations.

Who you live with and what you duet for: a review of the function of primate duets in relation to their social organization.

Duets are one of the most fascinating displays in animal vocal communication, where two animals fine-tune the timing of their emissions to create a coordinated signal. Duetting behavior is widespread in the animal kingdom and is present in insects, birds, and mammals. Duets are essential to regulate activities within and between social units. Few studies assessed the functions of these vocal emissions experimentally, and for many species, there is still no consensus on what duets are used for. Here, we reviewed the literature on the function of duets in non-human primates, investigating a possible link between the social organization of the species and the function of its duetting behavior. In primates and birds, social conditions characterized by higher promiscuity might relate to the emergence of duetting behavior. We considered both quantitative and qualitative studies, which led us to hypothesize that the shift in the social organization from pair living to a mixed social organization might have led to the emergence of mate defense and mate guarding as critical functions of duetting behavior. Territory/resource ownership and defense functions are more critical in obligate pair-living species. Finally, we encourage future experimental research on this topic to allow the formulation of empirically testable predictions.

Androgen signaling in LMAN regulates song stereotypy in male canaries.

During breeding when testosterone concentrations are high, male songbirds that are open-ended vocal learners like canaries (Serinus canaria) tend to produce a stable, stereotyped song that facilitates mate attraction or territory defense. Outside breeding contexts, song becomes more variable. The neuroendocrine mechanisms controlling this vocal variability across seasons are not entirely clear. We tested whether androgen signaling within the lateral magnocellular nucleus of the anterior nidopallium (LMAN), a cortical-like brain region of the vocal control system known as a vocal variability generator, plays a role in seasonal vocal variability. We first characterized song in birds housed alone on a short day (SD) photoperiod, which simulates non-breeding conditions. Then, cannulae filled with the androgen receptor (AR) blocker flutamide or left empty as control were implanted bilaterally in LMAN. Birds were then transferred to long days (LD) to simulate the breeding season and song was analyzed again. Blocking AR in LMAN increased acoustic variability of song and the acoustic variability of syllables. However, blocking AR in LMAN did not impact the variability of syllable usage nor their sequencing in LD birds, song features that are controlled by androgen signaling in a somatosensory brain region of the vocal control system called HVC. These findings highlight the multifactorial, non-redundant actions of steroid hormones in controlling complex social behaviors such as birdsong. They also support the hypothesis that LMAN is a key brain area for the effects of testosterone on song plasticity both seasonally in adults and during the song crystallization process at sexual maturity.

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.

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.

Translation, cultural adaptation, and validation of the Chinese standardized outcomes in nephrology-hemodialysis fatigue (C-SONG-HD fatigue) scale: a study of Chinese patients undergoing hemodialysis.

OBJECTIVE: This study aimed to translate and culturally adapt the standardized outcomes in nephrology-hemodialysis fatigue (SONG-HD fatigue) scale and to assess the psychometric properties of the Chinese version of the SONG-HD fatigue (C-SONG-HD fatigue) scale. METHODS: Forward and back translations were used to translate the SONG-HD fatigue scale into Chinese. We used the C-SONG-HD fatigue scale to survey Chinese patients undergoing hemodialysis (HD) in China. We examined the distribution of responses and floor and ceiling effects. Cronbach's alpha and McDonald's omega coefficient, intraclass coefficients, and Spearman correlations were used to assess internal consistency reliability, test-retest reliability, and convergent validity, respectively. Responsiveness was also evaluated. RESULTS: In total, 489 participants across southeast China, northwest China, and central China completed the study. The C-SONG-HD fatigue scale had good internal consistency (Cronbach's alpha coefficient 0.861, omega coefficient 0.916), test-retest reliability (intraclass correlation coefficient 0.695), and convergent validity (Spearman correlation 0.691). The analysis of all first-time HD patients did not show notable responsiveness, and only patients with temporary vascular access had good responsiveness with an effect size (ES) of 0.54, a standardized response mean (SRM) of 0.85, and a standard error of measurement (SEM) of 0.77. CONCLUSION: The Chinese version of the SONG-HD fatigue scale showed satisfactory reliability and validity in patients undergoing hemodialysis (HD) in China. It could be used as a tool to measure the fatigue of Chinese HD patients.

Development of the lyrics-based deep learning algorithm for identifying alcohol-related words (LYDIA).

BACKGROUND: Music is an integral part of our lives and is often played in public places like restaurants. People exposed to music that contained alcohol-related lyrics in a bar scenario consumed significantly more alcohol than those exposed to music with less alcohol-related lyrics. Existing methods to quantify alcohol exposure in song lyrics have used manual annotation that is burdensome and time intensive. In this paper, we aim to build a deep learning algorithm (LYDIA) that can automatically detect and identify alcohol exposure and its context in song lyrics. METHODS: We identified 673 potentially alcohol-related words including brand names, urban slang, and beverage names. We collected all the lyrics from the Billboard's top-100 songs from 1959 to 2020 (N = 6110). We developed an annotation tool to annotate both the alcohol-relation of the word (alcohol, non-alcohol, or unsure) and the context (positive, negative, or neutral) of the word in the song lyrics. RESULTS: LYDIA achieved an accuracy of 86.6% in identifying the alcohol-relation of the word, and 72.9% in identifying its context. LYDIA can distinguish with an accuracy of 97.24% between the words that have positive and negative relation to alcohol; and with an accuracy of 98.37% between the positive and negative context. CONCLUSION: LYDIA can automatically identify alcohol exposure and its context in song lyrics, which will allow for the swift analysis of future lyrics and can be used to help raise awareness about the amount of alcohol in music. Highlights Developed a deep learning algorithm (LYDIA) to identify alcohol words in songs. LYDIA achieved an accuracy of 86.6% in identifying alcohol-relation of the words. LYDIA's accuracy in identifying positive, negative, or neutral context was 72.9%. LYDIA can automatically provide evidence of alcohol in millions of songs. This can raise awareness of harms of listening to songs with alcohol words.

Singing in the rain! Climate constraints on the occurrence of indri's song.

The study of how animals adapt their behaviors depending on weather variables has gained particular significance in the context of climate change. This exploration offers insights into endangered species' potential threats and provides information on the direction to take in conservation activities. In this context, noninvasive, cost-effective, and potentially long-term monitoring systems, such as Passive Acoustic Monitoring (PAM), become particularly appropriate. Our study investigates the relationship between weather variables and the vocal behavior of Indri indri, the sole singing lemur species, within Madagascar's Maromizaha New Protected Area. Using PAM, we explore the factors shaping the vocalization patterns of this primate species in response to some environmental factors in their natural habitat. Analysis of an extensive audio data set collected across different years revealed the differential influence of temperature and precipitation on Indri indri vocal activity. We found that rainfall negatively influenced the emission of the vocalizations while warmer temperatures correlated with a greater emission of songs. The various environmental factors we considered also affected the timing of vocal emissions, showing the same pattern. Furthermore, our study confirms, once again, the strength of PAM as a valuable tool for studying vocal animal communication quickly, giving us information about long-term behavioral patterns that would be difficult to get in other ways. This research gives us further valuable information about how indris use vocalizations in their environment and how they adjust to environmental changes.

A synthesis of health benefits of natural sounds and their distribution in national parks.

Parks are important places to listen to natural sounds and avoid human-related noise, an increasingly rare combination. We first explore whether and to what degree natural sounds influence health outcomes using a systematic literature review and meta-analysis. We identified 36 publications examining the health benefits of natural sound. Meta-analyses of 18 of these publications revealed aggregate evidence for decreased stress and annoyance (g = -0.60, 95% CI = -0.97, -0.23) and improved health and positive affective outcomes (g = 1.63, 95% CI = 0.09, 3.16). Examples of beneficial outcomes include decreased pain, lower stress, improved mood, and enhanced cognitive performance. Given this evidence, and to facilitate incorporating public health in US national park soundscape management, we then examined the distribution of natural sounds in relation to anthropogenic sound at 221 sites across 68 parks. National park soundscapes with little anthropogenic sound and abundant natural sounds occurred at 11.3% of the sites. Parks with high visitation and urban park sites had more anthropogenic sound, yet natural sounds associated with health benefits also were frequent. These included animal sounds (audible for a mean of 59.3% of the time, SD: 23.8) and sounds from wind and water (mean: 19.2%, SD: 14.8). Urban and other parks that are extensively visited offer important opportunities to experience natural sounds and are significant targets for soundscape conservation to bolster health for visitors. Our results assert that natural sounds provide important ecosystem services, and parks can bolster public health by highlighting and conserving natural soundscapes.

The influence of self-generated song during aggression on brain serotonin levels in male crickets.

Pairs of adult male crickets, Gryllus bimaculatus, fight and immediately determine winner and loser statuses. The winner male repeatedly produces an aggressive (rival) song by rubbing his forewings together. In this study, I removed the plectrum, a sound-producing structure in the forewing, from male crickets and measured their brain serotonin (5-hydroxytryptamine: 5-HT) levels immediately after a 10-min aggressive interaction. Pairs of plectrum-removed males fought and established clear winner-loser relationships, like the case of intact males. The plectrum-removed winner males frequently rubbed their forewings together, but were unable to produce song. Aggressive interaction reduced significantly brain 5-HT levels in the plectrum-removed males, regardless of their winner and loser statuses. Furthermore, the reduction of brain 5-HT was detected primarily in the central body, a group of neuropils spanning the midline of the brain. In contrast, in pairs of intact males, aggressive interaction reduced brain 5-HT levels in the loser males, but not in the winner males. Plectrum removal alone did not affect the brain's 5-HT levels. These results suggest that aggressive song emitted by the winner male cricket prevents the reduction of 5-HT levels in his own brain, especially in the central body.

[Analysis of male reproduction based on the "inner kidney and outer kidney" theory advanced by nation-famous Chinese medicine Professor XU Fu-song].

Based on the traditional Chinese medicine theories and modern medical theories, Professor XU Fu-song, a famous veteran Chinese medicine physician in China, established the theory of "inner kidney and outer kidney", emphasizing concomitant treatment of inner kidney and outer kidney, which plays an important guiding role in deepening the understanding of the pathogenesis and clinical diagnosis and treatment of male infertility. This article summarizes the relevant academic thoughts and experiences of Professor XU, with an analysis of his advanced ideas in the field of male reproduction.