Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication.

In many species, vocal communication is essential for coordinating social behaviors including courtship, mating, parenting, rivalry, and alarm signaling. Effective communication requires accurate production, detection, and classification of signals, as well as selection of socially appropriate responses. Understanding how signals are generated and how acoustic signals are perceived is key to understanding the neurobiology of social behaviors. Here we review our long-standing research program focused on Xenopus, a frog genus which has provided valuable insights into the mechanisms and evolution of vertebrate social behaviors. In Xenopus laevis, vocal signals differ between the sexes, through development, and across the genus, reflecting evolutionary divergence in sensory and motor circuits that can be interrogated mechanistically. Using two ex vivo preparations, the isolated brain and vocal organ, we have identified essential components of the vocal production system: the sexually differentiated larynx at the periphery, and the hindbrain vocal central pattern generator (CPG) centrally, that produce sex- and species-characteristic sound pulse frequencies and temporal patterns, respectively. Within the hindbrain, we have described how intrinsic membrane properties of neurons in the vocal CPG generate species-specific vocal patterns, how vocal nuclei are connected to generate vocal patterns, as well as the roles of neurotransmitters and neuromodulators in activating the circuit. For sensorimotor integration, we identified a key forebrain node that links auditory and vocal production circuits to match socially appropriate vocal responses to acoustic features of male and female calls. The availability of a well supported phylogeny as well as reference genomes from several species now support analysis of the genetic architecture and the evolutionary divergence of neural circuits for vocal communication. Xenopus thus provides a vertebrate model in which to study vocal communication at many levels, from physiology, to behavior, and from development to evolution. As one of the most comprehensively studied phylogenetic groups within vertebrate vocal communication systems, Xenopus provides insights that can inform social communication across phyla.

Clinical pregnancy rates and experience with in vitro fertilization after uterus transplantation: Dallas Uterus Transplant Study.

BACKGROUND: The clinical pregnancy rates among patients with uterus transplantation have been reported by only a limited number of centers, and those centers have not used preimplantation genetic testing for aneuploidy in their protocol. OBJECTIVE: This study examined clinical pregnancy rates among women with absolute uterine-factor infertility undergoing in vitro fertilization using good-quality, expanded-blastocyst-stage, euploid embryos after uterus transplantation. STUDY DESIGN: This cohort observational study involved 20 women who underwent uterus transplantation over 3 years. Notably, 14 of these patients had successful transplants and were followed prospectively for a median of 14.1 months (range, 11-34.8 months). In vitro fertilization was performed before subjects underwent uterus transplantation, and good-quality expanded-blastocyst-stage euploid embryos were obtained and frozen for future embryo transfer. Interventions consisted of in vitro fertilization, preimplantation genetic testing for aneuploidy, uterus transplantation, and frozen embryo transfer. RESULTS: All 14 subjects with successful transplants underwent single embryo transfer of a warmed, good-quality, euploid, expanded blastocyst and had at least 1 documented clinical pregnancy within the uterus. In 71.4%, the first embryo transfer resulted in clinical pregnancy. The median time from successful uterus transplantation to first embryo transfer was 4.5 months; from successful uterus transplantation to first clinical pregnancy, 7.3 months; and from successful uterus transplantation to first live birth, 14.1 months. A total of 13 live births have occurred in 12 subjects. CONCLUSION: Women with absolute uterine-factor infertility who have surgically successful uterus transplantation and in vitro fertilization using preimplantation genetic testing for aneuploidy can achieve high clinical pregnancy rates. We have reduced the time interval from uterus transplantation to embryo transfer by at least 50% and the interval from uterus transplantation to clinical pregnancy by >6 months compared with previous studies. We believe our approach may shorten the time from transplant to clinical pregnancy and therefore decrease patient exposure to immunosuppressant therapies.

Novel system of communication in crickets originated at the same time as bat echolocation and includes male-male multimodal communication.

Understanding the evolutionary origins of communication signals requires careful study of multiple species within a known phylogenetic framework. Most cricket species produce low-frequency calls for mate attraction, whereas they startle to high-frequency sounds similar to bat echolocation. Male crickets in the tribe Lebinthini produce high-frequency calls, to which females reply with vibrational signals. This novel communication system likely evolved by male sensory exploitation of acoustic startle to high-frequency sounds in females. This behavior was previously described for the Lebinthini from Asia. Here we demonstrate that this novel communication system is found in a Neotropical species, Ponca hebardi, and is therefore likely shared by the whole tribe Lebinthini, dating the origin of this behavior to coincide with the origin of echolocation in bats. Furthermore, we document male duets involving both acoustic and vibratory signals not previously described in crickets, and we tentatively interpret it as competitive masking between males.

Taking turns: bridging the gap between human and animal communication.

Language, humans' most distinctive trait, still remains a 'mystery' for evolutionary theory. It is underpinned by a universal infrastructure-cooperative turn-taking-which has been suggested as an ancient mechanism bridging the existing gap between the articulate human species and their inarticulate primate cousins. However, we know remarkably little about turn-taking systems of non-human animals, and methodological confounds have often prevented meaningful cross-species comparisons. Thus, the extent to which cooperative turn-taking is uniquely human or represents a homologous and/or analogous trait is currently unknown. The present paper draws attention to this promising research avenue by providing an overview of the state of the art of turn-taking in four animal taxa-birds, mammals, insects and anurans. It concludes with a new comparative framework to spur more research into this research domain and to test which elements of the human turn-taking system are shared across species and taxa.

Deceptive vocal duets and multimodal display in a songbird.

Many group-living animals cooperatively signal to defend resources, but what stops deceptive signalling to competitors about coalition strength? Cooperative-signalling species include mated pairs of birds that sing duets to defend their territory. Individuals of these species sometimes sing 'pseudo-duets' by mimicking their partner's contribution, but it is unknown if these songs are deceptive, or why duets are normally reliable. We studied pseudo-duets in Australian magpie-larks, Grallina cyanoleuca, and tested whether multimodal signalling constrains deception. Magpie-larks give antiphonal duets coordinated with a visual display, with each sex typically choosing a different song type within the duet. Individuals produced pseudo-duets almost exclusively during nesting when partners were apart, but the two song types were used in sequence rather than antiphonally. Strikingly, birds hid and gave no visual displays, implying deceptive suppression of information. Acoustic playbacks showed that pseudo-duets provoked the same response from residents as true duets, regardless of whether they were sequential or antiphonal, and stronger response than that to true duets consisting of a single song type. By contrast, experiments with robot models showed that songs accompanied by movements of two birds prompted stronger responses than songs accompanied by movements of one bird, irrespective of the number of song types or singers. We conclude that magpie-larks used deceptive pseudo-duets when partners were apart, and suppressed the visual display to maintain the subterfuge. We suggest that the visual component of many species' duets provides the most reliable information about the number of signallers and may have evolved to maintain honesty in duet communication.

Corrigendum: Neural mechanisms for turn-taking in duetting plain-tailed wrens.

[This corrects the article DOI: 10.3389/fncir.2022.970434.].

Neural mechanisms for turn-taking in duetting plain-tailed wrens.

Recent studies conducted in the natural habitats of songbirds have provided new insights into the neural mechanisms of turn-taking. For example, female and male plain-tailed wrens (Pheugopedius euophrys) sing a duet that is so precisely timed it sounds as if a single bird is singing. In this review, we discuss our studies examining the sensory and motor cues that pairs of wrens use to coordinate the rapid alternation of syllable production. Our studies included behavioral measurements of freely-behaving wrens in their natural habitat and neurophysiological experiments conducted in awake and anesthetized individuals at field sites in Ecuador. These studies show that each partner has a pattern-generating circuit in their brain that is linked via acoustic feedback between individuals. A similar control strategy has been described in another species of duetting songbird, white-browed sparrow-weavers (Plocepasser mahali). Interestingly, the combination of neurophysiological results from urethane-anesthetized and awake wrens suggest a role for inhibition in coordinating the timing of turn-taking. Finally, we highlight some of the unique challenges of conducting these experiments at remote field sites.

The effect of noise variation over time and between populations on the fine spectrotemporal characteristics of different vocalization types.

Noise affects the recognition of acoustic signals by masking information. To compensate for increased noise, individuals often increase the minimum frequency of their vocalization to reduce noise interference. Our goal was to analyze the effect of noise on the characteristics of different bird vocalizations, through a comparative study of vocalizations on the same bird species. We analyzed the effects of noise variation on the fine spectrotemporal characteristics of calls, songs, and duets of White-eared Ground-sparrows (Melozone leucotis) across three populations over a three-year period. We recorded vocalizations and noise levels simultaneously from 41 territories between 2012 and 2014. We measured the duration, minimum, maximum, and maximum amplitude frequency, and counted the number of songs elements for each vocalization recorded. As we predicted, noise influences the minimum frequency of song, but did not have an effect on the fine spectrotemporal characteristics for calls and duets. We did, however, find that low and high frequency of calls and duets increased with noise-population-year interaction. Our results suggest that differences in noise values at each population were inadequate to observe changes in vocalization characteristics. In conclusion, evaluating responses to different noise levels on different vocalization types for the same species expands our understanding of the flexibility of birds to adjust vocalizations in response to anthropogenic noise.

Behavioral, morphological, and ecological trait evolution in two clades of New World Sparrows (Aimophila and Peucaea, Passerellidae).

The New World sparrows (Passerellidae) are a large, diverse group of songbirds that vary in morphology, behavior, and ecology. Thus, they are excellent for studying trait evolution in a phylogenetic framework. We examined lability versus conservatism in morphological and behavioral traits in two related clades of sparrows (Aimophila, Peucaea), and assessed whether habitat has played an important role in trait evolution. We first inferred a multi-locus phylogeny which we used to reconstruct ancestral states, and then quantified phylogenetic signal among morphological and behavioral traits in these clades and in New World sparrows more broadly. Behavioral traits have a stronger phylogenetic signal than morphological traits. Specifically, vocal duets and song structure are the most highly conserved traits, and nesting behavior appears to be maintained within clades. Furthermore, we found a strong correlation between open habitat and unpatterned plumage, complex song, and ground nesting. However, even within lineages that share the same habitat type, species vary in nesting, plumage pattern, song complexity, and duetting. Our findings highlight trade-offs between behavior, morphology, and ecology in sparrow diversification.

Structure and functions of Yellow-breasted Boubou (Laniarius atroflavus) solos and duets.

BACKGROUND: Birds have extremely well-developed acoustic communication and have become popular in bioacoustics research. The majority of studies on bird song have been conducted in the temperate zones where usually males of birds sing to attract females and defend territories. In over 360 bird species mostly inhabiting the tropics both males and females sing together in duets. Avian duets are usually formed when a male and female coordinate their songs. We focused on a species with relatively weakly coordinated duets, with male solo as the prevailing vocalisation type. METHODS: Instead of analysing a set of recordings spread over a long time, we analysed whole day microphone-array recordings of the Yellow-breasted Boubou (Laniarius atroflavus), a species endemic to West African montane rainforests. We described the structure of the solo and duet vocalisations and temporal characteristics of daily activity based on 5,934 vocal bouts of 18 focal pairs and their neighbours. RESULTS: Birds had small, sex specific repertoires. All males shared three types of loud whistles functioning as song type repertoires in both solos and duets. Females vocalised with five types of harsh, atonal notes with a more variable and usually lower amplitude. Three of them were produced both as solos and in duets, while two seem to function as alarm and excitement calls given almost exclusively as a solo. Solos were the most common vocalisation mode (75.4%), with males being more vocally active than females. Duets accounted for 24.6% of all vocalisations and in most cases were initiated by males (81%). The majority of duets were simple (85.1%) consisting of a single male and female song type, but altogether 38 unique duet combinations were described. Males usually initiated singing at dawn and for this used one particular song type more often than expected by chance. Male solo and duet activities peaked around dawn, while female solos were produced evenly throughout the day. DISCUSSION: Yellow-breasted Boubou is a duetting species in which males are much more vocal than females and duetting is not a dominating type of vocal activity. Duet structure, context and timing of daily production support the joint resource defence hypothesis and mate guarding/prevention hypotheses, however maintaining pair contact also seems to be important. This study provides for the first time the basic quantitative data describing calls, solos and duet songs in the Yellow-breasted Boubou.

Female indris determine the rhythmic structure of the song and sustain a higher cost when the chorus size increases.

Among the behavioral traits shared by some nonhuman primate species and humans there is singing. Unfortunately, our understanding of animals' rhythmic abilities is still in its infancy. Indris are the only lemurs who sing and live in monogamous pairs, usually forming a group with their offspring. All adult members of a group usually participate in choruses that are emitted regularly and play a role in advertising territorial occupancy and intergroup spacing. Males and females emit phrases that have similar frequency ranges but may differ in their temporal structure. We examined whether the individuals' contribution to the song may change according to chorus size, the total duration of the song or the duration of the individual contribution using the inter-onset intervals within a phrase and between phrases. We found that the rhythmic structure of indri's songs depends on factors that are different for males and females. We showed that females have significantly higher variation in the rhythm of their contribution to the song and that, changes according to chorus size. Our findings indicate that female indris sustain a higher cost of singing than males when the number of singers increases. These results suggest that cross-species investigations will be crucial to understanding the evolutionary frame in which such sexually dimorphic traits occurred.

A duetting perspective on avian song learning.

Avian song learning has a rich history of study and has become the preeminent system for understanding the ontogeny of vocal communication in animals. Song learning in birds has many parallels with human language learning, ranging from the neural mechanisms involved to the importance of social factors in shaping signal acquisition. While much has been learned about the process of song learning, virtually all of the research done to date has focused on temperate species, where often only one sex (the male) sings. Duetting species, in which both males and females learn to sing and learn to combine their songs into temporally coordinated joint displays, could provide many insights into the processes by which vocal learning takes place. Here we highlight three key features of song learning-neuroendocrine control mechanisms, timing and life history stages of song acquisition, and the role of social factors in song selection and use-that have been elucidated from species where only males sing, and compare these with duetting species. We summarize what is known about song learning in duetting species and then provide several suggestions for fruitful directions for future research. We suggest that focusing research efforts on duetting species could significantly advance our understanding of vocal learning in birds and further cement the importance of avian species as models for understanding human conversations and the processes of vocal learning more broadly.

Psychic Song and Dance: Dissociation and Duets in the Analysis of Trauma.

The author offers observations on the nature of pathological dissociation, emphasizing the compartmentalization of unsymbolized affective experience. The irrelevance of personal agency and intentionality in the pathogenesis of dissociative psychopathology along with the deficiency in symbolization that is a sequela of trauma present special problems for traditional as well as for Relational approaches to technique. To a significant extent, "technique" must be replaced by the analyst's way of being. The author posits, as metaphor and model for this way of being, a notion of "psychoanalytic duets" occurring in the realms of both prosody and action-song and dance. An extended clinical vignette is presented to illustrate these ideas and to point toward a transformational effect of this kind of duetting.

Differentiating the evolution of female song and male-female duets in the New World blackbirds: can tropical natural history traits explain duet evolution?

Female bird song and combined vocal duets of mated pairs are both frequently associated with tropical, monogamous, sedentary natural histories. Little is known, however, about what selects for duetting behavior versus female song. Female song likely preceded duet evolution and could drive apparent relationships between duets and these natural histories. We compared the evolution of female song and male-female duets in the New World blackbirds (Icteridae) by investigating patterns of gains and losses of both traits and their relationships with breeding latitude, mating system, nesting pattern, and migratory behavior. We found that duets evolved only in lineages in which female song was likely ancestral. Both female song and duets were correlated with tropical breeding, social monogamy, territorial nesting, and sedentary behavior when all taxa were included; however, correlations between duets and these natural history traits disappeared when comparisons were limited to taxa with female song. Also, likelihood values supported stronger relationships between the natural history traits and female song than between these traits and duets. Our results suggest that the natural histories thought to favor the evolution of duetting may in fact be associated with female song and that additional selection pressures are responsible for the evolution of duets.

Patients', clinicians' and the research communities' priorities for treatment research: there is an important mismatch.

PLAIN ENGLISH SUMMARY: There is some evidence that there is a mismatch between what patients and health professionals want to see researched and the research that is actually done. The James Lind Alliance (JLA) research Priority Setting Partnerships (PSPs) were created to address this mismatch. Between 2007 and 2014, JLA partnerships of patients, carers and health professionals agreed on important treatment research questions (priorities) in a range of health conditions, such as Type 1 diabetes, eczema and stroke. We were interested in how much these JLA PSP priorities were similar to treatments undergoing evaluation and research over the same time span. We identified the treatments described in all the JLA PSP research priority lists and compared these to the treatments described in a group of research studies (randomly selected) registered publically. The priorities identified by JLA PSPs emphasised the importance of non-drug treatment research, compared to the research actually being done over the same time period, which mostly involved evaluations of drugs. These findings suggest that the research community should make greater efforts to address issues of importance to users of research, such as patients and healthcare professionals. ABSTRACT: Background Comparisons of treatment research priorities identified by patients and clinicians with research actually being done by researchers are very rare. One of the best known of these comparisons (Tallon et al. Relation between agendas of the research community and the research consumer 355:2037-40, 2000) revealed important mismatches in priorities in the assessment of treatments for osteoarthritis of the knee: researchers preferenced drug trials, patients and clinicians prioritised non-drug treatments. These findings were an important stimulus in creating the James Lind Alliance (JLA). The JLA supports research Priority Setting Partnerships (PSPs) of patients, carers and clinicians, who are actively involved in all aspects of the process, to develop shared treatment research priorities. We have compared the types of treatments (interventions) prioritised for evaluation by JLA PSPs with those being studied in samples of clinical trials being done over the same period. Objective We used treatment research priorities generated by JLA PSPs to assess whether, on average, treatments prioritised by patients and clinicians differ importantly from those being studied by researchers. Methods We identified treatments mentioned in prioritised research questions generated by the first 14 JLA PSPs. We compared these treatments with those assessed in random samples of commercial and non-commercial clinical trials recruiting in the UK over the same period, which we identified using WHO's International Clinical Trials Registry Platform. Results We found marked differences between the proportions of different types of treatments proposed by patients, carers and clinicians and those currently being evaluated by researchers. In JLA PSPs, drugs accounted for only 18 % (23/126) of the treatments mentioned in priorities; in registered non-commercial trials, drugs accounted for 37 % (397/1069) of the treatments mentioned; and in registered commercial trials, drugs accounted for 86 % (689/798) of the treatments mentioned. Discussion Our findings confirm the mismatch first described by Tallon et al. 15 years ago. On average, drug trials are being preferenced by researchers, and non-drug treatments are preferred by patients, carers and clinicians. This general finding should be reflected in more specific assessments of the extent to which research is addressing priorities identified by the patient and clinician end users of research. It also suggests that the research culture is slow to change in regard to how important and relevant treatment research questions are identified and prioritised.