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.

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.

Size differences among canaries, goldfinches and allies may explain correlated evolution of song and colour.

Sexual signals such as colour ornamentation and birdsong evolve independently of each other in some clades, and in others they evolve positively or negatively correlated. We rarely know why correlated evolution does or does not occur. Here, we show positively correlated evolution between plumage colour and song motor performance among canaries, goldfinches and allies, associated with species differences in body size. When controlling for body size, the pattern of correlated evolution between song performance and colour disappeared. Syllable diversity was not as strongly associated with size, and did not evolve in a correlated manner with colour. We argue that correlated evolution between song and colour was mediated by large size limiting song motor performance, likely due to constraints on the speed of moving heavier bills, and by larger species having less saturated plumage colour, possibly due to life-history traits of larger birds (e.g. longevity, stable pairs) contributing to weaker sexual selection. Results are consistent with the hypothesis that correlated evolution between sexual signals is influenced by how, in a clade, selective pressures and constraints affecting each type of signal happen to be co-distributed across species. Such contingency helps explain the diversity in clade-specific patterns of correlated evolution between sexual signals.

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.

Note similarities affect syntactic stability in zebra finches.

The acquisition of an acoustic template is a fundamental component of vocal imitation learning, which is used to refine innate vocalizations and develop a species-specific song. In the absence of a model, birds fail to develop species typical songs. In zebra finches (Taeniopygia guttata), tutored birds produce songs with a stereotyped sequence of distinct acoustic elements, or notes, which form the song motif. Songs of untutored individuals feature atypical acoustic and temporal structure. Here we studied songs and associated respiratory patterns of tutored and untutored male zebra finches to investigate whether similar acoustic notes influence the sequence of song elements. A subgroup of animals developed songs with multiple acoustically similar notes that are produced with alike respiratory motor gestures. These birds also showed increased syntactic variability in their adult motif. Sequence variability tended to occur near song elements which showed high similarity in acoustic structure and underlying respiratory motor gestures. The duration and depth of the inspirations preceding the syllables where syntactic variation occurred did not allow prediction of the following sequence of notes, suggesting that the varying duration and air requirement of the following expiratory pulse is not predictively encoded in the motor program. This study provides a novel method for calculation of motor/acoustic similarity, and the results of this study suggest that the note is a fundamental acoustic unit in the organization of the motif and could play a role in the neural code for song syntax.

The effect of exposure to natural sounds on stress reduction: a systematic review and meta-analysis.

The main aim of this review is to compare whether natural sounds or a quiet environment is more beneficial for alleviating stress. The results showed that there is a statistically significant difference between exposure to natural sounds and a quiet environment in terms of their effect on heart rate (p = 0.006), blood pressure (p = 0.001), and respiratory rate (p = 0.032). However, no significant difference was found between exposure to natural sounds and a quiet environment in terms of their effect on MAP (p = 0.407), perceived stress, and SPO2 (p = 0.251). Although the evidence was slightly inconsistent, overall, natural sounds were found more beneficial for stress reduction than quiet environments.

5G AI-IoT System for Bird Species Monitoring and Song Classification.

Identification of different species of animals has become an important issue in biology and ecology. Ornithology has made alliances with other disciplines in order to establish a set of methods that play an important role in the birds' protection and the evaluation of the environmental quality of different ecosystems. In this case, the use of machine learning and deep learning techniques has produced big progress in birdsong identification. To make an approach from AI-IoT, we have used different approaches based on image feature comparison (through CNNs trained with Imagenet weights, such as EfficientNet or MobileNet) using the feature spectrogram for the birdsong, but also the use of the deep CNN (DCNN) has shown good performance for birdsong classification for reduction of the model size. A 5G IoT-based system for raw audio gathering has been developed, and different CNNs have been tested for bird identification from audio recordings. This comparison shows that Imagenet-weighted CNN shows a relatively high performance for most species, achieving 75% accuracy. However, this network contains a large number of parameters, leading to a less energy efficient inference. We have designed two DCNNs to reduce the amount of parameters, to keep the accuracy at a certain level, and to allow their integration into a small board computer (SBC) or a microcontroller unit (MCU).

Performance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds.

Motor skills learned through practice are consolidated at later time, which can include nighttime, but the time course of motor memory consolidation and its underlying mechanisms remain poorly understood. We investigated neural substrates underlying motor memory consolidation of learned changes in birdsong, a tractable model system for studying neural basis of motor skill learning. Previous studies in male zebra finches and Bengalese finches have demonstrated that adaptive changes in adult song structure learned through a reinforcement paradigm are initially driven by a cortical-basal ganglia circuit, and subsequently consolidated into downstream cortical motor circuitry. However, the time course of the consolidation process, including whether it occurs offline during nighttime or online during daytime, remains unclear and even controversial. Here, we provide in both species experimental evidence of virtually no consolidation of learned vocal changes during nighttime. We demonstrate instead that the consolidation occurs during daytime and the amount of consolidation is strongly correlated with the amount of learning, suggesting online, performance-dependent mechanisms of consolidation of learned vocal changes. Moreover, by using computer simulations based on our experimental results, we demonstrate that such online, performance-dependent consolidation can account for the contradicting conclusions concerning the time course of consolidation process reached by previous studies. These results thus reconcile a controversy in the study of vocal motor consolidation in songbirds, and illustrate the neural substrates through which newly learned motor skills initially implemented by cortical-basal ganglia circuits become encoded in the cortical motor circuitry.SIGNIFICANCE STATEMENT Motor skills learned through repetitive practice become stable and are consolidated into cortical motor circuits. We investigate neural substrates of this "motor memory consolidation" in adult songbirds, which produce songs that are complex motor skills learned and maintained through repetitive vocal practice. We demonstrate that learned changes in song acoustic structure are consolidated into the cortical motor circuits predominantly during daytime, but not during nighttime, depending on ongoing song performance. These consolidation mechanisms reconcile seemingly contradicting results of previous studies regarding the time course of vocal learning consolidation, and provide fundamental insights into the process through which learned performance of complex motor skills is consolidated and encoded in in motor circuits.

The molecular architecture of a complex social behavior: gregarious song.

The medial preoptic area (mPOA) regulates the probability and intensity of singing behavior in birds. Polzin and colleagues examined the molecular changes in the mPOA that were associated with gregarious song in European starlings (Sturnus vulgaris). High-throughput transcriptome analyses identified glutamate and dopamine pathways were highly enriched with gregarious song.

The dynamics behind diversity in suboscine songs.

Vocal behavior plays a crucial evolutionary role. In the case of birds, song is critically important in courtship, male-male competition and other key behaviors linked to reproduction. However, under natural conditions, a variety of avian species live in close proximity and share an 'acoustic landscape'. Therefore, they need to be able to differentiate their calls or songs from those of other species and also from those of other individuals of the same species. To do this efficiently, birds display a remarkable diversity of sounds. For example, in the case of vocal learners, such as oscine passerines (i.e. songbirds), complex sequences and subtle acoustic effects are produced through the generation of complex neuromuscular instructions driving the vocal organ, which is remarkably conserved across approximately 4000 oscine species. By contrast, the majority of the sister clade of oscines, the suboscine passerines, are thought not to be vocal learners. Despite this, different suboscine species can generate a rich variety of songs and quite subtle acoustic effects. In the last few years, different suboscine species have been shown to possess morphological adaptations that allow them to produce a diversity of acoustic characteristics. Here, we briefly review the mechanisms of sound production in birds, before considering three suboscine species in more detail. The examples discussed in this Review, integrating biological experiments and biomechanical modeling using non-linear dynamical systems, illustrate how a morphological adaptation can produce complex acoustic properties without the need for complex neuromuscular control.

Zebra finches (Taeniopygia guttata) demonstrate cognitive flexibility in using phonology and sequence of syllables in auditory discrimination.

Zebra finches rely mainly on syllable phonology rather than on syllable sequence when they discriminate between two songs. However, they can also learn to discriminate two strings containing the same set of syllables by their sequence. How learning about the phonological characteristics of syllables and their sequence relate to each other and to the composition of the stimuli is still an open question. We compared whether and how the zebra finches' relative sensitivity for syllable phonology and syllable sequence depends on the differences between syllable strings. Two groups of zebra finches were trained in a Go-Left/Go-Right task to discriminate either between two strings in which each string contained a unique set of song syllables ('Different-syllables group') or two strings in which both strings contained the same set of syllables, but in a different sequential order ('Same-syllables group'). We assessed to what extent the birds in the two experimental groups attend to the spectral characteristics and the sequence of the syllables by measuring the responses to test strings consisting of spectral modifications or sequence changes. Our results showed no difference in the number of trials needed to discriminate strings consisting of either different or identical sets of syllables. Both experimental groups attended to changes in spectral features in a similar way, but the group for which both training strings consisted of the same set of syllables responded more strongly to changes in sequence than the group for which the training strings consisted of different sets of syllables. This outcome suggests the presence of an additional learning process to learn about syllable sequence when learning about syllable phonology is not sufficient to discriminate two strings. Our study thus demonstrates that the relative importance of syllable phonology and sequence depends on how these features vary among stimuli. This indicates cognitive flexibility in the acoustic features that songbirds might use in their song recognition.

Learning to pause: Fidelity of and biases in the developmental acquisition of gaps in the communicative signals of a songbird.

The temporal organization of sounds used in social contexts can provide information about signal function and evoke varying responses in listeners (receivers). For example, music is a universal and learned human behavior that is characterized by different rhythms and tempos that can evoke disparate responses in listeners. Similarly, birdsong is a social behavior in songbirds that is learned during critical periods in development and used to evoke physiological and behavioral responses in receivers. Recent investigations have begun to reveal the breadth of universal patterns in birdsong and their similarities to common patterns in speech and music, but relatively little is known about the degree to which biological predispositions and developmental experiences interact to shape the temporal patterning of birdsong. Here, we investigated how biological predispositions modulate the acquisition and production of an important temporal feature of birdsong, namely the duration of silent pauses ("gaps") between vocal elements ("syllables"). Through analyses of semi-naturally raised and experimentally tutored zebra finches, we observed that juvenile zebra finches imitate the durations of the silent gaps in their tutor's song. Further, when juveniles were experimentally tutored with stimuli containing a wide range of gap durations, we observed biases in the prevalence and stereotypy of gap durations. Together, these studies demonstrate how biological predispositions and developmental experiences differently affect distinct temporal features of birdsong and highlight similarities in developmental plasticity across birdsong, speech, and music. RESEARCH HIGHLIGHTS: The temporal organization of learned acoustic patterns can be similar across human cultures and across species, suggesting biological predispositions in acquisition. We studied how biological predispositions and developmental experiences affect an important temporal feature of birdsong, namely the duration of silent intervals between vocal elements ("gaps"). Semi-naturally and experimentally tutored zebra finches imitated the durations of gaps in their tutor's song and displayed some biases in the learning and production of gap durations and in gap variability. These findings in the zebra finch provide parallels with the acquisition of temporal features of speech and music in humans.

High-fidelity continuum modeling predicts avian voiced sound production.

Voiced sound production is the primary form of acoustic communication in terrestrial vertebrates, particularly birds and mammals, including humans. Developing a causal physics-based model that ultimately links descending vocal motor control to tissue vibration and sound requires embodied approaches that include realistic representations of voice physiology. Here, we first implement and then experimentally test a high-fidelity three-dimensional (3D) continuum model for voiced sound production in birds. Driven by individual-based physiologically quantifiable inputs, combined with noninvasive inverse methods for tissue material parameterization, our model accurately predicts observed key vibratory and acoustic performance traits. These results demonstrate that realistic models lead to accurate predictions and support the continuum model approach as a critical tool toward a causal model of voiced sound production.

Long-distance dependencies in birdsong syntax.

Songbird syntax is generally thought to be simple, in particular lacking long-distance dependencies in which one element affects choice of another occurring considerably later in the sequence. Here, we test for long-distance dependencies in the sequences of songs produced by song sparrows (Melospiza melodia). Song sparrows sing with eventual variety, repeating each song type in a consecutive series termed a 'bout'. We show that in switching between song types, song sparrows follow a 'cycling rule', cycling through their repertoires in close to the minimum possible number of bouts. Song sparrows do not cycle in a set order but rather vary the order of song types from cycle to cycle. Cycling in a variable order strongly implies long-distance dependencies, in which choice of the next type depends on the song types sung over the past cycle, in the range of 9-10 bouts. Song sparrows also follow a 'bout length rule', whereby the number of repetitions of a song type in a bout is positively associated with the length of the interval until that type recurs. This rule requires even longer distance dependencies that cross one another; such dependencies are characteristic of more complex levels of syntax than previously attributed to non-human animals.

Higher-order sequences of vocal mimicry performed by male Albert's lyrebirds are socially transmitted and enhance acoustic contrast.

Most studies of acoustic communication focus on short units of vocalization such as songs, yet these units are often hierarchically organized into higher-order sequences and, outside human language, little is known about the drivers of sequence structure. Here, we investigate the organization, transmission and function of vocal sequences sung by male Albert's lyrebirds (Menura alberti), a species renowned for vocal imitations of other species. We quantified the organization of mimetic units into sequences, and examined the extent to which these sequences are repeated within and between individuals and shared among populations. We found that individual males organized their mimetic units into stereotyped sequences. Sequence structures were shared within and to a lesser extent among populations, implying that sequences were socially transmitted. Across the entire species range, mimetic units were sung with immediate variety and a high acoustic contrast between consecutive units, suggesting that sequence structure is a means to enhance receiver perceptions of repertoire complexity. Our results provide evidence that higher-order sequences of vocalizations can be socially transmitted, and that the order of vocal units can be functionally significant. We conclude that, to fully understand vocal behaviours, we must study both the individual vocal units and their higher-order temporal organization.

Where to from here? Perspectives on steroid-induced and naturally-occurring singing in female songbirds.

In many species, male and female animals differ in the types and frequency of particular behaviors (e.g. reproductive behavior, parental behavior, etc.). These differences in behavior are quite often related to the neural and hormonal control of said behaviors. In the temperate zone it is commonly stated that male songbirds sing much more frequently and with much greater quality compared to their female counterparts. However, recent evidence has called these claims into question (Odom et al., 2014; Price et al., 2008; Webb et al., 2016). That said, neuroendocrine studies of song behavior have primarily focused on male birds and relatively little work has been done exclusively or comparatively with female songbirds. What we do know, however, is that there is wide variability in the vocal ability and capacity of female songbirds and that there is a developmental link between the hormonal milieu and neuro-social development that facilitate these behavioral phenotypes. Both testosterone and estradiol have been demonstrated to play pivotal roles in behavioral and neural differentiation of male and female song behavior profiles. Here we review a brief history of empirical investigation into steroid regulation of song in female birds, including the pattern of song activation, constraints on the ability of testosterone to induce singing, and the role of the anterior forebrain in supporting song learning. We conclude with a brief analysis of a major gap in the field's knowledge regarding naturally occurring female song and the neuroendocrine underpinnings of a socially salient learned behavior ripe for systematic investigation.

Sex differences in seasonal brain plasticity and the neuroendocrine regulation of vocal behavior in songbirds.

Birdsong is controlled in part by a discrete network of interconnected brain nuclei regulated in turn by steroid hormones and environmental stimuli. This complex interaction results in neural changes that occur seasonally as the environment varies (e.g., photoperiod, food/water availability, etc.). Variation in environment, vocal behavior, and neuroendocrine control has been primarily studied in male songbirds in both laboratory studies of captive birds and field studies of wild caught birds. The bias toward studying seasonality in the neuroendocrine regulation of song in male birds comes from a historic focus on sexually selected male behaviors. In fact, given that male song is often loud and accompanied by somewhat extravagant courtship behaviors, female song has long been overlooked. To compound this bias, the primary model songbird species for studies in the lab, zebra finches (Taeniopygia guttata) and canaries (Serinus canaria), exhibit little or no female song. Therefore, understanding the degree of variation and neuroendocrine control of seasonality in female songbirds is a major gap in our knowledge. In this review, we discuss the importance of studying sex differences in seasonal plasticity and the song control system. Specifically, we discuss sex differences in 1) the neuroanatomy of the song control system, 2) the distribution of receptors for androgens and estrogens and 3) the seasonal neuroplasticity of the hypothalamo-pituitary-gonadal axis as well as in the neural and cellular mechanisms mediating song system changes. We also discuss how these neuroendocrine mechanisms drive sex differences in seasonal behavior. Finally, we highlight specific gaps in our knowledge and suggest experiments critical for filling these gaps.

Design of a robotic zebra finch for experimental studies on developmental song learning.

Birdsong learning has been consolidated as the model system of choice for exploring the biological substrates of vocal learning. In the zebra finch (Taeniopygia guttata), only males sing and they develop their song during a sensitive period in early life. Different experimental procedures have been used in the laboratory to train a young finch to learn a song. So far, the best method to achieve a faithful imitation is to keep a young bird singly with an adult male. Here, we present the different characteristics of a robotic zebra finch that was developed with the goal to be used as a song tutor. The robot is morphologically similar to a life-sized finch: it can produce movements and sounds contingently to the behaviours of a live bird. We present preliminary results on song imitation, and other possible applications beyond the scope of developmental song learning.

Importance of sleep for avian vocal communication.

Sleep is one of the few truly ubiquitous animal behaviours, and though many animals spend enormous periods of time asleep, we have only begun to understand the consequences of sleep disturbances. In humans, sleep is crucial for effective communication. Birds are classic models for understanding the evolution and mechanisms of human language and speech. Bird vocalizations are remarkably diverse, critical, fitness-related behaviours, and the way sleep affects vocalizations is likely similarly varied. However, research on the effects of sleep disturbances on avian vocalizations is shockingly scarce. Consequently, there is a critical gap in our understanding of the extent to which sleep disturbances disrupt communication. Here, we argue that sleep disturbances are likely to affect all birds' vocal performance by interfering with motivation, memory consolidation and vocal maintenance. Further, we suggest that quality sleep is likely essential when learning new vocalizations and that sleep disturbances will have especially strong effects on learned vocalizations. Finally, we advocate for future research to address gaps in our understanding of how sleep influences vocal learning and performance in birds.

Acoustic Characteristics of Songs in a Recently Established Population of the Japanese Bush Warbler on an Oceanic Island.

The acoustic structure of birdsongs is determined by ecological and social factors. Moreover, the founder effect can occur when a few colonizers bring a small subset of the song diversity from a source population to a newly established population, generating the acoustic features of its songs. Around 2000, the Japanese bush warbler (Cettia diphone) naturally colonized Minami-Daito, an oceanic island in the northwest Pacific. This raises the question of whether the songs in this population have changed through adaptation to the insular environment or maintained the features of songs in the mainland population. In this study, the acoustic characteristics of Japanese bush warbler songs on Minami-Daito Island at present (i.e., approximately 20 years after colonization) were compared with the songs of conspecifics on the mainland and another island. The acoustic structure of one of two basic song types on this island did not differ from that on the mainland. The other song type had a simpler structure on the island than on the mainland. Analyses of intonation structure showed that a certain pattern of frequency increase and decrease among sound elements was rare (< 10%) on the mainland but dominant on the island. The song characteristics substantially overlapped between the island and the mainland, and have not changed on the island since its colonization. These results suggest that the song characteristics on Minami-Daito Island can be explained by the founder effect. The songs on this island may change adaptively over a long period. Continuous investigation to follow the changes is required.