TCF7L2 acts as a molecular switch in midbrain to control mammal vocalization through a transcriptional repression mechanism

Vocalization is an essential medium for sexual and social signaling in birds and mammals. Periaqueductal gray (PAG) a conserved midbrain structure is believed to be responsible for innate vocalizations, but its molecular regulation remains largely unknown. Here, through a mouse forward genetic screening we identified one of the key Wnt/β-catenin effectors TCF7L2/TCF4 controls ultrasonic vocalization (USV) production and syllable complexity during maternal deprivation and sexual encounter. Expression of TCF7L2 in PAG excitatory neurons is necessary for the complex trait, while TCF7L2 loss reduces neuronal gene expressions and synaptic transmission in PAG. TCF7L2-mediated vocal control is independent of its β-catenin-binding domain but dependent of its DNA binding ability. Patient mutations associated with severe speech delay disrupt the transcriptional repression effect of TCF7L2, while mice carrying those mutations display severe USV impairments. Therefore, we conclude that TCF7L2 orchestrates gene expression in midbrain to control vocal production through a transcriptional repression mechanism.

The resting frequency of echolocation signals changes with body temperature in the hipposiderid bat, Hipposideros armiger

Doppler shift (DS) compensating bats adjust in flight the second harmonic of the constant-frequency component (CF2) of their echolocation signals so that the frequency of the Doppler shifted echoes returning from ahead is kept constant with high precision (0.1-0.2%) at the so-called reference frequency (fref). This feedback adjustment is mediated by an audio-vocal control system which correlates with a maximal activation of the foveal resonance area in the cochlea. Stationary bats adjust the average CF2 with similar precision at the resting frequency (frest), which is slightly below the fref. Over a variety of time periods (from minutes up to years) variations of the coupled fref and frest have been observed, and were attributed to age, social influences and behavioural situations in rhinolophids and hipposiderids, and to body temperature effects and flight activity in Pteronotus parnellii. We assume that, for all DS compensating bats, a change in body temperature has a strong effect on the activation state of the foveal resonance area in the cochlea which leads to a concomitant change in emission frequency. We tested our hypothesis in a hipposiderid bat, Hipposideros armiger, and measured how the circadian variation of body temperature at activation phases affected frest. With a miniature temperature logger, we recorded the skin temperature on the back of the bats simultaneously with echolocation signals produced. During warm-up from torpor strong temperature increases were accompanied by an increase in frest, of up to 1.44 kHz. We discuss the implications of our results for the organization and function of the audio-vocal control systems of all DS compensating bats.

A Call to Expand Avian Vocal Development Research

Birds are our best models to understand vocal learning – a vocal production ability guided by auditory feedback, which includes human language. Among all vocal learners, songbirds have the most diverse life histories, and some aspects of their vocal learning ability are well-known, such as the neural substrates and vocal control centers, through vocal development studies. Currently, species are classified as either vocal learners or non-learners, and a key difference between the two is the development period, extended in learners, but short in non-learners. But this clear dichotomy has been challenged by the vocal learning continuum hypothesis. One way to address this challenge is to examine both learners and canonical non-learners and determine whether their vocal development is dichotomous or falls along a continuum. However, when we examined the existing empirical data we found that surprisingly few species have their vocal development periods documented. Furthermore, we identified multiple biases within previous vocal development studies in birds, including an extremely narrow focus on (1) a few model species, (2) oscines, (3) males, and (4) songs. Consequently, these biases may have led to an incomplete and possibly erroneous conclusions regarding the nature of the relationships between vocal development patterns and vocal learning ability. Diversifying vocal development studies to include a broader range of taxa is urgently needed to advance the field of vocal learning and examine how vocal development patterns might inform our understanding of vocal learning.

Voice modulation: from origin and mechanism to social impact

Research on within-individual modulation of vocal cues is surprisingly scarce outside of human speech. Yet, voice modulation serves diverse functions in human and nonhuman nonverbal communication, from dynamically signalling motivation and emotion, to exaggerating physical traits such as body size and masculinity, to enabling song and musicality. The diversity of anatomical, neural, cognitive and behavioural adaptations necessary for the production and perception of voice modulation make it a critical target for research on the origins and functions of acoustic communication. This diversity also implicates voice modulation in numerous disciplines and technological applications. In this two-part theme issue comprising 21 articles from leading and emerging international researchers, we highlight the multidisciplinary nature of the voice sciences. Every article addresses at least two, if not several, critical topics: (i) development and mechanisms driving vocal control and modulation; (ii) cultural and other environmental factors affecting voice modulation; (iii) evolutionary origins and adaptive functions of vocal control including cross-species comparisons; (iv) social functions and real-world consequences of voice modulation; and (v) state-of-the-art in multidisciplinary methodologies and technologies in voice modulation research. With this collection of works, we aim to facilitate cross-talk across disciplines to further stimulate the burgeoning field of voice modulation. This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part I)’.

Cockatiels sing human music in synchrony with a playback of the melody

It is known among aviculturists that cockatiels imitate human music with their whistle-like vocal sounds. The present study examined whether cockatiels are also able to sing “in unison”, or, line up their vocalizations with a musical melody so that they occur at the same time. Three hand-raised cockatiels were exposed to a musical melody of human whistling produced by an experimenter. All the birds learned to sing the melody. Then, two out of these three birds spontaneously joined in singing during an ongoing melody, so that the singing by the bird and the whistling by the human were nearly perfectly synchronous. Further experiments revealed that the birds actively adjusted their vocal timing to playback of a recording of the same melody. This means cockatiels have a remarkable ability for flexible vocal control similar to what is seen in human singing. The proximate/ultimate factors for this behavior and implications for musicality in humans are discussed.

Singers and non-singers differ in the performance and neural representation of vocal imitation

Humans have a remarkable capacity to finely control the muscles of the larynx, via distinct patterns of cortical topography and innervation that may underpin our sophisticated vocal capabilities compared with non-human primates. Here, we investigated the behavioural and neural correlates of laryngeal control, and their relationship to vocal expertise, using an imitation task that required adjustments of larynx musculature during speech. Highly-trained human singers and non-singer control participants modulated voice pitch and vocal tract length (VTL) to mimic auditory speech targets, while undergoing real-time anatomical scans of the vocal tract and functional scans of brain activity. Multivariate analyses of speech acoustics, larynx movements and brain activation data were used to quantify vocal modulation behaviour, and to search for neural representations of the two modulated vocal parameters during the preparation and execution of speech. We found that singers showed more accurate task-relevant modulations of speech pitch and VTL (i.e. larynx height, as measured with vocal tract MRI) during speech imitation; this was accompanied by stronger representation of VTL within a region of right dorsal somatosensory cortex. Our findings suggest a common neural basis for enhanced vocal control in speech and song.

Songbirds can learn flexible contextual control over syllable sequencing

The flexible control of sequential behavior is a fundamental aspect of speech, enabling endless reordering of a limited set of learned vocal elements (syllables or words). Songbirds are phylogenetically distant from humans but share both the capacity for vocal learning and neural circuitry for vocal control that includes direct pallial-brainstem projections. Based on these similarities, we hypothesized that songbirds might likewise be able to learn flexible, moment-by-moment control over vocalizations. Here, we demonstrate that Bengalese finches (Lonchura striata domestica), which sing variable syllable sequences, can learn to rapidly modify the probability of specific sequences (e.g. ‘ab-c’ versus ‘ab-d’) in response to arbitrary visual cues. Moreover, once learned, this modulation of sequencing occurs immediately following changes in contextual cues and persists without external reinforcement. Our findings reveal a capacity in songbirds for learned contextual control over syllable sequencing that parallels human cognitive control over syllable sequencing in speech.

Changes of Voice Production in Artificial Acoustic Environments

The physical production of speech level dynamic range is directly affected by the physiological features of the speaker such as vocal tract size and lung capacity; however, the regulation of these production systems is affected by the perception of the communication environment and auditory feedback. The current study examined the effects of room acoustics in an artificial setting on voice production in terms of sound pressure level and the relationship with the perceived vocal comfort and vocal control. Three independent room acoustic parameters were considered: gain (alteration of the sidetone or playback of one’s own voice), reverberation time, and background noise. An increase in the sidetone led to a decrease in vocal sound pressure levels, thus increasing vocal comfort and vocal control. This effect was consistent in the different reverberation times considered. Mid-range reverberation times (T30 ≈ 1.3 s) led to a decrease in vocal sound pressure level along with an increase in vocal comfort and vocal control, however, the effect of the reverberation time was smaller than the effect of the gain. The presence of noise amplified the aforementioned effects for the variables analyzed.