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.

The Use of the Voice Trainer App for Vocal Control in People with a Degenerative Ataxia: A Pilot Intervention Study.

Dysarthria is disabling in persons with degenerative ataxia. There is limited evidence for speech therapy interventions. In this pilot study, we used the Voice trainer app, which was originally developed for patients with Parkinson's disease, as a feedback tool for vocal control. We hypothesized that patients with ataxic dysarthria would benefit from the Voice trainer app to better control their loudness and pitch, resulting in a lower speaking rate and better intelligibility. This intervention study consisted of five therapy sessions of 30 min within 3 weeks using the principles of the Pitch Limiting Voice Treatment. Patients received real-time visual feedback on loudness and pitch during the exercises. Besides, they were encouraged to practice at home or to use the Voice trainer in daily life. We used observer-rated and patient-rated outcome measures. The primary outcome measure was intelligibility, as measured by the Dutch sentence intelligibility test. Twenty-one out of 25 included patients with degenerative ataxia completed the therapy. We found no statistically significant improvements in intelligibility (p = .56). However, after the intervention, patients were speaking slower (p = .03) and the pause durations were longer (p < .001). The patients were satisfied about using the app. At the group level, we found no evidence for an effect of the Voice trainer app on intelligibility in degenerative ataxia. Because of the heterogeneity of ataxic dysarthria, a more tailor-made rather than generic intervention seems warranted.

Cognitive control of orofacial motor and vocal responses in the ventrolateral and dorsomedial human frontal cortex.

In the primate brain, a set of areas in the ventrolateral frontal (VLF) cortex and the dorsomedial frontal (DMF) cortex appear to control vocalizations. The basic role of this network in the human brain and how it may have evolved to enable complex speech remain unknown. In the present functional neuroimaging study of the human brain, a multidomain protocol was utilized to investigate the roles of the various areas that comprise the VLF-DMF network in learning rule-based cognitive selections between different types of motor actions: manual, orofacial, nonspeech vocal, and speech vocal actions. Ventrolateral area 44 (a key component of the Broca's language production region in the human brain) is involved in the cognitive selection of orofacial, as well as, speech and nonspeech vocal responses; and the midcingulate cortex is involved in the analysis of speech and nonspeech vocal feedback driving adaptation of these responses. By contrast, the cognitive selection of speech vocal information requires this former network and the additional recruitment of area 45 and the presupplementary motor area. We propose that the basic function expressed by the VLF-DMF network is to exert cognitive control of orofacial and vocal acts and, in the language dominant hemisphere of the human brain, has been adapted to serve higher speech function. These results pave the way to understand the potential changes that could have occurred in this network across primate evolution to enable speech production.

Vocomotor and Social Brain Networks Work Together to Express Social Traits in Voices.

Voice modulation is important when navigating social interactions-tone of voice in a business negotiation is very different from that used to comfort an upset child. While voluntary vocal behavior relies on a cortical vocomotor network, social voice modulation may require additional social cognitive processing. Using functional magnetic resonance imaging, we investigated the neural basis for social vocal control and whether it involves an interplay of vocal control and social processing networks. Twenty-four healthy adult participants modulated their voice to express social traits along the dimensions of the social trait space (affiliation and competence) or to express body size (control for vocal flexibility). Naïve listener ratings showed that vocal modulations were effective in evoking social trait ratings along the two primary dimensions of the social trait space. Whereas basic vocal modulation engaged the vocomotor network, social voice modulation specifically engaged social processing regions including the medial prefrontal cortex, superior temporal sulcus, and precuneus. Moreover, these regions showed task-relevant modulations in functional connectivity to the left inferior frontal gyrus, a core vocomotor control network area. These findings highlight the impact of the integration of vocal motor control and social information processing for socially meaningful voice modulation.

Chance, long tails, and inference in a non-Gaussian, Bayesian theory of vocal learning in songbirds.

Traditional theories of sensorimotor learning posit that animals use sensory error signals to find the optimal motor command in the face of Gaussian sensory and motor noise. However, most such theories cannot explain common behavioral observations, for example, that smaller sensory errors are more readily corrected than larger errors and large abrupt (but not gradually introduced) errors lead to weak learning. Here, we propose a theory of sensorimotor learning that explains these observations. The theory posits that the animal controls an entire probability distribution of motor commands rather than trying to produce a single optimal command and that learning arises via Bayesian inference when new sensory information becomes available. We test this theory using data from a songbird, the Bengalese finch, that is adapting the pitch (fundamental frequency) of its song following perturbations of auditory feedback using miniature headphones. We observe the distribution of the sung pitches to have long, non-Gaussian tails, which, within our theory, explains the observed dynamics of learning. Further, the theory makes surprising predictions about the dynamics of the shape of the pitch distribution, which we confirm experimentally.

Long-lasting vocal plasticity in adult marmoset monkeys.

Humans exhibit a high level of vocal plasticity in speech production, which allows us to acquire both native and foreign languages and dialects, and adapt to local accents in social communication. In comparison, non-human primates exhibit limited vocal plasticity, especially in adulthood, which would limit their ability to adapt to different social and environmental contexts in vocal communication. Here, we quantitatively examined the ability of adult common marmosets ( Callithrix jacchus), a highly vocal New World primate species, to modulate their vocal production in social contexts. While recent studies have demonstrated vocal learning in developing marmosets, we know much less about the extent of vocal learning and plasticity in adult marmosets. We found, in the present study, that marmosets were able to adaptively modify the spectrotemporal structure of their vocalizations when they encountered interfering sounds. Our experiments showed that marmosets shifted the spectrum of their vocalizations away from the spectrum of the interfering sounds in order to avoid the overlap. More interestingly, we found that marmosets made predictive and long-lasting spectral shifts in their vocalizations after they had experienced a particular type of interfering sound. These observations provided evidence for directional control of the vocalization spectrum and long-term vocal plasticity by adult marmosets. The findings reported here have important implications for the ability of this New World primate species in voluntarily and adaptively controlling their vocal production in social communication.

Voice pitch modulation in human mate choice.

Inter-individual differences in human fundamental frequency ( F0, perceived as voice pitch) predict mate quality and reproductive success, and affect listeners' social attributions. Although humans can readily and volitionally manipulate their vocal apparatus and resultant voice pitch, for instance, in the production of speech sounds and singing, little is known about whether humans exploit this capacity to adjust the non-verbal dimensions of their voices during social (including sexual) interactions. Here, we recorded full-length conversations of 30 adult men and women taking part in real speed-dating events and tested whether their voice pitch (mean, range and variability) changed with their personal mate choice preferences and the overall desirability of each dating partner. Within-individual analyses indicated that men lowered the minimum pitch of their voices when interacting with women who were overall highly desired by other men. Men also lowered their mean voice pitch on dates with women they selected as potential mates, particularly those who indicated a mutual preference (matches). Interestingly, although women spoke with a higher and more variable voice pitch towards men they selected as potential mates, women lowered both voice pitch parameters towards men who were most desired by other women and whom they also personally preferred. Between-individual analyses indicated that men in turn preferred women with lower-pitched voices, wherein women's minimum voice pitch explained up to 55% of the variance in men's mate preferences. These results, derived in an ecologically valid setting, show that individual- and group-level mate preferences can interact to affect vocal behaviour, and support the hypothesis that human voice modulation functions in non-verbal communication to elicit favourable judgements and behaviours from others, including potential mates.

Ability to modulate birdsong across social contexts develops without imitative social learning.

Many important behaviours are socially learned. For example, the acoustic structure of courtship songs in songbirds is learned by listening to and interacting with conspecifics during a sensitive period in development. Signallers modify the spectral and temporal structures of their vocalizations depending on the social context, but the degree to which this modulation requires imitative social learning remains unknown. We found that male zebra finches (Taeniopygia guttata) that were not exposed to context-dependent song modulations throughout development significantly modulated their song in ways that were typical of socially reared birds. Furthermore, the extent of these modulations was not significantly different between finches that could or could not observe these modulations during tutoring. These data suggest that this form of vocal flexibility develops without imitative social learning in male zebra finches.

Difference between the vocalizations of two sister species of pigeons explained in dynamical terms.

Vocal communication is an unique example, where the nonlinear nature of the periphery can give rise to complex sounds even when driven by simple neural instructions. In this work we studied the case of two close-related bird species, Patagioenas maculosa and Patagioenas picazuro, whose vocalizations differ only in the timbre. The temporal modulation of the fundamental frequency is similar in both cases, differing only in the existence of sidebands around the fundamental frequency in the P. maculosa. We tested the hypothesis that the qualitative difference between these vocalizations lies in the nonlinear nature of the syrinx. In particular, we propose that the roughness of maculosa's vocalizations is due to an asymmetry between the right and left vibratory membranes, whose nonlinear dynamics generate the sound. To test the hypothesis, we generated a biomechanical model for vocal production with an asymmetric parameter Q with which we can control the level of asymmetry between these membranes. Using this model we generated synthetic vocalizations with the principal acoustic features of both species. In addition, we confirmed the anatomical predictions by making post mortem inspection of the syrinxes, showing that the species with tonal song (picazuro) has a more symmetrical pair of membranes compared to maculosa.

Functional morphology of the Alligator mississippiensis larynx with implications for vocal production.

Sauropsid vocalization is mediated by the syrinx in birds and the larynx in extant reptiles; but whereas avian vocal production has received much attention, the vocal mechanism of basal reptilians is poorly understood. The American alligator (Alligator mississippiensis) displays a large vocal repertoire during mating and in parent-offspring interactions. Although vocal outputs of these behaviors have received some attention, the underlying mechanism of sound production remains speculative. Here, we investigate the laryngeal anatomy of juvenile and adult animals by macroscopic and histological methods. Observations of the cartilaginous framework and associated muscles largely corroborate earlier findings, but one muscle, the cricoarytenoideus, exhibits a heretofore unknown extrinsic insertion that has important implications for effective regulation of vocal fold length and tension. Histological investigation of the larynx revealed a layered vocal fold morphology. The thick lamina propria consists of non-homogenous extracellular matrix containing collagen fibers that are tightly packed below the epithelium but loosely organized deep inside the vocal fold. We found few elastic fibers but comparatively high proportions of hyaluronan. Similar organizational complexity is also seen in mammalian vocal folds and the labia of the avian syrinx: convergent morphologies that suggest analogous mechanisms for sound production. In tensile tests, alligator vocal folds demonstrated a linear stress-strain behavior in the low strain region and nonlinear stress responses at strains larger than 15%, which is similar to mammalian vocal fold tissue. We have integrated morphological and physiological data in a two-mass vocal fold model, providing a systematic description of the possible acoustic space that could be available to an alligator larynx. Mapping actual call production onto possible acoustic space validates the model's predictions.

Vernal growth of vocal control nucleus Area X, but not HVC, precedes gonadal recrudescence in wild black-capped chickadees (Poecile atricapillus).

In temperate-zone songbirds, the neuroanatomical changes which occur in advance of breeding, including the growth of nuclei of the vocal control system, are believed to occur downstream of gonadal recrudescence. However, evidence from wild birds is mixed. Here, we captured black-capped chickadees from the wild in early spring (March-April), summer (August-September), and winter (December-January); in addition to measuring the volumes of two vocal control nuclei (Area X and HVC), we also quantified two indicators of reproductive state (gonads and circulating gonadal steroids). Most birds captured in early spring had regressed gonads and low levels of circulating gonadal steroids, indicating these birds were not yet in full breeding condition. However, these early spring birds still had a significantly larger Area X than winter birds, while HVC did not differ in size across groups. Using data from a previously published seasonal study of black-capped chickadees (Phillmore et al., Developmental Neurobiology, 2015;75:203-216), we then compared Area X and HVC volumes from our early spring group to a breeding group of chickadees captured 3-4 weeks later in the spring. While Area X volume did not differ between the studies, breeding males in Phillmore et al. (2015) had a significantly larger HVC. Taken together, this suggests that the vernal growth of Area X occurs ahead of HVC in black-capped chickadees, and that the overall vernal changes in the vocal control system occur at least partially in advance of the breeding-associated upregulation of the hypothalamic-pituitary-gonadal axis.

Spontaneous vocal coordination of vocalizations to water noise in rooks (Corvus frugilegus): An exploratory study.

The ability to control one's vocal production is a major advantage in acoustic communication. Yet, not all species have the same level of control over their vocal output. Several bird species can interrupt their song upon hearing an external stimulus, but there is no evidence how flexible this behavior is. Most research on corvids focuses on their cognitive abilities, but few studies explore their vocal aptitudes. Recent research shows that crows can be experimentally trained to vocalize in response to a brief visual stimulus. Our study investigated vocal control abilities with a more ecologically embedded approach in rooks. We show that two rooks could spontaneously coordinate their vocalizations to a long-lasting stimulus (the sound of their small bathing pool being filled with a water hose), one of them adjusting roughly (in the second range) its vocalizations as the stimuli began and stopped. This exploratory study adds to the literature showing that corvids, a group of species capable of cognitive prowess, are indeed able to display good vocal control abilities.

Aberrant modulation of broadband neural oscillations reflects vocal sensorimotor deficits in post-stroke aphasia.

OBJECTIVE: The present study investigated the neural oscillatory correlates of impaired vocal sensorimotor control in left-hemisphere stroke. METHODS: Electroencephalography (EEG) signals were recorded from 34 stroke and 46 control subjects during speech vowel vocalization and listening tasks under normal and pitch-shifted auditory feedback. RESULTS: Time-frequency analyses revealed aberrantly decreased theta (4-8 Hz) and increased gamma band (30-80 Hz) power in frontal and posterior parieto-occipital regions as well as reduced alpha (8-13 Hz) and beta (13-30 Hz) desynchronization over sensorimotor areas before speech vowel vocalization in left-hemisphere stroke compared with controls. Subjects with the stroke also presented with aberrant modulation of broadband (4-80 Hz) neural oscillations over sensorimotor regions after speech vowel onset during vocalization and listening under normal and altered auditory feedback. We found that the atypical pattern of broadband neural oscillatory modulation was correlated with diminished vocal feedback error compensation behavior and the severity of co-existing language-related aphasia symptoms associated with left-hemisphere stroke. CONCLUSIONS: These findings indicate complex interplays between the underlying mechanisms of speech and language and their deficits in post-stroke aphasia. SIGNIFICANCE: Our data motivate the notion of studying neural oscillatory dynamics as a critical component for the examination of speech and language disorders in post-stroke aphasia.

Wild orangutans can simultaneously use two independent vocal sound sources similarly to songbirds and human beatboxers.

Speech is among the most complex motoric tasks humans ever perform. Songbirds match this achievement during song production through the precise and simultaneous motor control of two sound sources in the syrinx. Integrated and intricate motor control has made songbirds comparative models par excellence for the evolution of speech, however, phylogenetic distance with humans prevents an improved understanding of the precursors that, within the human lineage, drove the emergence of advanced vocal motor control and speech. Here, we report two types of biphonic call combination in wild orangutans that articulatorily resemble human beatboxing and that result from the simultaneous exercise of two vocal sound sources: one unvoiced source achieved through articulatory maneuvering of the lips, tongue, and jaw as typically used for consonant-like call production, plus one voiced source achieved through laryngeal action and voice activation as typically used for vowel-like call production. Orangutan biphonic call combinations showcase unappreciated levels of, and distinct neuromotor channels for, vocal motor control in a wild great ape, providing a direct vocal motor analogy with birdsong based on the precise and simultaneous co-control of two sound sources. Findings suggest that speech and human vocal fluency likely built upon complex call combination, coordination and coarticulation capacities that involved vowel-like and consonant-like calls in an ancestral hominid.

Auditory Feedback Control of Vocal Pitch in Spasmodic Dysphonia.

OBJECTIVES/HYPOTHESIS: Hearing plays an important role in the maintenance of vocal control in normal individuals. In patients with spasmodic dysphonia (SD), however, the ability to maintain sustained control of phonation is impaired. The origins of SD are unknown, and it is unclear whether auditory feedback-dependent vocal control is compromised in these patients. STUDY DESIGN: Prospective case-control study. METHODS: We tested 15 SD patients and 11 age-matched controls. Voice recordings were performed while subjects repeated the vowel /e/ and auditory feedback of their vocal sounds was altered in real-time to introduce a pitch-shift (±2 semitones), presented back to subjects using headphones. Recordings were analyzed to determine voice changes following the pitch-shifted feedback. Results were further compared with patient demographics and subjective measures of dysphonia, including the Voice Handicap Index (VHI). RESULTS: Despite considerable pitch variability and vocal breaks, SD patients exhibited significantly higher average vocal pitch compensation than control subjects. SD patients also exhibited greater variability than controls. However, there were no significant correlations between vocal compensation and patient demographics, although there was a significant inverse correlation with VHI. CONCLUSIONS: In this pilot study, patients with SD exhibited increased sensitivity to altered auditory feedback during sustained phonation. These results are consistent with recent theories of SD as a disorder of sensory-motor feedback processing, and suggest possible avenues for future investigation. LEVEL OF EVIDENCE: 3 Laryngoscope, 131:2070-2075, 2021.

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)'.

Adults with a history of recreational cannabis use have altered speech production.

Stereotypical depictions of speech in cannabis users often suggest slow, laboured output, yet objective evidence supporting this assumption is extremely limited. We know that depressants or hallucinogenic drugs such as cannabis can cause acute changes in communication and speech rate, but the long-lasting effects of cannabis use on speech are not well described. The aim of this study was to investigate speech in individuals with a history of recreational cannabis use compared to non-drug-using healthy controls. Speech samples were collected from a carefully described cohort of 31 adults with a history of cannabis use (but not use of illicit stimulant drugs) and 40 non-drug-using controls. Subjects completed simple and complex speech tasks including a monologue, a sustained vowel, saying the days of the week, and reading a phonetically balanced passage. Audio samples were analysed objectively using acoustic analysis for measures of timing, vocal control, and quality. Subtle differences in speech timing, vocal effort, and voice quality may exist between cannabis and control groups, however data remain equivocal. After controlling for lifetime alcohol and tobacco use and applying a false discovery rate, only spectral tilt (vocal effort and intensity) differed between groups and appeared to change in line with duration of abstinence from cannabis use. Differences between groups may reflect longer term changes to the underlying neural control of speech. Our digital analysis of speech shows there may be a signal differentiating individuals with a history of recreational cannabis use from healthy controls, in line with similar findings from gait and hand function studies.

Real-time feedback control of voice in cochlear implant recipients.

OBJECTIVES: To evaluate feedback-dependent vocal control in cochlear implant patients using pitch-shifted auditory feedback. METHODS: Twenty-three CI recipients with at least 6 months of implant experience were enrolled. Vocal recordings were performed while subjects repeated the vowel /e/ and vocal signals were altered in real-time using a digital effects processor to introduce a pitch-shift, presented back to subjects using headphones. Recordings were analyzed to determine pitch changes following the pitch-shifted feedback, and results compared to the magnitude of the shift as well as patient demographics. RESULTS: Consistent with previous results, CI patients' voices had higher pitches with their implant turned off, a change explainable by increases in vocal loudness without the CI. CI patients rapidly compensated for pitch-shifted feedback by changing their vocal pitch, but only for larger shifts. Considerable inter-subject variability was present, and weakly correlated with the duration of implant experience and implant sound thresholds. CONCLUSIONS: CI patients, like normal hearing individuals, are capable of real-time feedback-dependent control of their vocal pitch. However, CI patients are less sensitive to small feedback changes, possibly a result of courser CI frequency precision, and may explain poorer than normal vocal control in these patients. LEVEL OF EVIDENCE: Level 3b.

Cochlear Implant Users' Vocal Control CorrelatesAcross Tasks.

Cochlear implants (CIs) provide access to auditory information that can affect vocal control. For example, previous research shows that, when producing a sustained vowel, CI users will alter the pitch of their voice when the feedback of their own voice is perceived to shift. Although these results can be informative as to how perception and production are linked for CI users, the artificial nature of the task raises questions as to the applicability of the results to real-world vocal productions. To examine how vocal control, when producing sustained vowels, relates to vocal control for more ecologically valid tasks, 10 CI users' vocal control was measured across two tasks: (1) sustained vowel production, and (2) singing. The results found that vocal control, as measured by the variability of the participants' fundamental frequency, was significantly correlated when producing sustained vowels and when singing, although variability was significantly greater when singing. This suggests that, despite the artificial nature of sustained vowel production, vocal control on such tasks is related to vocal control for more ecologically valid tasks. However, the results also suggest that vocal control may be overestimated with sustained vowel production tasks.

Bound for Specific Sounds: Vocal Predisposition in Animal Communication.

Mechanical constraints imposed by anatomical adaptations are a ubiquitous feature of animal sound production. They can give rise to 'vocal predispositions' (i.e., acoustic structures strictly determined by vocal anatomy). Such predispositions are crucial to the investigation of the cognitive and evolutionary processes underlying acoustic communication in vertebrates, including human speech.