Breathing control of vocalization.

A crucial brainstem circuit for vocal-respiratory coordination of the larynx is revealed.

Dysfunction of specific auditory fibers impacts cortical oscillations, driving an autism phenotype despite near-normal hearing.

Autism spectrum disorder is discussed in the context of altered neural oscillations and imbalanced cortical excitation-inhibition of cortical origin. We studied here whether developmental changes in peripheral auditory processing, while preserving basic hearing function, lead to altered cortical oscillations. Local field potentials (LFPs) were recorded from auditory, visual, and prefrontal cortices and the hippocampus of BdnfPax2 KO mice. These mice develop an autism-like behavioral phenotype through deletion of BDNF in Pax2+ interneuron precursors, affecting lower brainstem functions, but not frontal brain regions directly. Evoked LFP responses to behaviorally relevant auditory stimuli were weaker in the auditory cortex of BdnfPax2 KOs, connected to maturation deficits of high-spontaneous rate auditory nerve fibers. This was correlated with enhanced spontaneous and induced LFP power, excitation-inhibition imbalance, and dendritic spine immaturity, mirroring autistic phenotypes. Thus, impairments in peripheral high-spontaneous rate fibers alter spike synchrony and subsequently cortical processing relevant for normal communication and behavior.

Linguistic law-like compression strategies emerge to maximize coding efficiency in marmoset vocal communication.

Human language follows statistical regularities or linguistic laws. For instance, Zipf's law of brevity states that the more frequently a word is used, the shorter it tends to be. All human languages adhere to this word structure. However, it is unclear whether Zipf's law emerged de novo in humans or whether it also exists in the non-linguistic vocal systems of our primate ancestors. Using a vocal conditioning paradigm, we examined the capacity of marmoset monkeys to efficiently encode vocalizations. We observed that marmosets adopted vocal compression strategies at three levels: (i) increasing call rate, (ii) decreasing call duration and (iii) increasing the proportion of short calls. Our results demonstrate that marmosets, when able to freely choose what to vocalize, exhibit vocal statistical regularities consistent with Zipf's law of brevity that go beyond their context-specific natural vocal behaviour. This suggests that linguistic laws emerged in non-linguistic vocal systems in the primate lineage.

Neural representations of the content and production of human vocalization.

Speech, as the spoken form of language, is fundamental for human communication. The phenomenon of covert inner speech implies functional independence of speech content and motor production. However, it remains unclear how a flexible mapping between speech content and production is achieved on the neural level. To address this, we recorded magnetoencephalography in humans performing a rule-based vocalization task. On each trial, vocalization content (one of two vowels) and production form (overt or covert) were instructed independently. Using multivariate pattern analysis, we found robust neural information about vocalization content and production, mostly originating from speech areas of the left hemisphere. Production signals dynamically transformed upon presentation of the content cue, whereas content signals remained largely stable throughout the trial. In sum, our results show dissociable neural representations of vocalization content and production in the human brain and provide insights into the neural dynamics underlying human vocalization.

Marmoset monkeys use different avoidance strategies to cope with ambient noise during vocal behavior.

Multiple strategies have evolved to compensate for masking noise, leading to changes in call features. One call adjustment is the Lombard effect, an increase in call amplitude in response to noise. Another strategy involves call production in periods where noise is absent. While mechanisms underlying vocal adjustments have been well studied, mechanisms underlying noise avoidance strategies remain largely unclear. We systematically perturbed ongoing phee calls of marmosets to investigate noise avoidance strategies. Marmosets canceled their calls after noise onset and produced longer calls after noise-phases ended. Additionally, the number of uttered syllables decreased during noise perturbation. This behavior persisted beyond the noise-phase. Using machine learning techniques, we found that a fraction of single phees were initially planned as double phees and became interrupted after the first syllable. Our findings indicate that marmosets use different noise avoidance strategies and suggest vocal flexibility at different complexity levels in the marmoset brain.

Cardiovascular mechanisms underlying vocal behavior in freely moving macaque monkeys.

Communication is a keystone of animal behavior. However, the physiological states underlying natural vocal signaling are still largely unknown. In this study, we investigated the correlation of affective vocal utterances with concomitant cardiorespiratory mechanisms. We telemetrically recorded electrocardiography, blood pressure, and physical activity in six freely moving and interacting cynomolgus monkeys (Macaca fascicularis). Our results demonstrate that vocal onsets are strengthened during states of sympathetic activation, and are phase locked to a slower Mayer wave and a faster heart rate signal at ∼2.5 Hz. Vocalizations are coupled with a distinct peri-vocal physiological signature based on which we were able to predict the onset of vocal output using three machine learning classification models. These findings emphasize the role of cardiorespiratory mechanisms correlated with vocal onsets to optimize arousal levels and minimize energy expenditure during natural vocal production.

High plasticity in marmoset monkey vocal development from infancy to adulthood.

The vocal behavior of human infants undergoes marked changes across their first year while becoming increasingly speech-like. Conversely, vocal development in nonhuman primates has been assumed to be largely predetermined and completed within the first postnatal months. Contradicting this assumption, we found a dichotomy between the development of call features and vocal sequences in marmoset monkeys, suggestive of a role for experience. While changes in call features were related to physical maturation, sequences of and transitions between calls remained flexible until adulthood. As in humans, marmoset vocal behavior developed in stages correlated with motor and social development stages. These findings are evidence for a prolonged phase of plasticity during marmoset vocal development, a crucial primate evolutionary preadaptation for the emergence of vocal learning and speech.

Theta Synchronization of Phonatory and Articulatory Systems in Marmoset Monkey Vocal Production.

Human speech shares a 3-8-Hz theta rhythm across all languages [1-3]. According to the frame/content theory of speech evolution, this rhythm corresponds to syllabic rates derived from natural mandibular-associated oscillations [4]. The underlying pattern originates from oscillatory movements of articulatory muscles [4, 5] tightly linked to periodic vocal fold vibrations [4, 6, 7]. Such phono-articulatory rhythms have been proposed as one of the crucial preadaptations for human speech evolution [3, 8, 9]. However, the evolutionary link in phono-articulatory rhythmicity between vertebrate vocalization and human speech remains unclear. From the phonatory perspective, theta oscillations might be phylogenetically preserved throughout all vertebrate clades [10-12]. From the articulatory perspective, theta oscillations are present in non-vocal lip smacking [1, 13, 14], teeth chattering [15], vocal lip smacking [16], and clicks and faux-speech [17] in non-human primates, potential evolutionary precursors for speech rhythmicity [1, 13]. Notably, a universal phono-articulatory rhythmicity similar to that in human speech is considered to be absent in non-human primate vocalizations, typically produced with sound modulations lacking concomitant articulatory movements [1, 9, 18]. Here, we challenge this view by investigating the coupling of phonatory and articulatory systems in marmoset vocalizations. Using quantitative measures of acoustic call structure, e.g., amplitude envelope, and call-associated articulatory movements, i.e., inter-lip distance, we show that marmosets display speech-like bi-motor rhythmicity. These oscillations are synchronized and phase locked at theta rhythms. Our findings suggest that oscillatory rhythms underlying speech production evolved early in the primate lineage, identifying marmosets as a suitable animal model to decipher the evolutionary and neural basis of coupled phono-articulatory movements.

Compensatory mechanisms affect sensorimotor integration during ongoing vocal motor acts in marmoset monkeys.

Any transmission of vocal signals faces the challenge of acoustic interferences such as heavy rain, wind, animal or urban sounds. Consequently, several mechanisms and strategies have evolved to optimize signal-to-noise ratio. Examples to increase detectability are the Lombard effect, an involuntary rise in call amplitude in response to masking ambient noise, which is often associated with other vocal changes such as call frequency and duration, as well as the animals' capability of limiting calling to periods where noise perturbation is absent. Previous studies revealed vocal flexibility and various audio-vocal integration mechanisms in marmoset monkeys. Using acoustic perturbation triggered by vocal behaviour, we investigated whether marmosets are capable of exhibiting changes in call structure when perturbing noise starts after call onset or whether such effects only occur if noise perturbation starts prior to call onset. We show that marmosets are capable of rapidly modulating call amplitude and frequency in response to such noise perturbation. Vocalizations swiftly increased call frequency after noise onset indicating a rapid effect of perturbing noise on vocal motor production. Call amplitudes were also affected. Interestingly, however, the marmosets did not exhibit the Lombard effect as previously reported but decreased call intensity in response to noise. Our findings indicate that marmosets possess a general avoidance strategy to call in the presence of ambient noise and suggest that these animals are capable of counteracting a previously thought involuntary audio-vocal mechanism, the Lombard effect. These findings will pave the way to investigate the underlying audio-vocal integration mechanisms explaining these behaviours.

The role of auditory feedback on vocal pattern generation in marmoset monkeys.

Marmoset monkeys are known for their rich vocal repertoire. However, the underlying call production mechanisms remain unclear. By showing that marmoset moneys are capable of interrupting and modulating ongoing vocalizations, recent studies in marmoset monkeys challenged the decades-old concepts of primate vocal pattern generation that suggested that monkey calls consist of one discrete call pattern. The current article will present a revised version of the brainstem vocal pattern-generating network in marmoset monkeys that is capable of responding to perturbing auditory stimuli with rapid modulatory changes of the acoustic call structure during ongoing calls. These audio-vocal integration processes might potentially happen at both the cortical and subcortical brain level.

Author Correction: Cognitive control of complex motor behavior in marmoset monkeys.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Volitional control of vocalizations in corvid songbirds.

Songbirds are renowned for their acoustically elaborate songs. However, it is unclear whether songbirds can cognitively control their vocal output. Here, we show that crows, songbirds of the corvid family, can be trained to exert control over their vocalizations. In a detection task, three male carrion crows rapidly learned to emit vocalizations in response to a visual cue with no inherent meaning (go trials) and to withhold vocalizations in response to another cue (catch trials). Two of these crows were then trained on a go/nogo task, with the cue colors reversed, in addition to being rewarded for withholding vocalizations to yet another cue (nogo trials). Vocalizations in response to the detection of the go cue were temporally precise and highly reliable in all three crows. Crows also quickly learned to withhold vocal output in nogo trials, showing that vocalizations were not produced by an anticipation of a food reward in correct trials. The results demonstrate that corvids can volitionally control the release and onset of their vocalizations, suggesting that songbird vocalizations are under cognitive control and can be decoupled from affective states.

Cognitive control of complex motor behavior in marmoset monkeys.

Marmosets have attracted significant interest in the life sciences. Similarities with human brain anatomy and physiology, such as the granular frontal cortex, as well as the development of transgenic lines and potential for transferring rodent neuroscientific techniques to small primates make them a promising neurodegenerative and neuropsychiatric model system. However, whether marmosets can exhibit complex motor tasks in highly controlled experimental designs-one of the prerequisites for investigating higher-order control mechanisms underlying cognitive motor behavior-has not been demonstrated. We show that marmosets can be trained to perform vocal behavior in response to arbitrary visual cues in controlled operant conditioning tasks. Our results emphasize the marmoset as a suitable model to study complex motor behavior and the evolution of cognitive control underlying speech.

Limited capabilities for condition-dependent modulation of vocal turn-taking behavior in marmoset monkeys.

Taking turns plays an important role in primate communication and involves individuals producing species-specific calls in response to conspecific vocalizations. Recent studies have revealed that marmoset monkeys are an ideal primate model system to investigate vocal turn-taking behavior and the corresponding sensory-motor interactions. However, it is largely unknown how external factors such as conspecific call latency influence this vocal behavior. Using interactive playback, we systematically answered vocalizations of monkeys with either short- or long-call response latencies. By placing marmosets in these different behavioral conditions, we demonstrate that vocal turn taking is a robust behavior with only minor condition-dependent changes that is exhibited not only in the range of species-specific call latencies of vocal partners but also in conditions well outside natural behavioral boundaries. We find that specific features of vocal performance such as call response rates and call sequences remain surprisingly stable, whereas others such as turn-taking rates and response latencies exhibit condition-dependent differences during this behavior. These condition-dependent modulations suggest that a combination of flexible and more rigid mechanisms control marmoset vocal turn-taking behavior. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Semi-chronic laminar recordings in the brainstem of behaving marmoset monkeys.

BACKGROUND: Chronic recordings with multi-electrode arrays are widely used to study neural networks underlying complex primate behaviors. Most of these systems are designed for studying neural activity in the cortical hemispheres resulting in a lack of devices being capable of simultaneously recording from ensembles of neurons in deep brainstem structures. However, to fully understand complex behavior, it is fundamental to also decipher the intrinsic mechanisms of the underlying motor pattern generating circuits in the brainstem. NEW METHOD: We report a light-weight system that simultaneously measures single-unit activity from a large number of recording sites in the brainstem of marmoset monkeys. It includes a base chamber fixed to the animal's skull and a removable upper chamber that can be semi-chronically mounted to the base chamber to flexibly position an embedded micro-drive containing a 32-channel laminar probe to record from various positions within the brainstem for several weeks. RESULTS: The current system is capable of simultaneously recording stable single-unit activity from a large number of recording sites in the brainstem of vocalizing marmoset monkeys. COMPARISON WITH EXISTING METHODS: To the best of our knowledge, chronic systems to record from deep brainstem structures with multi-site laminar probes in awake, behaving monkeys do not yet exist. CONCLUSIONS: The semi-chronic implantation of laminar electrodes into the brainstem of behaving marmoset monkeys opens new research possibilities in fully understanding the neural mechanisms underlying complex behaviors in marmoset monkeys.

The Lombard Effect: From Acoustics to Neural Mechanisms.

Understanding the neural underpinnings of vocal-motor control in humans and other animals remains a major challenge in neurobiology. The Lombard effect - a rise in call amplitude in response to background noise - has been demonstrated in a wide range of vertebrates. Here, we review both behavioral and neurophysiological data and propose that the Lombard effect is driven by a subcortical neural network, which can be modulated by cortical processes. The proposed framework offers mechanistic explanations for two fundamental features of the Lombard effect: its widespread taxonomic distribution across the vertebrate phylogenetic tree and the widely observed variations in compensation magnitude. We highlight the Lombard effect as a model behavioral paradigm for unraveling some of the neural underpinnings of audiovocal integration.

Limiting parental interaction during vocal development affects acoustic call structure in marmoset monkeys.

Human vocal development is dependent on learning by imitation through social feedback between infants and caregivers. Recent studies have revealed that vocal development is also influenced by parental feedback in marmoset monkeys, suggesting vocal learning mechanisms in nonhuman primates. Marmoset infants that experience more contingent vocal feedback than their littermates develop vocalizations more rapidly, and infant marmosets with limited parental interaction exhibit immature vocal behavior beyond infancy. However, it is yet unclear whether direct parental interaction is an obligate requirement for proper vocal development because all monkeys in the aforementioned studies were able to produce the adult call repertoire after infancy. Using quantitative measures to compare distinct call parameters and vocal sequence structure, we show that social interaction has a direct impact not only on the maturation of the vocal behavior but also on acoustic call structures during vocal development. Monkeys with limited parental interaction during development show systematic differences in call entropy, a measure for maturity, compared with their normally raised siblings. In addition, different call types were occasionally uttered in motif-like sequences similar to those exhibited by vocal learners, such as birds and humans, in early vocal development. These results indicate that a lack of parental interaction leads to long-term disturbances in the acoustic structure of marmoset vocalizations, suggesting an imperative role for social interaction in proper primate vocal development.

Auditory and audio-vocal responses of single neurons in the monkey ventral premotor cortex.

Monkey vocalization is a complex behavioral pattern, which is flexibly used in audio-vocal communication. A recently proposed dual neural network model suggests that cognitive control might be involved in this behavior, originating from a frontal cortical network in the prefrontal cortex and mediated via projections from the rostral portion of the ventral premotor cortex (PMvr) and motor cortex to the primary vocal motor network in the brainstem. For the rapid adjustment of vocal output to external acoustic events, strong interconnections between vocal motor and auditory sites are needed, which are present at cortical and subcortical levels. However, the role of the PMvr in audio-vocal integration processes remains unclear. In the present study, single neurons in the PMvr were recorded in rhesus monkeys (Macaca mulatta) while volitionally producing vocalizations in a visual detection task or passively listening to monkey vocalizations. Ten percent of randomly selected neurons in the PMvr modulated their discharge rate in response to acoustic stimulation with species-specific calls. More than four-fifths of these auditory neurons showed an additional modulation of their discharge rates either before and/or during the monkeys' motor production of the vocalization. Based on these audio-vocal interactions, the PMvr might be well positioned to mediate higher order auditory processing with cognitive control of the vocal motor output to the primary vocal motor network. Such audio-vocal integration processes in the premotor cortex might constitute a precursor for the evolution of complex learned audio-vocal integration systems, ultimately giving rise to human speech.