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.

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.

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.

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.

Audio-vocal interaction in single neurons of the monkey ventrolateral prefrontal cortex.

Complex audio-vocal integration systems depend on a strong interconnection between the auditory and the vocal motor system. To gain cognitive control over audio-vocal interaction during vocal motor control, the PFC needs to be involved. Neurons in the ventrolateral PFC (VLPFC) have been shown to separately encode the sensory perceptions and motor production of vocalizations. It is unknown, however, whether single neurons in the PFC reflect audio-vocal interactions. We therefore recorded single-unit activity in the VLPFC of rhesus monkeys (Macaca mulatta) while they produced vocalizations on command or passively listened to monkey calls. We found that 12% of randomly selected neurons in VLPFC modulated their discharge rate in response to acoustic stimulation with species-specific calls. Almost three-fourths of these auditory neurons showed an additional modulation of their discharge rates either before and/or during the monkeys' motor production of vocalization. Based on these audio-vocal interactions, the VLPFC might be well positioned to combine higher order auditory processing with cognitive control of the vocal motor output. Such audio-vocal integration processes in the VLPFC might constitute a precursor for the evolution of complex learned audio-vocal integration systems, ultimately giving rise to human speech.

Developmental changes of cognitive vocal control in monkeys.

The evolutionary origins of human language are obscured by the scarcity of essential linguistic characteristics in non-human primate communication systems. Volitional control of vocal utterances is one such indispensable feature of language. We investigated the ability of two monkeys to volitionally utter species-specific calls over many years. Both monkeys reliably vocalized on command during juvenile periods, but discontinued this controlled vocal behavior in adulthood. This emerging disability was confined to volitional vocal production, as the monkeys continued to vocalize spontaneously. In addition, they continued to use hand movements as instructed responses during adulthood. This greater vocal flexibility of monkeys early in ontogeny supports the neoteny hypothesis in human evolution. This suggests that linguistic capabilities were enabled via an expansion of the juvenile period during the development of humans.

Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats.

The Lombard effect, an involuntary rise in call amplitude in response to masking ambient noise, represents one of the most efficient mechanisms to optimize signal-to-noise ratio. The Lombard effect occurs in birds and mammals, including humans, and is often associated with several other vocal changes, such as call frequency and duration. Most studies, however, have focused on noise-dependent changes in call amplitude. It is therefore still largely unknown how the adaptive changes in call amplitude relate to associated vocal changes such as frequency shifts, how the underlying mechanisms are linked, and if auditory feedback from the changing vocal output is needed. Here, we examined the Lombard effect and the associated changes in call frequency in a highly vocal mammal, echolocating horseshoe bats. We analyzed how bandpass-filtered noise (BFN; bandwidth 20 kHz) affected their echolocation behavior when BFN was centered on different frequencies within their hearing range. Call amplitudes increased only when BFN was centered on the dominant frequency component of the bats' calls. In contrast, call frequencies increased for all but one BFN center frequency tested. Both amplitude and frequency rises were extremely fast and occurred in the first call uttered after noise onset, suggesting that no auditory feedback was required. The different effects that varying the BFN center frequency had on amplitude and frequency rises indicate different neural circuits and/or mechanisms underlying these changes.

Ambient noise causes independent changes in distinct spectro-temporal features of echolocation calls in horseshoe bats.

One of the most efficient mechanisms to optimize signal-to-noise ratios is the Lombard effect - an involuntary rise in call amplitude due to ambient noise. It is often accompanied by changes in the spectro-temporal composition of calls. We examined the effects of broadband-filtered noise on the spectro-temporal composition of horseshoe bat echolocation calls, which consist of a constant-frequency component and initial and terminal frequency-modulated components. We found that the frequency-modulated components became larger for almost all noise conditions, whereas the bandwidth of the constant-frequency component increased only when broadband-filtered noise was centered on or above the calls' dominant or fundamental frequency. This indicates that ambient noise independently modifies the associated acoustic parameters of the Lombard effect, such as spectro-temporal features, and could significantly affect the bat's ability to detect and locate targets. Our findings may be of significance in evaluating the impact of environmental noise on echolocation behavior in bats.

Brain mechanisms of acoustic communication in humans and nonhuman primates: an evolutionary perspective.

Any account of "what is special about the human brain" (Passingham 2008) must specify the neural basis of our unique ability to produce speech and delineate how these remarkable motor capabilities could have emerged in our hominin ancestors. Clinical data suggest that the basal ganglia provide a platform for the integration of primate-general mechanisms of acoustic communication with the faculty of articulate speech in humans. Furthermore, neurobiological and paleoanthropological data point at a two-stage model of the phylogenetic evolution of this crucial prerequisite of spoken language: (i) monosynaptic refinement of the projections of motor cortex to the brainstem nuclei that steer laryngeal muscles, presumably, as part of a "phylogenetic trend" associated with increasing brain size during hominin evolution; (ii) subsequent vocal-laryngeal elaboration of cortico-basal ganglia circuitries, driven by human-specific FOXP2 mutations.;>This concept implies vocal continuity of spoken language evolution at the motor level, elucidating the deep entrenchment of articulate speech into a "nonverbal matrix" (Ingold 1994), which is not accounted for by gestural-origin theories. Moreover, it provides a solution to the question for the adaptive value of the "first word" (Bickerton 2009) since even the earliest and most simple verbal utterances must have increased the versatility of vocal displays afforded by the preceding elaboration of monosynaptic corticobulbar tracts, giving rise to enhanced social cooperation and prestige. At the ontogenetic level, the proposed model assumes age-dependent interactions between the basal ganglia and their cortical targets, similar to vocal learning in some songbirds. In this view, the emergence of articulate speech builds on the "renaissance" of an ancient organizational principle and, hence, may represent an example of "evolutionary tinkering" (Jacob 1977).

Breathing control of vocalization.

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

Cognitive control of distinct vocalizations in rhesus monkeys.

Whether nonhuman primates can decouple their innate vocalizations from accompanied levels of arousal or specific events in the environment to achieve cognitive control over their vocal utterances has been a matter of debate for decades. We show that rhesus monkeys can be trained to elicit different call types on command in response to arbitrary visual cues. Furthermore, we report that a monkey learned to switch between two distinct call types from trial to trial in response to different visual cues. A controlled behavioral protocol and data analysis based on signal detection theory showed that noncognitive factors as a cause for the monkeys' vocalizations could be excluded. Our findings also suggest that monkeys also have rudimentary control over acoustic call parameters. These findings indicate that monkeys are able to volitionally initiate their vocal production and, therefore, are able to instrumentalize their vocal behavior to perform a behavioral task successfully.

Temporal vocal features suggest different call-pattern generating mechanisms in mice and bats.

BACKGROUND: Mice produce ultrasonic vocalizations in various inter-individual encounters and with high call rates. However, it is so far virtually unknown how these vocal patterns are generated. On the one hand, these vocal patterns could be embedded into the normal respiratory cycle, as happens in bats and other mammals that produce similar call rates and frequencies. On the other, mice could possess distinct vocal pattern generating systems that are capable of modulating the respiratory cycle, which is what happens in non-human and human primates. In the present study, we investigated the temporal call patterns of two different mammalian species, bats and mice, in order to differentiate between these two possibilities for mouse vocalizations. Our primary focus was on comparing the mechanisms for the production of rapid, successive ultrasound calls of comparable frequency ranges in the two species. RESULTS: We analyzed the temporal call pattern characteristics of mice, and we compared these characteristics to those of ultrasonic echolocation calls produced by horseshoe bats. We measured the distributions of call durations, call intervals, and inter-call intervals in the two species. In the bat, and consistent with previous studies, we found that call duration was independent of corresponding call intervals, and that it was negatively correlated with the corresponding inter-call interval. This indicates that echolocation call production mechanisms in the bat are highly correlated with the respiratory cycle. In contrast, call intervals in the mouse were directly correlated with call duration. Importantly, call duration was not, or was only slightly, correlated with inter-call intervals, consistent with the idea that vocal production in the mouse is largely independent of the respiratory cycle. CONCLUSIONS: Our findings suggest that ultrasonic vocalizations in mice are produced by call-pattern generating mechanisms that seem to be similar to those that have been found in primates. This is in contrast to the production mechanisms of ultrasonic echolocation calls in horseshoe bats. These results are particularly interesting, especially since mouse vocalizations have recently attracted increased attention as potential indicators for the degree of progression of several disease patterns in mouse models for neurodegenerative and neurodevelopmental disorders of humans.

Audio-vocal interactions during vocal communication in squirrel monkeys and their neurobiological implications.

Several strategies have evolved in the vertebrate lineage to facilitate signal transmission in vocal communication. Here, I present a mechanism to facilitate signal transmission in a group of communicating common squirrel monkeys (Saimiri sciureus sciureus). Vocal onsets of a conspecific affect call initiation in all other members of the group in less than 100 ms. The probability of vocal onsets in a range of 100 ms after the beginning of a vocalization of another monkey was significantly decreased compared to the mean probability of call onsets. Additionally, the probability for vocal onsets of conspecifics was significantly increased just a few hundreds of milliseconds after call onset of others. These behavioral data suggest neural mechanisms that suppress vocal output just after the onset of environmental noise, such as vocalizations of conspecifics, and increase the probability of call initiation of group mates shortly after. These findings add new audio-vocal behaviors to the known strategies that modulate signal transmission in vocal communication. The present study will guide future neurobiological studies that explore how the observed audio-vocal behaviors are implemented in the monkey brain.

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.

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.

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.

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).