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.

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.

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.

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.

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.

Precise Motor Control Enables Rapid Flexibility in Vocal Behavior of Marmoset Monkeys.

Investigating the evolution of human speech is difficult and controversial because human speech surpasses nonhuman primate vocal communication in scope and flexibility [1-3]. Monkey vocalizations have been assumed to be largely innate, highly affective, and stereotyped for over 50 years [4, 5]. Recently, this perception has dramatically changed. Current studies have revealed distinct learning mechanisms during vocal development [6-8] and vocal flexibility, allowing monkeys to cognitively control when [9, 10], where [11], and what to vocalize [10, 12, 13]. However, specific call features (e.g., duration, frequency) remain surprisingly robust and stable in adult monkeys, resulting in rather stereotyped and discrete call patterns [14]. Additionally, monkeys seem to be unable to modulate their acoustic call structure under reinforced conditions beyond natural constraints [15, 16]. Behavioral experiments have shown that monkeys can stop sequences of calls immediately after acoustic perturbation but cannot interrupt ongoing vocalizations, suggesting that calls consist of single impartible pulses [17, 18]. Using acoustic perturbation triggered by the vocal behavior itself and quantitative measures of resulting vocal adjustments, we show that marmoset monkeys are capable of producing calls with durations beyond the natural boundaries of their repertoire by interrupting ongoing vocalizations rapidly after perturbation onset. Our results indicate that marmosets are capable of interrupting vocalizations only at periodic time points throughout calls, further supported by the occurrence of periodically segmented phees. These ideas overturn decades-old concepts on primate vocal pattern generation, indicating that vocalizations do not consist of one discrete call pattern but are built of many sequentially uttered units, like human speech.

Simultaneous epidural functional near-infrared spectroscopy and cortical electrophysiology as a tool for studying local neurovascular coupling in primates.

Simultaneous measurements of intra-cortical electrophysiology and hemodynamic signals in primates are essential for relating human neuroimaging studies with intra-cortical electrophysiology in monkeys. Previously, technically challenging and resourcefully demanding techniques such as fMRI and intrinsic-signal optical imaging have been used for such studies. Functional near-infrared spectroscopy is a relatively less cumbersome neuroimaging method that uses near-infrared light to detect small changes in concentrations of oxy-hemoglobin (HbO), deoxy-hemoglobin (HbR) and total hemoglobin (HbT) in a volume of tissue with high specificity and temporal resolution. FNIRS is thus a good candidate for hemodynamic measurements in primates to acquire local hemodynamic signals during electrophysiological recordings. To test the feasibility of using epidural fNIRS with concomitant extracellular electrophysiology, we recorded neuronal and hemodynamic activity from the primary visual cortex of two anesthetized monkeys during visual stimulation. We recorded fNIRS epidurally, using one emitter and two detectors. We performed simultaneous cortical electrophysiology using tetrodes placed between the fNIRS sensors. We observed robust and reliable responses to the visual stimulation in both [HbO] and [HbR] signals, and quantified the signal-to-noise ratio of the epidurally measured signals. We also observed a positive correlation between stimulus-induced modulation of [HbO] and [HbR] signals and strength of neural modulation. Briefly, our results show that epidural fNIRS detects single-trial responses to visual stimuli on a trial-by-trial basis, and when coupled with cortical electrophysiology, is a promising tool for studying local hemodynamic signals and neurovascular coupling.