Active neural coordination of motor behaviors with internal states.

The brain continuously coordinates skeletomuscular movements with internal physiological states like arousal, but how is this coordination achieved? One possibility is that the brain simply reacts to changes in external and/or internal signals. Another possibility is that it is actively coordinating both external and internal activities. We used functional ultrasound imaging to capture a large medial section of the brain, including multiple cortical and subcortical areas, in marmoset monkeys while monitoring their spontaneous movements and cardiac activity. By analyzing the causal ordering of these different time series, we found that information flowing from the brain to movements and heart-rate fluctuations were significantly greater than in the opposite direction. The brain areas involved in this external versus internal coordination were spatially distinct, but also extensively interconnected. Temporally, the brain alternated between network states for this regulation. These findings suggest that the brain's dynamics actively and efficiently coordinate motor behavior with internal physiology.

A mechanism for punctuating equilibria during mammalian vocal development.

Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes (states of equilibrium can be punctuated by sudden change. Here, we studied the early vocal development of three different mammals: common marmoset monkeys, Egyptian fruit bats, and humans. Consistent with the notion of punctuated equilibria, we found that all three species undergo at least one sudden transition in the acoustics of their developing vocalizations. To understand the mechanism, we modeled different developmental landscapes. We found that the transition was best described as a shift in the balance of two vocalization landscapes. We show that the natural dynamics of these two landscapes are consistent with the dynamics of energy expenditure and information transmission. By using them as constraints for each species, we predicted the differences in transition timing from immature to mature vocalizations. Using marmoset monkeys, we were able to manipulate both infant energy expenditure (vocalizing in an environment with lighter air) and information transmission (closed-loop contingent parental vocal playback). These experiments support the importance of energy and information in leading to punctuated equilibrium states of vocal development.

Arousal elevation drives the development of oscillatory vocal output.

Adult behaviors, such as vocal production, often exhibit temporal regularity. In contrast, their immature forms are more irregular. We ask whether the coupling of motor behaviors with arousal changes gives rise to temporal regularity: Do they drive the transition from variable to regular motor output over the course of development? We used marmoset monkey vocal production to explore this putative influence of arousal on the nonlinear changes in their developing vocal output patterns. Based on a detailed analysis of vocal and arousal dynamics in marmosets, we put forth a general model incorporating arousal and auditory feedback loops for spontaneous vocal production. Using this model, we show that a stable oscillation can emerge as the baseline arousal increases, predicting the transition from stochastic to periodic oscillations observed during marmoset vocal development. We further provide a solution for how this model can explain vocal development as the joint consequence of energetic growth and social feedback. Together, we put forth a plausible mechanism for the development of arousal-mediated adaptive behavior.NEW & NOTEWORTHY The development of motor behaviors, and the influence of energetic and social factors on it, has long been of interest, yet we lack an integrated picture of how these different systems may interact. Through the lens of vocal development in infant marmosets, this study offers a solution for social behavior development by linking motor production with arousal states. Increases in arousal can drive the system out of stochastic states toward oscillatory dynamics ready for communication.

Vocal development through morphological computation.

The vocal behavior of infants changes dramatically during early life. Whether or not such a change results from the growth of the body during development-as opposed to solely neural changes-has rarely been investigated. In this study of vocal development in marmoset monkeys, we tested the putative causal relationship between bodily growth and vocal development. During the first two months of life, the spontaneous vocalizations of marmosets undergo (1) a gradual disappearance of context-inappropriate call types and (2) an elongation in the duration of context-appropriate contact calls. We hypothesized that both changes are the natural consequences of lung growth and do not require any changes at the neural level. To test this idea, we first present a central pattern generator model of marmoset vocal production to demonstrate that lung growth can affect the temporal and oscillatory dynamics of neural circuits via sensory feedback from the lungs. Lung growth qualitatively shifted vocal behavior in the direction observed in real marmoset monkey vocal development. We then empirically tested this hypothesis by placing the marmoset infants in a helium-oxygen (heliox) environment in which air is much lighter. This simulated a reversal in development by decreasing the effort required to respire, thus increasing the respiration rate (as though the lungs were smaller). The heliox manipulation increased the proportions of inappropriate call types and decreased the duration of contact calls, consistent with a brief reversal of vocal development. These results suggest that bodily growth alone can play a major role in shaping the development of vocal behavior.

Internal states and extrinsic factors both determine monkey vocal production.

A key question for understanding speech evolution is whether or not the vocalizations of our closest living relatives-nonhuman primates-represent the precursors to speech. Some believe that primate vocalizations are not volitional but are instead inextricably linked to internal states like arousal and thus bear little resemblance to human speech. Others disagree and believe that since many primates can use their vocalizations strategically, this demonstrates a degree of voluntary vocal control. In the current study, we present a behavioral paradigm that reliably elicits different types of affiliative vocalizations from marmoset monkeys while measuring their heart rate fluctuations using noninvasive electromyography. By modulating both the physical distance between marmosets and the sensory information available to them, we find that arousal levels are linked, but not inextricably, to vocal production. Different arousal levels are, generally, associated with changes in vocal acoustics and the drive to produce different call types. However, in contexts where marmosets are interacting, the production of these different call types is also affected by extrinsic factors such as the timing of a conspecific's vocalization. These findings suggest that variability in vocal output as a function of context might reflect trade-offs between the drive to perpetuate vocal contact and conserving energy.

Cooperative care and the evolution of the prelinguistic vocal learning.

The development of the earliest vocalizations of human infants is influenced by social feedback from caregivers. As these vocalizations change, they increasingly elicit such feedback. This pattern of development is in stark contrast to that of our close phylogenetic relatives, Old World monkeys and apes, who produce mature-sounding vocalizations at birth. We put forth a scenario to account for this difference: Humans have a cooperative breeding strategy, which pressures infants to compete for the attention from caregivers. Humans use this strategy because large brained human infants are energetically costly and born altricial. An altricial brain accommodates vocal learning. To test this hypothetical scenario, we present findings from New World marmoset monkeys indicating that, through convergent evolution, this species adopted a largely identical developmental system-one that includes vocal learning and cooperative breeding.

Arousal dynamics drive vocal production in marmoset monkeys.

Vocal production is the result of interacting cognitive and autonomic processes. Despite claims that changes in one interoceptive state (arousal) govern primate vocalizations, we know very little about how it influences their likelihood and timing. In this study we investigated the role of arousal during naturally occurring vocal production in marmoset monkeys. Throughout each session, naturally occurring contact calls are produced more quickly, and with greater probability, during higher levels of arousal, as measured by heart rate. On average, we observed a steady increase in heart rate 23 s before the production of a call. Following call production, there is a sharp and steep cardiac deceleration lasting ∼8 s. The dynamics of cardiac fluctuations around a vocalization cannot be completely predicted by the animal's respiration or movement. Moreover, the timing of vocal production was tightly correlated to the phase of a 0.1-Hz autonomic nervous system rhythm known as the Mayer wave. Finally, a compilation of the state space of arousal dynamics during vocalization illustrated that perturbations to the resting state space increase the likelihood of a call occurring. Together, these data suggest that arousal dynamics are critical for spontaneous primate vocal production, not only as a robust predictor of the likelihood of vocal onset but also as scaffolding on which behavior can unfold.

Dynamic faces speed up the onset of auditory cortical spiking responses during vocal detection.

How low-level sensory areas help mediate the detection and discrimination advantages of integrating faces and voices is the subject of intense debate. To gain insights, we investigated the role of the auditory cortex in face/voice integration in macaque monkeys performing a vocal-detection task. Behaviorally, subjects were slower to detect vocalizations as the signal-to-noise ratio decreased, but seeing mouth movements associated with vocalizations sped up detection. Paralleling this behavioral relationship, as the signal to noise ratio decreased, the onset of spiking responses were delayed and magnitudes were decreased. However, when mouth motion accompanied the vocalization, these responses were uniformly faster. Conversely, and at odds with previous assumptions regarding the neural basis of face/voice integration, changes in the magnitude of neural responses were not related consistently to audiovisual behavior. Taken together, our data reveal that facilitation of spike latency is a means by which the auditory cortex partially mediates the reaction time benefits of combining faces and voices.

Monkeys are perceptually tuned to facial expressions that exhibit a theta-like speech rhythm.

Human speech universally exhibits a 3- to 8-Hz rhythm, corresponding to the rate of syllable production, which is reflected in both the sound envelope and the visual mouth movements. Artificial perturbation of the speech rhythm outside the natural range reduces speech intelligibility, demonstrating a perceptual tuning to this frequency band. One theory posits that the mouth movements at the core of this speech rhythm evolved through modification of ancestral primate facial expressions. Recent evidence shows that one such communicative gesture in macaque monkeys, lip-smacking, has motor parallels with speech in its rhythmicity, its developmental trajectory, and the coordination of vocal tract structures. Whether monkeys also exhibit a perceptual tuning to the natural rhythms of lip-smacking is unknown. To investigate this, we tested rhesus monkeys in a preferential-looking procedure, measuring the time spent looking at each of two side-by-side computer-generated monkey avatars lip-smacking at natural versus sped-up or slowed-down rhythms. Monkeys showed an overall preference for the natural rhythm compared with the perturbed rhythms. This lends behavioral support for the hypothesis that perceptual processes in monkeys are similarly tuned to the natural frequencies of communication signals as they are in humans. Our data provide perceptual evidence for the theory that speech may have evolved from ancestral primate rhythmic facial expressions.

Cooperative vocal control in marmoset monkeys via vocal feedback.

Humans adjust speech amplitude as a function of distance from a listener; we do so in a manner that would compensate for such distance. This ability is presumed to be the product of high-level sociocognitive skills. Nonhuman primates are thought to lack such socially related flexibility in vocal production. Using predictions from a simple arousal-based model whereby vocal feedback from a conspecific modulates the drive to produce a vocalization, we tested whether another primate exhibits this type of cooperative vocal control. We conducted a playback experiment with marmoset monkeys and simulated "far-away" and "nearby" conspecifics using contact calls that differed in sound intensity. We found that marmoset monkeys increased the amplitude of their contact calls and produced such calls with shorter response latencies toward more distant conspecifics. The same was not true in response to changing levels of background noise. To account for how simulated conspecific distance can change both the amplitude and timing of vocal responses, we developed a model that incorporates dynamic interactions between the auditory system and limbic "drive" systems. Overall, our data show that, like humans, marmoset monkeys cooperatively control the acoustics of their vocalizations according to changes in listener distance, increasing the likelihood that a conspecific will hear their call. However, we propose that such cooperative vocal control is a system property that does not necessitate any particularly advanced sociocognitive skill. At least in marmosets, this vocal control can be parsimoniously explained by the regulation of arousal states across two interacting individuals via vocal feedback.

Facial expressions and the evolution of the speech rhythm.

In primates, different vocalizations are produced, at least in part, by making different facial expressions. Not surprisingly, humans, apes, and monkeys all recognize the correspondence between vocalizations and the facial postures associated with them. However, one major dissimilarity between monkey vocalizations and human speech is that, in the latter, the acoustic output and associated movements of the mouth are both rhythmic (in the 3- to 8-Hz range) and tightly correlated, whereas monkey vocalizations have a similar acoustic rhythmicity but lack the concommitant rhythmic facial motion. This raises the question of how we evolved from a presumptive ancestral acoustic-only vocal rhythm to the one that is audiovisual with improved perceptual sensitivity. According to one hypothesis, this bisensory speech rhythm evolved through the rhythmic facial expressions of ancestral primates. If this hypothesis has any validity, we expect that the extant nonhuman primates produce at least some facial expressions with a speech-like rhythm in the 3- to 8-Hz frequency range. Lip smacking, an affiliative signal observed in many genera of primates, satisfies this criterion. We review a series of studies using developmental, x-ray cineradiographic, EMG, and perceptual approaches with macaque monkeys producing lip smacks to further investigate this hypothesis. We then explore its putative neural basis and remark on important differences between lip smacking and speech production. Overall, the data support the hypothesis that lip smacking may have been an ancestral expression that was linked to vocal output to produce the original rhythmic audiovisual speech-like utterances in the human lineage.

Individual recognition through olfactory-auditory matching in lemurs.

Individual recognition can be facilitated by creating representations of familiar individuals, whereby information from signals in multiple sensory modalities become linked. Many vertebrate species use auditory-visual matching to recognize familiar conspecifics and heterospecifics, but we currently do not know whether representations of familiar individuals incorporate information from other modalities. Ring-tailed lemurs (Lemur catta) are highly visual, but also communicate via scents and vocalizations. To investigate the role of olfactory signals in multisensory recognition, we tested whether lemurs can recognize familiar individuals through matching scents and vocalizations. We presented lemurs with female scents that were paired with the contact call either of the female whose scent was presented or of another familiar female from the same social group. When the scent and the vocalization came from the same individual versus from different individuals, females showed greater interest in the scents, and males showed greater interest in both the scents and the vocalizations, suggesting that lemurs can recognize familiar females via olfactory-auditory matching. Because identity signals in lemur scents and vocalizations are produced by different effectors and often encountered at different times (uncoupled in space and time), this matching suggests lemurs form multisensory representations through a newly recognized sensory integration underlying individual recognition.

Convergent evolution of vocal cooperation without convergent evolution of brain size.

One pragmatic underlying successful vocal communication is the ability to take turns. Taking turns - a form of cooperation - facilitates the transmission of signals by reducing the amount of their overlap. This allows vocalizations to be better heard. Until recently, non-human primates were not thought of as particularly cooperative, especially in the vocal domain. We recently demonstrated that common marmosets (Callithrix jacchus), a small New World primate species, take turns when they exchange vocalizations with both related and unrelated conspecifics. As the common marmoset is distantly related to humans (and there is no documented evidence that Old World primates exhibit vocal turn taking), we argue that this ability arose as an instance of convergent evolution, and is part of a suite of prosocial behavioral tendencies. Such behaviors seem to be, at least in part, the outcome of the cooperative breeding strategy adopted by both humans and marmosets. Importantly, this suite of shared behaviors occurs without correspondence in encephalization. Marmoset vocal turn taking demonstrates that a large brain size and complex cognitive machinery is not needed for vocal cooperation to occur. Consistent with this idea, the temporal structure of marmoset vocal exchanges can be described in terms of coupled oscillator dynamics, similar to quantitative descriptions of human conversations. We propose a simple neural circuit mechanism that may account for these dynamics and, at its core, involves vocalization-induced reductions of arousal. Such a mechanism may underlie the evolution of vocal turn taking in both marmoset monkeys and humans.

Vocal communication is multi-sensorimotor coordination within and between individuals.

Speech is an exquisitely coordinated interaction among effectors both within and between individuals. No account of human communication evolution that ignores its foundational multisensory characteristics and cooperative nature will be satisfactory. Here, we describe two additional capacities - rhythmic audiovisual speech and cooperative communication - and suggest that they may utilize the very same or similar circuits as those proposed for vocal learning.

The central role of the individual in the history of brains.

Every species' brain, body and behavior is shaped by the contingencies of their evolutionary history; these exert pressures that change their developmental trajectories. There is, however, another set of contingencies that shape us and other animals: those that occur during a lifetime. In this perspective piece, we show how these two histories are intertwined by focusing on the individual. We suggest that organisms--their brains and behaviors--are not solely the developmental products of genes and neural circuitry but individual centers of action unfolding in time. To unpack this idea, we first emphasize the importance of variation and the central role of the individual in biology. We then go over "errors in time" that we often make when comparing development across species. Next, we reveal how an individual's development is a process rather than a product by presenting a set of case studies. These show developmental trajectories as emerging in the contexts of the "the actual now" and "the presence of the past". Our consideration reveals that individuals are slippery-they are never static; they are a set of on-going, creative activities. In light of this, it seems that taking individual development seriously is essential if we aspire to make meaningful comparisons of neural circuits and behavior within and across species.

Active sampling as an information seeking strategy in primate vocal interactions.

Active sensing is a behavioral strategy for exploring the environment. In this study, we show that contact vocal behaviors can be an active sensing mechanism that uses sampling to gain information about the social environment, in particular, the vocal behavior of others. With a focus on the real-time vocal interactions of marmoset monkeys, we contrast active sampling to a vocal accommodation framework in which vocalizations are adjusted simply to maximize responses. We conduct simulations of a vocal accommodation and an active sampling policy and compare them with actual vocal interaction data. Our findings support active sampling as the best model for real-time marmoset monkey vocal exchanges. In some cases, the active sampling model was even able to partially predict the distribution of vocal durations for individuals to approximate the optimal call duration. These results suggest a non-traditional function for primate vocal interactions in which they are used by animals to seek information about their social environments.

Facial muscle coordination in monkeys during rhythmic facial expressions and ingestive movements.

Evolutionary hypotheses regarding the origins of communication signals generally suggest, particularly for the case of primate orofacial signals, that they derive by ritualization of noncommunicative behaviors, notably including ingestive behaviors such as chewing and nursing. These theories are appealing in part because of the prominent periodicities in both types of behavior. Despite their intuitive appeal, however, there are little or no data with which to evaluate these theories because the coordination of muscles innervated by the facial nucleus has not been carefully compared between communicative and ingestive movements. Such data are especially crucial for reconciling neurophysiological assumptions regarding facial motor control in communication and ingestion. We here address this gap by contrasting the coordination of facial muscles during different types of rhythmic orofacial behavior in macaque monkeys, finding that the perioral muscles innervated by the facial nucleus are rhythmically coordinated during lipsmacks and that this coordination appears distinct from that observed during ingestion.

Active Sampling in Primate Vocal Interactions.

Active sensing is a behavioral strategy for exploring the environment. In this study, we show that contact vocal behaviors can be an active sensing mechanism that uses sampling to gain information about the social environment, in particular, the vocal behavior of others. With a focus on the realtime vocal interactions of marmoset monkeys, we contrast active sampling to a vocal accommodation framework in which vocalizations are adjusted simply to maximize responses. We conducted simulations of a vocal accommodation and an active sampling policy and compared them with real vocal exchange data. Our findings support active sampling as the best model for marmoset monkey vocal exchanges. In some cases, the active sampling model was even able to predict the distribution of vocal durations for individuals. These results suggest a new function for primate vocal interactions in which they are used by animals to seek information from social environments.