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.

Author Correction: Vocal state change through laryngeal development.

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

A Hierarchy of Autonomous Systems for Vocal Production.

Vocal production is hierarchical in the time domain. These hierarchies build upon biomechanical and neural dynamics across various timescales. We review studies in marmoset monkeys, songbirds, and other vertebrates. To organize these data in an accessible and across-species framework, we interpret the different timescales of vocal production as belonging to different levels of an autonomous systems hierarchy. The first level accounts for vocal acoustics produced on short timescales; subsequent levels account for longer timescales of vocal output. The hierarchy of autonomous systems that we put forth accounts for vocal patterning, sequence generation, dyadic interactions, and context dependence by sequentially incorporating central pattern generators, intrinsic drives, and sensory signals from the environment. We then show the framework's utility by providing an integrative explanation of infant vocal production learning in which social feedback modulates infant vocal acoustics through the tuning of a drive signal.

Vocal state change through laryngeal development.

Across vertebrates, progressive changes in vocal behavior during postnatal development are typically attributed solely to developing neural circuits. How the changing body influences vocal development remains unknown. Here we show that state changes in the contact vocalizations of infant marmoset monkeys, which transition from noisy, low frequency cries to tonal, higher pitched vocalizations in adults, are caused partially by laryngeal development. Combining analyses of natural vocalizations, motorized excised larynx experiments, tensile material tests and high-speed imaging, we show that vocal state transition occurs via a sound source switch from vocal folds to apical vocal membranes, producing louder vocalizations with higher efficiency. We show with an empirically based model of descending motor control how neural circuits could interact with changing laryngeal dynamics, leading to adaptive vocal development. Our results emphasize the importance of embodied approaches to vocal development, where exploiting biomechanical consequences of changing material properties can simplify motor control, reducing the computational load on the developing brain.

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.

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.

Temperature Manipulation in Songbird Brain Implicates the Premotor Nucleus HVC in Birdsong Syntax.

Variable motor sequences of animals are often structured and can be described by probabilistic transition rules between action elements. Examples include the songs of many songbird species such as the Bengalese finch, which consist of stereotypical syllables sequenced according to probabilistic rules (song syntax). The neural mechanisms behind such rules are poorly understood. Here, we investigate where the song syntax is encoded in the brain of the Bengalese finch by rapidly and reversibly manipulating the temperature in the song production pathway. Cooling the premotor nucleus HVC (proper name) slows down the song tempo, consistent with the idea that HVC controls moment-to-moment timings of acoustic features in the syllables. More importantly, cooling HVC alters the transition probabilities between syllables. Cooling HVC reduces the number of repetitions of long-repeated syllables and increases the randomness of syllable sequences. In contrast, cooling the downstream motor area RA (robust nucleus of the acropallium), which is critical for singing, does not affect the song syntax. Unilateral cooling of HVC shows that control of syllables is mostly lateralized to the left HVC, whereas transition probabilities between the syllables can be affected by cooling HVC in either hemisphere to varying degrees. These results show that HVC is a key site for encoding song syntax in the Bengalese finch. HVC is thus involved both in encoding timings within syllables and in sequencing probabilistic transitions between syllables. Our finding suggests that probabilistic selections and fine-grained timings of action elements can be integrated within the same neural circuits.SIGNIFICANCE STATEMENT Many animal behaviors such as birdsong consist of variable sequences of discrete actions. Where and how the probabilistic rules of such sequences are encoded in the brain is poorly understood. We locally and reversibly cooled brain areas in songbirds during singing. Mild cooling of area HVC in the Bengalese finch brain-a premotor area homologous to the mammalian premotor cortex-alters the statistics of the syllable sequences, suggesting that HVC is critical for birdsong sequences. HVC is also known for controlling moment-to-moment timings within syllables. Our results show that timing and probabilistic sequencing of actions can share the same neural circuits in local brain areas.

The autonomic nervous system is the engine for vocal development through social feedback.

At least one non-human primate species-the marmoset monkey-exhibits developmental processes similar to human vocal development. These processes include babbling-like early vocal output and a role for social feedback in changing this output into mature-sounding vocalizations. Such parallel behaviors provide a window through which we can begin to understand the physiological mechanisms for how early vocalizations are produced and shaped by social feedback. The latest work shows that the acoustic structure of babbling in infant monkeys is driven by oscillations of the autonomic nervous system. It is hypothesized that this autonomic nervous system rhythm is perturbed through vocal interactions between infants and parents. These interactions gradually accelerate the transformation of immature vocalizations into mature forms.

Perinatally Influenced Autonomic System Fluctuations Drive Infant Vocal Sequences.

The variable vocal behavior of human infants is the scaffolding upon which speech and social interactions develop. It is important to know what factors drive this developmentally critical behavioral output. Using marmoset monkeys as a model system, we first addressed whether the initial conditions for vocal output and its sequential structure are perinatally influenced. Using dizygotic twins and Markov analyses of their vocal sequences, we found that in the first postnatal week, twins had more similar vocal sequences to each other than to their non-twin siblings. Moreover, both twins and their siblings had more vocal sequence similarity with each other than with non-sibling infants. Using electromyography, we then investigated the physiological basis of vocal sequence structure by measuring respiration and arousal levels (via changes in heart rate). We tested the hypothesis that early-life influences on vocal output are via fluctuations of the autonomic nervous system (ANS) mediated by vocal biomechanics. We found that arousal levels fluctuate at ∼0.1 Hz (the Mayer wave) and that this slow oscillation modulates the amplitude of the faster, ∼1.0 Hz respiratory rhythm. The systematic changes in respiratory amplitude result in the different vocalizations that comprise infant vocal sequences. Among twins, the temporal structure of arousal level changes was similar and therefore indicates why their vocal sequences were similar. Our study shows that vocal sequences are tightly linked to respiratory patterns that are modulated by ANS fluctuations and that the temporal structure of ANS fluctuations is perinatally influenced.