Abstract

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.

Highlights

  • It is well established that central pattern generators (CPGs) are constrained and modulated by the body in which they are embedded [1,2]

  • The body is not a device to be controlled by the brain, but rather is directly involved in making some behaviors less complicated for the nervous system

  • We tested this idea in a real biological system by investigating how marmoset monkey infants change their vocal behavior over time

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Summary

Introduction

It is well established (though often ignored) that central pattern generators (CPGs) are constrained and modulated by the body in which they are embedded [1,2]. In the field of robotics, much work has demonstrated how the shape and material properties of the body can be exploited to make analogous central control processes simpler; this is known as “morphological computation” [3,4,5]. In this view, the body is not a device to be controlled by the brain, but rather is directly involved in making some behaviors less complicated for the nervous system. What is not known is the role that morphological computation may or may not play in vocal development

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