Vocal development in a Waddington landscape

Abstract

Vocal development is the adaptive coordination of the vocal apparatus, muscles, the nervous system, and social interaction. Here, we use a quantitative framework based on optimal control theory and Waddington’s landscape metaphor to provide an integrated view of this process. With a biomechanical model of the marmoset monkey vocal apparatus and behavioral developmental data, we show that only the combination of the developing vocal tract, vocal apparatus muscles and nervous system can fully account for the patterns of vocal development. Together, these elements influence the shape of the monkeys’ vocal developmental landscape, tilting, rotating or shifting it in different ways. We can thus use this framework to make quantitative predictions regarding how interfering factors or experimental perturbations can change the landscape within a species, or to explain comparative differences in vocal development across species

DOI: http://dx.doi.org/10.7554/eLife.20782.001

eLife digest

As infants develop they learn new behaviors and refine existing ones. For example, human infants progress from crying to babbling to producing speech-like sounds. A complex sequence of changes in muscles, the nervous system and in patterns of interactions with other individuals all contribute to these emerging behaviors.

Despite this complexity, most studies of vocal development have only considered single factors in isolation. A study of speech development, for example, might examine how changes in the brain enable infants to imitate sounds. However, that same study will probably ignore how changes in the structure of the vocal cords, or in the behavior of the parents, also promote imitation.

Young marmoset monkeys, like human infants, gradually develop from producing immature cries to adult-like calls. Teramoto, Takahashi et al. built a computational model of this process and compared the model to data from real animals. The first version of the model focused solely on how the marmosets’ vocal cords grow, and did not fully reproduce how adult-like calls emerge in real marmosets. Teramoto, Takahashi et al. therefore added factors to the model that simulate improvements in muscle control, learning in the nervous system and in the behavior of other animals. These findings show that, to reflect how adult-like calls emerge in real marmosets, the model needs to include all of these factors.

The model developed by Teramoto, Takahashi et al. may also provide insights into why vocal learning and some other behaviors emerge in some species and not others. It may also be used to predict the consequences of disrupting individual processes in young animals at particular points in time and how such disruptions shape the way an animal develops on its way to adulthood.

DOI: http://dx.doi.org/10.7554/eLife.20782.002