A primal role for the vestibular sense in the development of coordinated locomotion.

David E Ehrlich,David Schoppik

doi:10.7554/elife.45839

Abstract

Mature locomotion requires that animal nervous systems coordinate distinct groups of muscles. The pressures that guide the development of coordination are not well understood. To understand how and why coordination might emerge, we measured the kinematics of spontaneous vertical locomotion across early development in zebrafish (Danio rerio) . We found that zebrafish used their pectoral fins and bodies synergistically during upwards swims. As larvae developed, they changed the way they coordinated fin and body movements, allowing them to climb with increasingly stable postures. This fin-body synergy was absent in vestibular mutants, suggesting sensed imbalance promotes coordinated movements. Similarly, synergies were systematically altered following cerebellar lesions, identifying a neural substrate regulating fin-body coordination. Together these findings link the vestibular sense to the maturation of coordinated locomotion. Developing zebrafish improve postural stability by changing fin-body coordination. We therefore propose that the development of coordinated locomotion is regulated by vestibular sensation.

Highlights

To locomote, the nervous system coordinates multiple effectors, such as the trunk and limbs or fins, that collectively generate propulsive forces and maintain body posture
To examine how and why fish regulate fin-body coordination across development, we studied larval zebrafish (Danio rerio) as they spontaneously climbed in the water column
We found that larvae at all ages exhibited correlated fin-driven lift and body rotations, strong evidence for active fin-body coordination

Summary

Introduction

The nervous system coordinates multiple effectors, such as the trunk and limbs or fins, that collectively generate propulsive forces and maintain body posture. Humans walk by using the legs to move the body forward, swinging the arms to reduce angular momentum, and using axial musculature to support the trunk (Collins et al, 2009). As animals mature they change the way they coordinate these effectors, a process driven both by experience and by changing motor goals (Sporns and Edelman, 1993; Thelen, 1995; Adolph, 1997). Which sensations and goals guide the development of coordination is poorly understood During development, both physical body shape and neural coordination change simultaneously (Dickinson et al, 2000). Understanding the constraints that guide neural control of coordination requires a model in which the maturation of locomotion can be dissociated from changes in physical form (Thelen and Ulrich, 1991)

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Conclusion