Repulsive Interactions Shape the Morphologies and Functional Arrangement of Zebrafish Peripheral Sensory Arbors

Background: Trigeminal sensory neurons detect thermal and mechanical stimuli in the skin through their elaborately arborized peripheral axons. We investigated the developmental mechanisms that determine the size and shape of individual trigeminal arbors in zebrafish and analyzed how these interactions affect the functional organization of the peripheral sensory system.

Results: Time-lapse imaging indicated that direct repulsion between growing axons restricts arbor territories. Removal of one trigeminal ganglion allowed axons of the contralateral ganglion to cross the midline, and removal of both resulted in the expansion of spinal cord sensory neuron arbors. Generation of embryos with single, isolated sensory neurons resulted in axon arbors that possessed a vast capacity for growth and expanded to encompass the entire head. Embryos in which arbors were allowed to aberrantly cross the midline were unable to respond in a spatially appropriate way to mechanical stimuli.

Conclusions: Direct repulsive interactions between developing trigeminal and spinal cord sensory axon arbors determine sensory neuron organization and control the shapes and sizes of individual arbors. This spatial organization is crucial for sensing the location of objects in the environment. Thus, a combination of undirected growth and mutual repulsion results in the formation of a functionally organized system of peripheral sensory arbors.