Rapid structural remodeling of peripheral taste fibers is independent of taste cell turnover

Abstract

Taste bud cells are constantly replaced in taste buds as old cells die and new cells migrate into the bud. The perception of taste relies on new taste bud cells integrating with existing neural circuitry, yet how these new cells connect with a taste ganglion neuron is unknown. Do taste ganglion neurons remodel to accommodate taste bud cell renewal? If so, how much of the taste axon structure is fixed and how much remodels? Here we measured the motility and branching of individual taste arbors (the portion of the axon innervating taste buds) over time with two-photon in vivo microscopy. Terminal branches of taste arbors continuously and rapidly remodel within the taste bud. This remodeling is faster than predicted by taste bud cell renewal, with terminal branches added and lost concurrently. Surprisingly, ablating new taste cells with chemotherapeutic agents revealed that remodeling of the terminal branches of taste arbors does not rely of the renewal of taste bud cells. Although the arbor structure remodeling was fast and intrinsically controlled, no new arbors were added, and few were lost over 100 days. Taste ganglion neurons maintain a stable number of nerve arbors that are each capable of high-speed remodeling. Arbor structural plasticity would permit arbors to locate new taste bud cells, while stability of arbor number could support constancy in the degree of connectivity and function for each neuron over time.