Embryonic origin of gustatory cranial sensory neurons

Abstract

Cranial nerves VII, IX and X provide both gustatory (taste) and non-gustatory (touch, pain, temperature) innervation to the oral cavity of vertebrates. Gustatory neurons innervate taste buds and project centrally to the rostral nucleus of the solitary tract (NTS), whereas neurons providing general epithelial innervation to the oropharynx project to non-gustatory hindbrain regions, i.e., spinal trigeminal nucleus. In addition to this dichotomy in function, cranial ganglia VII, IX and X have dual embryonic origins, comprising sensory neurons derived from both cranial neural crest and epibranchial placodes. We used a fate mapping approach to test the hypothesis that epibranchial placodes give rise to gustatory neurons, whereas the neural crest generates non-gustatory cells. Placodal ectoderm or neural crest was grafted from Green Fluorescent Protein (GFP) expressing salamander embryos into unlabeled hosts, allowing us to discern the postembryonic central and peripheral projections of each embryonic neuronal population. Neurites that innervate taste buds are exclusively placodal in origin, and their central processes project to the NTS, consistent with a gustatory fate. In contrast, neural crest-derived neurons do not innervate taste buds; instead, neurites of these sensory neurons terminate as free nerve endings within the oral epithelium. Further, the majority of centrally directed fibers of neural crest neurons terminate outside the NTS, in regions that receive general epithelial afferents. Our data provide empirical evidence that embryonic origin dictates mature neuron function within cranial sensory ganglia: specifically, gustatory neurons derive from epibranchial placodes, whereas neural crest-derived neurons provide general epithelial innervation to the oral cavity.