Initial innervation of embryonic rat tongue and developing taste papillae: nerves follow distinctive and spatially restricted pathways.
The rat tongue has an extensive, complex innervation from four cranial nerves. However, the precise developmental time course and spatial routes of these nerves into the embryonic tongue are not known, although this knowledge is crucial for studying mechanisms that regulate development and innervation of the lingual taste organs, gustatory papillae and resident taste buds. We determined the initial spatial course of nerves in the developing tongue and papillae, and tested the hypothesis that sensory nerves first innervate the tongue homogeneously and then retract to more densely innervate papillae and taste buds. Antibodies to GAP-43 and neurofilaments were used to label nerve fibers in rat embryo heads from gestational day 11 through 16 (E11-E16). Serial sagittal sections were traced and reconstructed to follow paths of each nerve. In E11 rat, geniculate, trigeminal and petrosal ganglia were labeled and fibers left the ganglia and extended toward respective branchial arches. At E13 when the developing tongue is still a set of tissue swellings, the combined chorda/lingual, hypoglossal and petrosal nerves approached the lingual swellings from separate positions. Only the chorda/lingual entered the tongue base at this stage. At E14 and E15, the well-developed tongue was innervated by all four cranial nerves. However, the nerves maintained distinctive entry points and relatively restricted mesenchymal territories within the tongue, and did not follow one another in common early pathways. Furthermore, the chorda/lingual and glossopharyngeal nerves did not set up an obvious prepattern for gustatory papilla development, but rather seemed attracted to developing papillae which became very densely innervated compared to surrounding epithelium at E15. To effect this dense papilla innervation, sensory nerves did not first innervate the tongue in a homogeneous manner with subsequent retraction and/or extensive redirection of fibers into the taste organs. Results contribute to a set of working principles for development of tongue innervation. Points of entry and initial neural pathways are restricted from time of tongue formation through morphogenesis, suggesting distinctive lingual territories for each nerve. Thus, sensory and motor nerves distribute independently of each other, and sensory innervation to anterior and posterior tongue remains discrete. For taste organ innervation, gustatory papillae are not induced by a prepatterned nerve distribution. In fact, papillae might attract dense sensory innervation because neither chorda/lingual nor glossopharyngeal nerve grows homogeneously to the lingual epithelium and then redistributes to individual papillae.
Department of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor 48109-1078, USA.
J P
JP
Mbiene
C M
CM
Mistretta
D000818:Animals; D001369:Axons / Q000737:chemistry / Q000502:physiology / Q000648:ultrastructure; D002814:Chorda Tympani Nerve / Q000196:embryology; D003391:Cranial Nerves / Q000196:embryology*; D019922:GAP-43 Protein / Q000032:analysis; D017950:Ganglia, Sensory / Q000737:chemistry; D005930:Glossopharyngeal Nerve / Q000196:embryology; D007002:Hypoglossal Nerve / Q000196:embryology; D007150:Immunohistochemistry; D008036:Lingual Nerve / Q000196:embryology; D009024:Morphogenesis; D009434:Neural Pathways; D016501:Neurites / Q000648:ultrastructure; D051381:Rats; D017207:Rats, Sprague-Dawley; D013650:Taste Buds / Q000196:embryology*; D014059:Tongue / Q000196:embryology* / Q000294:innervation*
D019922:GAP-43 Protein