Neurotrophins and functional differentiation of the geniculate and trigeminal ganglia.

Abstract

Neurotrophins are essential for the development of sensory neurons. The trigeminal ganglion provides most of the orofacial somatosensory innervation (touch, pain, and temperature) while the geniculate ganglion is a major source of innervation to mammalian taste organs, the taste buds, including those in the soft palate and in fungiform papillae on the anterior two thirds of the tongue. Neurites from these two ganglia join outside of the skull and course together to innervate adjacent but distinct regions of taste papillae on the anterior tongue. In and around the papilla, neurotrophins are expressed in a distinct spatial pattern with brain-derived neurotrophic factor (BDNF) mRNA located in the area of future taste bud development, while neurotrophin 3 (NT3) mRNA is located in adjacent non-taste epithelium and in the papilla core. Geniculate neurons will innervate the BDNF-containing area where taste buds will develop, while trigeminal neurons will innervate the NT3-containing non-taste epithelium of the papillae. This unique arrangement, where neurons from two anatomically distinct ganglia innervate adjacent but distinct targets with different neurotrophin expression patterns, provides a model to study the effects of neurotrophins on developmental biology of sensory neurons. To study the role of neurotrophins in development of geniculate and trigeminal neurons, ganglia were explanted from embryonic rats and maintained in culture with added BDNF, neurotrophin 4 (NT4), nerve growth factor (NGF), or NT3. Survival (cell counts), morphological (density of neurite outgrowth), and functional (electrophysiological properties) differentiation of neurons were evaluated at two embryonically distinct stages, before and after papilla innervation. Results indicate that geniculate ganglion neurons have highly neurotrophin-specific survival, morphological, and functional characteristics, so that neurons supported under different neurotrophin conditions are very different from each other. On the other hand, trigeminal neurons have similar neurite outgrowth density under different neurotrophins, suggesting a less specific response to neurotrophins that perhaps reflects the more heterogeneous neuronal population compared to the geniculate ganglion. The results indicate that geniculate neurons have neurotrophin-specific responses at early embryonic stages and suggest that neurotrophins encountered by geniculate neurons in and on their way to target organs can play a vital role in determining survival, morphological, and functional differentiation. In turn, differentiation of these properties will be essential to the formation of a properly functioning taste system.