The transcription factor Phox2b distinguishes between oral and non‐oral sensory neurons in the geniculate ganglion

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Taste receptor cells located on the tongue and palate detect the chemical content of food and respond to various taste qualities such as bitter or sweet (Chaudhari & Roper, 2010). Afferent fibers from neurons in the geniculate and petrosal ganglia innervate these taste receptor cells and carry taste information to the first synaptic relay of the brain, the nucleus of the solitary tract (Krimm, 2007). Although our understanding of taste receptor cells has advanced considerably over the past two decades, the neurons that innervate these cells are still poorly understood, at least in part due to the lack of specific molecular markers for taste neurons.
The geniculate ganglion contains taste neurons that project through the chorda tympani and greater superficial petrosal nerves; however, it also contains non‐gustatory neurons, most notably those innervating the external acoustic meatus through the posterior auricular nerve (Folan‐Curran & Cooke, 2001; Gomez, 1978; Semba, Sood, Shu, Nagele, & Egger, 1984). Although the exact proportion of geniculate ganglion neurons that project to the tongue and palate is unknown, estimates in the rat range from 50 to 70% (Gomez, 1978; Semba et al., 1984). The quantification of innervation to taste buds is limited by labels that do not primarily label taste fibers (e.g., neurofilaments; Krimm, Miller, Kitzman, Davis, & Albers, 2001), labels that also identify certain subpopulations of taste cells (e.g., NCAM; Nosrat, Margolskee, & Nosrat, 2012; Yee, Yang, Bottger, Finger, & Kinnamon, 2001), or that show a patchy appearance and likely do not label entire nerve fibers (e.g., P2X3; Huang, Ma, & Krimm, 2015).
Taste neurons, similarly to those innervating digestive, respiratory, and cardiovascular end organs, can be described as “visceral” sensory neurons, whereas those innervating the pinna and external ear canal can be classified as somatosensory neurons, because they innervate external structures. Thus, a transcription factor that regulates visceral sensory neuron development would be a useful candidate for identifying gustatory neurons in the geniculate ganglion. Phox2b is a homeodomain transcription factor that is essential for development of the placodally‐derived geniculate and petrosal ganglion (Dauger et al., 2003). An early study reports the widespread expression of Phox2b in the geniculate ganglion and the degeneration of the entire ganglion upon Phox2b deficiency (Dauger et al., 2003), implying limited specificity. However, Phox2b was more recently found to be expressed in roughly half of the geniculate ganglion (D'Autreaux, Coppola, Hirsch, Birchmeier, & Brunet, 2011), suggesting that Phox2b might be specifically expressed by gustatory neurons within the ganglion.
Here, our goal was to characterize a genetic label for taste neurons projecting through the chorda tympani and greater superficial petrosal nerves that could be used to further investigate taste bud innervation. To accomplish this goal, we used a Phox2b‐Cre‐tdTomato mouse line in which all neurons expressing Phox2b (at any time during development) would be genetically labeled. We found that Phox2b was specifically expressed in the 42% of geniculate ganglion neurons that projected through the chorda tympani and the greater superficial petrosal nerves. All tdTomato‐positive fibers within taste buds in the fungiform papillae originated from the chorda tympani permitting measurement of total volume of innervation within the taste bud. The Phox2b construct allows for both genetic access and labeling of taste neurons.
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