5‐HT_3A‐driven green fluorescent protein delineates gustatory fibers innervating sour‐responsive taste cells: A labeled line for sour taste?

Abstract

Taste buds contain multiple cell types with each type expressing receptors and transduction components for a subset of taste qualities. The sour sensing cells, Type III cells, release serotonin (5-HT) in response to the presence of sour (acidic) tastants and this released 5-HT activates 5-HT3 receptors on the gustatory nerves. We show here, using Htr3a-EGFP mice, that 5-HT3-expressing nerve fibers preferentially contact and synapse with Type III taste cells. Further, these 5-HT3-expressing nerve fibers terminate in a restricted central-lateral portion of the nucleus of the solitary tract (nTS) – the same area that shows increased c-Fos expression upon presentation of a sour tastant (30 mM citric acid). This acid stimulation also evokes c-Fos in the laterally adjacent mediodorsal spinal trigeminal nucleus (DMSp5), but this trigeminal activation is not associated with the presence of 5-HT3-expressing nerve fibers as it is in the nTS. Rather, the neuronal activation in the trigeminal complex likely is attributable to direct depolarization of acid-sensitive trigeminal nerve fibers, e.g. polymodal nociceptors, rather than through taste buds. Taken together, these findings suggest that transmission of sour taste information involves communication between Type III taste cells and 5-HT3-expressing afferent nerve fibers that project to a restricted portion of the nTS consistent with the mapping of taste quality information in the primary gustatory nucleus.

Function, Innervation, and Neurotransmitter Signaling in Mice Lacking Type-II Taste Cells

“…We have expanded on this observation to examine the geniculate ganglion using mice expressing GFP from the serotonin receptor Htr3a promoter. Geniculate neurons expressing 5-HT 3A -GFP preferentially innervate the serotonergic Type III taste cells and these neurons respond to both 5-HT and ATP, while neurons lacking GFP expression respond only to ATP Stratford et al, 2017). A recent study confirms that most 5-HT 3A fibers innervate Type III cells.…”

“…Skn-1a -/mice have the same number of 5-HT 3Aexpressing geniculate ganglion neurons as the WT littermates Maeda et al (2017) showed, via retrograde transfer of WGA from Type III cells, that the total number of nodose/ petrosal ganglion neurons that innervate Type III cells remains unchanged in Skn-1a -/mice, despite the increased number of Type III cells. All gustatory neurons express the P2X-family purinergic receptors and a subset expresses 5-HT 3 receptors which preferentially contacts Type III cells Stratford et al, 2017). We tested the hypothesis that additional geniculate ganglia express x 2 (5, N = 302) = 219.74, p , 0.0001 CV_WT vs CV_KO: p , 0.0001 FF_WT vs FF_KO: p = 0.0395 SP_WT vs SP_KO: p = 0.00331 Figure 3A Two-factors (genotype and tastants); data are continuous Two-way ANOVA WT mice: n = 6 Skn-1a -/mice: n = 6…”

“…These results suggest that connections between taste cells and ganglion cells are not influenced by the type of cells expressed in the tongue but are predetermined. What is not clear, however, is whether the additional Type III cells in the Skn-1a -/mice are innervated by ganglion neurons expressing the serotonin receptor 5-HT 3A , as in WT mice (Stratford et al, 2017). Here, we have crossed the Skn-1a -/animals with mice expressing GFP from the Htr3a promoter and examined the progeny for 5-HT 3A expression and function in the geniculate ganglion.…”

Transcriptomes and neurotransmitter profiles of classes of gustatory and somatosensory neurons in the geniculate ganglion

“…Recent reports 26 , 31 have proposed that Htr3a -GFP marks gustatory neurons that selectively innervate sour-sensing taste bud cells. In contrast, our transcriptome data indicate that Htr3a is expressed quite broadly within all sub-types of gustatory and even some somatosensory neurons (Fig.…”

Variable branching characteristics of peripheral taste neurons indicates differential convergence

“…While individual contacts may not be particularly meaningful, numbers or patterns can be compared across groups. For example, taste neurons expressing the serotonin receptor contact more sour receptor cells (which produce serotonin) than other cell types (Stratford, Larson et al 2017).…”