Abstract
<p>Taste information travels from the taste end organ, taste buds, to gustatory sensory neurons before integrating into central gustatory regions. In taste buds, receptor cells transduce sweet, bitter, or umami taste. Presynaptic cells directly transduce sour taste although they respond to multiple tastes as well via cell-cell communications. Salty taste is believed to be sensed by ENaC-expressing taste cells. Despite this consensus about coding in taste buds, whether information in gustatory sensory neurons is organized following the labeled-line theory or more complex coding mechanisms remains controversial. The geniculate ganglion is a major sensory ganglion of the gustatory system; it innervates fungiform and palatal taste buds. I have developed a novel approach to directly record in vivo calcium activities from neuron ensembles in the geniculate ganglion. This technique employed pirt-GCaMP3 transgenic mice, which express the genetically encoded calcium indicator GCaMP3 in all sensory neurons including geniculate neurons. In the search of how geniculate neurons encode information from taste buds, I have examined neuron responses to a panel of 5 prototypical taste stimuli (representing the five basic tastes) at three different concentrations: low (~ ½ EC50), mid-range (~ EC50) and high (saturating). I have recorded 101 neurons at low concentrations and found that 72% (N=73) of neurons responded to one of the five taste qualities (“specialists”) while 28% (N=28) of neurons responded to multiple taste qualities (“generalists”). The proportion of generalist neurons increased significantly at mid-range concentrations (51%; 79/155, p<0.0001). Consistently, the breadth of tuning of neurons at mid-range concentrations was significantly higher than at low concentrations (unpaired t test, p=0.0002). Furthermore, I have recorded neurons in response to taste stimuli at both low and high concentrations. I found that individual neurons frequently increased their breadth of tuning and specialists at low concentrations could convert to generalists at high concentrations. My observations suggest a more complex coding scheme instead of the labeled-line coding theory. In addition, I found there was no apparent topographical mapping of taste qualities onto the geniculate ganglion. I also examined salty and sour taste transmission in the taste periphery. Albeit that dilute salt (< ~ 150 mM) and high salt (> 200 mM) solutions evoke contrasting behaviors in mammals, I found that there were no separate representations for low and high salt in geniculate neurons. As for sour taste, my study suggested different mechanisms in presynaptic cells to sense weak acid and strong acid (extracellular protons). This is different from the current understanding that both extracellular protons and weak acid depolarize and evoke calcium influx in presynaptic cells. In addition, I found that GABA inhibited citric acid-evoked responses in geniculate neurons, possibly by targeting presynaptic cells. In short, my study substantiates and extends the current knowledge of taste representations in the geniculate ganglion and taste transmission in the taste periphery.</p>