Temperature Modulates Taste Responsiveness and Stimulates Gustatory Neurons in the Rat Geniculate Ganglion

Abstract

In humans, temperature influences taste intensity and quality perception, and thermal stimulation itself may elicit taste sensations. However, peripheral coding mechanisms of taste have generally been examined independently of the influence of temperature. In anesthetized rats, we characterized the single-cell responses of geniculate ganglion neurons to 0.5 M sucrose, 0.1 M NaCl, 0.01 M citric acid, and 0.02 M quinine hydrochloride at a steady, baseline temperature (adapted) of 10, 25, and 40°C; gradual cooling and warming (1°C/s change in water temperature >5 s) from an adapted tongue temperature of 25°C; gradual cooling from an adapted temperature of 40°C; and gradual warming from an adapted temperature of 10°C. Hierarchical cluster analysis of the taste responses at 25°C divided 50 neurons into two major categories of narrowly tuned (Sucrose-specialists, NaCl-specialists) and broadly tuned (NaCl-generalistsI, NaCl- generalistsII, Acid-generalists, and QHCl-generalists) groups. NaCl specialists were excited by cooling from 25 to 10°C and inhibited by warming from 10 to 25°C. Acid-generalists were excited by cooling from 40 to 25°C but not from 25 to 10°C. In general, the taste responses of broadly tuned neurons decreased systematically to all stimuli with decreasing adapted temperatures. The response selectivity of Sucrose-specialists for sucrose and NaCl-specialists for NaCl was unaffected by adapted temperature. However, Sucrose-specialists were unresponsive to sucrose at 10°C, whereas NaCl-specialists responded equally to NaCl at all adapted temperatures. In conclusion, we have shown that temperature modulates taste responsiveness and is itself a stimulus for activation in specific types of peripheral gustatory neurons.