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 degrees C; gradual cooling and warming (1 degrees C/s change in water temperature >5 s) from an adapted tongue temperature of 25 degrees C; gradual cooling from an adapted temperature of 40 degrees C; and gradual warming from an adapted temperature of 10 degrees C. Hierarchical cluster analysis of the taste responses at 25 degrees C divided 50 neurons into two major categories of narrowly tuned (Sucrose-specialists, NaCl-specialists) and broadly tuned (NaCl-generalists(I), NaCl- generalists(II), Acid-generalists, and QHCl-generalists) groups. NaCl specialists were excited by cooling from 25 to 10 degrees C and inhibited by warming from 10 to 25 degrees C. Acid-generalists were excited by cooling from 40 to 25 degrees C but not from 25 to 10 degrees 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 degrees 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.

Temperature Influences Chorda Tympani Nerve Responses to Sweet, Salty, Sour, Umami, and Bitter Stimuli in Mice

“…Most electrophysiological investigations in the taste field are employed at room temperature. In rats, the majority taste stimuli are severely reduced if not abolished below room temperature (Breza et al 2006). Additionally, we (Breza et al 2006;Lu et al 2012) and Lyall et al (2004) have shown that responses to some taste stimuli increase with increasing temperature, whereas responses to other taste stimuli show an inverted U-shaped function.…”

“…In rats, the majority taste stimuli are severely reduced if not abolished below room temperature (Breza et al 2006). Additionally, we (Breza et al 2006;Lu et al 2012) and Lyall et al (2004) have shown that responses to some taste stimuli increase with increasing temperature, whereas responses to other taste stimuli show an inverted U-shaped function. However, much is still unknown on how temperature influences taste intensity within (e.g., sucrose vs. sucralose or HCl vs. acetic acid) and across separate taste qualities in the peripheral nervous system.…”

“…We used stimulus concentrations that could be analyzed over a large temperature range, because cool temperatures suppress the magnitude of peripheral taste responses in rats (Nakamura and Kurihara 1988;Lundy et al 1997;Talavera et al 2005;Breza et al 2006). We used 0.5 M sucrose, glucose, fructose, and maltose and 0.02 M saccharin and sucralose, all highly preferred by B6 mice Inoue et al 2001).…”

“…it is generally accepted that changes in solution temperature activate trigeminal nerve fibers in the oral cavity (Lundy and Contreras 1994;Pittman and Contreras 1998), solution temperature modulates responses of peripheral-gustatory neurons to taste stimuli and can act as a stimulus alone in these gustatory neurons (Ogawa et al 1968;Lundy and Contreras 1999;Breza et al 2006). This latter point indicates that temperature's influence on taste perception begins at a peripheral level.…”

“…Furthermore, despite numerous lines of evidence that sucrose, salt, sour, and bitter taste neurons are modulated by temperature in the peripheral nervous system of rats (Ogawa et al 1968;Lundy and Contreras 1999;Breza et al 2006), the influence of temperature on taste responses representing the 5 basic taste qualities has not been reported in the peripheral nervous system of mice. Most electrophysiological investigations in the taste field are employed at room temperature.…”