Modulation of taste processing by temperature

Abstract

Taste stimuli have a temperature that can stimulate thermosensitive neural machinery in the mouth during gustatory experience. Although taste and oral temperature are sometimes discussed as different oral sensory modalities, there is a body of literature that demonstrates temperature is an important component and modulator of the intensity of gustatory neural and perceptual responses. Available data indicate that the influence of temperature on taste, herein referred to as "thermogustation," can vary across taste qualities, can also vary among stimuli presumed to share a common taste quality, and is conditioned on taste stimulus concentration, with neuronal and psychophysical data revealing larger modulatory effects of temperature on gustatory responding to weakened taste solutions compared with concentrated. What is more, thermogustation is evidenced to involve interplay between mouth and stimulus temperature. Given these and other dependencies, identifying principles by which thermal input affects gustatory information flow in the nervous system may be important for ultimately unravelling the organization of neural circuits for taste and defining their involvement with multisensory processing related to flavor. Yet thermal effects are relatively understudied in gustatory neuroscience. Major gaps in our understanding of the mechanisms and consequences of thermogustation include delineating supporting receptors, the potential involvement of oral thermal and somatosensory trigeminal neurons in thermogustatory interactions, and the broader operational roles of temperature in gustatory processing. This review will discuss these and other issues in the context of the literature relevant to understanding thermogustation.

Keywords: flavor; multisensory; somatosensation; taste; temperature.

Fig. 1.

Schematic of peripheral and early central nervous system (CNS) pathways in the rodent associated with thermogustatory and oral thermal processing. This schematic does not intend to show anatomically precise scale or projection routes and highlights only forward connections between peripheral and central pathways related to the literature discussed in this review. Cranial nerves known to mediate thermogustatory and oral thermal input to CNS structures are marked by Roman numerals. Pathways and receptor mechanisms implicated for taste and thermal processing are marked green. Trigeminal-specific pathways and mechanisms are marked red. Dotted red arrows denote known trigeminal projections [references: V → NTS (28, 38); Sp5 → NTS (154); Sp5 → PbN (23)] of unknown function in thermotaste processing. ENaC, epithelial sodium channel; TRP, transient receptor potential; TRPM5, TRP melastatin 5 ion channel; TRPM8, TRP melastatin 8 ion channel; TRPV1, TRP vanilloid 1 ion channel; NTS, nucleus tractus solitarius; Sp5, spinal trigeminal nucleus; PbN, parabrachial nucleus.

Fig. 2.

Effects of temperature can differ across taste qualities. Example electrophysiological data depicting the mean standardized maximum response of the rat chorda tympani nerve (ordinate) to reduced concentrations of sodium chloride (NaCl; “salty”) and hydrochloric acid (HCl; “sour”) plotted against temperature (abscissa). This work aimed to determine whether lower concentrations of HCl would elicit a decrease in gustatory nerve firing with warming, as shown for a low concentration (0.01 M) of NaCl. Yet across concentrations, nerve responses to HCl peaked with warming to around 30°C. Adapted from Yamashita and Sato (149) with permission.

Fig. 3.

Effect of temperature on gustatory responding can rely on stimulus concentration. Example electrophysiological data depicting the mean standardized initial response of the rat chorda tympani nerve (ordinate) to various concentrations of sodium chloride (NaCl) plotted against temperature (abscissa). The temperature that optimizes nerve firing to 0.01, 0.03, and 0.1 M NaCl is seen to systematically increase with concentration. Adapted from Yamashita and Sato (149) with permission.

Fig. 4.

Temperature and concentration interact to shape gustatory neural firing. Example electrophysiological data obtained from sodium-sensitive rat chorda tympani neurons showing their mean spike firing (ordinate) to a series of low to high concentrations of NaCl (abscissa) applied to the tongue at multiple cool and warm temperatures. Data are plotted in double logarithmic coordinates. Cooling markedly enhanced neural firing to low concentrations of NaCl (e.g., 0.01 M), whereas select warmer temperatures could enhance firing to high concentrations (e.g., 0.3 M), albeit the latter effect was relatively smaller. The ability of temperature to modulate unit firing to NaCl is generally decreased at high concentrations. These data represent an early description of how temperature and concentration can interactively control gustatory response magnitude in single neurons. Adapted from Yamashita, Ogawa, Kiyohara, and Sato (148) with permission.

Fig. 5.

Superadditive effects of temperature on gustatory neural responding. A: example raw electrophysiological sweeps depicting spiking activity by an individual taste-active neuron in the mouse nucleus tractus solitarius (NTS) to oral delivery of water (top) and 0.3 M sucrose (bottom) at 21°C (left) and 31°C (right). Temperature values reflect oral stimulus temperature within ±1°C. Upward arrow denotes stimulus onset. As shown, this neuron was mostly insensitive to thermal stimulation in the absence of taste, giving 0.6 and 0.3 spikes/s to water at 21°C and 31°C, respectively. However, the cell was responsive to sucrose and increased its firing to this input from 4.1 to 14.4 spikes/s with warming from 21°C to 31°C. This increase reflects a +251% change in firing that is considered superadditive; the increase far exceeds the response level that would be achieved if sucrose and warmth inputs to this neuron combined through simple addition (i.e., the sum of activity to 21°C sucrose and 31°C water). Unpublished cell; methods for data acquisition as described in Wilson and Lemon (144). B: peristimulus time histograms (PSTHs; 500 ms bins) showing the mean spike firing (ordinate) of 39 mouse NTS neurons during 5-s oral deliveries of warm (~30°C) water and 0.1 M sucrose tested at room (~22°C) and warm temperatures. The black-lined PSTH is the addition of the PSTHs for room temperature sucrose and warm water; this additive-predicted trace represents the response level expected if enhanced firing to warm sucrose was caused by simple addition of activity to warmth and room temperature sucrose. Yet during the stimulus period (0 to 5 s), the additive-predicted PSTH is lower than the PSTH for warm sucrose (shaded regions represent ± SE). Furthermore, the mean number of spikes present during the stimulus period was greater for warm sucrose compared with the additive-predicted response (paired t-test on normally distributed data: t₃₈ = 3.3, P = 0.002). Thus the increase in firing to sucrose with warming is superadditive. Data are from neurons described in Wilson and Lemon (144).

Fig. 6.

Temperature can change the breadth of neural responsiveness across taste qualities. A: example raw electrophysiological sweeps depicting spiking activity by an individual taste-active neuron in the mouse nucleus tractus solitarius (NTS) to oral delivery of sucrose (“sweet”), NaCl (“salty”), HCl (“sour”), quinine (“bitter), and water at 18°C (left) and 30°C (right). The H metric, which quantitatively gauges the breadth of tuning of individual neurons to gustatory stimuli (123), is given at the top of the column for each temperature condition. For four taste stimuli as shown here, an H that that approaches 0 indicates narrow responsiveness by a neuron to only one taste stimulus, a value around 0.5 can reflect robust firing to two stimuli, and a value approaching 1 can reflect responding by a cell across all four tastants (e.g., 128, 144). This unit fired spikes to only NaCl and HCl when stimuli were tested at 18°C. The cell showed increased breath of tuning and responded to all tastants when stimuli were warmed to 30°C. Note that for this cell, spike firing to warmed sucrose and quinine is greater than elicited by warming alone, which is represented by the sweep for 30°C water. Neuron from Wilson and Lemon (144). B: analysis of temperature effects on the breath of gustatory neural tuning. Depicted are histograms of bootstrapped median H values computed from electrophysiological responses by 39 mouse NTS neurons to oral delivery of 0.1 M sucrose, 0.03 M NaCl, 0.003 M HCl, and 0.003 M quinine delivered at each of five stimulus temperatures. The sample median H value and its bootstrapped ± 95% confidence interval is given as a point and whiskers above each histogram. Neural H values increased with warming, as revealed by no overlap among confidence intervals for the coolest (16°C and 18°C) and warmest (30°C and 37°C) temperatures. Thus cooling can narrow and warming can broaden the tuning of gustatory neurons to taste qualities. Data are from neurons described in Wilson and Lemon (144).