Modulation of central gustatory coding by temperature

Abstract

Changes in oral temperature can influence taste perception, indicating overlap among mechanisms for taste and oral somesthesis. Medullary gustatory neurons can show cosensitivity to temperature, albeit how these cells process combined taste and thermal input is poorly understood. Here, we electrophysiologically recorded orosensory responses (spikes) from 39 taste-sensitive neurons in the nucleus tractus solitarii of anesthetized mice during oral delivery of tastants adjusted to innocuous cool (16 and 18°C), room (22°C, baseline), and warm (30 and 37°C) oral temperatures. Stimuli included (in mM) 100 sucrose, 30 NaCl, 3 HCl, 3 quinine, an umami mixture, and water. Although cooled water excited few cells, water warmed to 30 and 37°C significantly excited 33% and 64% of neurons, respectively. Warmth induced responses of comparable magnitude to room temperature tastants. Furthermore, warming taste solutions influenced the distribution of gustatory responses among neurons and increased (P < 0.05) neuronal breadth of tuning across taste qualities. The influence of warmth on response magnitude was stimulus specific. Across neurons, warming facilitated responses to sucrose and umami in a superadditive manner, as these responses exceeded (P < 0.05) the arithmetic sum of activity to warming alone and the taste stimulus tested at room temperature. Superadditive increases (P < 0.05) in responding were also noted in some cells for warmed HCl. Yet warming induced only simple additive or subtractive effects on responses to quinine and NaCl. Data show temperature is a parameter of gustatory processing, like taste quality and concentration, in medullary circuits for taste.

Temperature systematically modifies neural activity for sweet taste

“…Our discussion centers on how temperature operates as a parameter of the magnitude and timing of gustatory activity to sucrose. Moreover, the present data further build on the postulate that oral somatosensory cues importantly guide and modulate the operation of neurobiological substrates for taste (e.g., Green 2002;Green and Nachtigal 2012;Wilson and Lemon 2013).…”

“…The presentation of taste solutions was carried out with a custom apparatus, as described previously (Lemon and Margolskee 2009;Wilson and Lemon 2013). Briefly, stimuli were loaded one at a time into a funnel and tubing system suspended above the preparation and drawn into the mouse oral cavity by gravity.…”

“…Temperature values were selected to provide nonnoxious cooling and warming (cf. Wilson and Lemon 2013). The actual mean temperatures measured within condition, as sampled during the last 3 s of stimulus delivery across all sucrose trials, were (ϮSD; in°C/ms) 17.8 Ϯ 1.3, 21.8 Ϯ 1.2, 30.1 Ϯ 1.4, and 37.1 Ϯ 1.2.…”

“…The NTS was located in mice as described previously (Lemon and Margolskee 2009;Wilson et al 2012;Wilson and Lemon 2013). When searching for single units, the electrode was lowered into the nucleus and neural activity to oral delivery of 0.5 M sucrose was monitored.…”

“…A recent electrophysiology study on gustatory neurons in the mouse nucleus of the solitary tract (NTS) showed that warming taste solutions increased responses to 0.1 M sucrose in a supralinear manner and that cooling taste solutions largely inhibited sucrose activity (Wilson and Lemon 2013). These results suggested that temperature modified the gain of the neural response to sucrose.…”