Abstract
Introduction
This mini-review discusses some of the parallels between rodent neurophysiological and human psychophysical data concerning temperature effects on sweet taste.
Methods and Purpose
“Sweet” is an innately rewarding taste sensation that is associated in part with foods that contain calories in the form of sugars. Humans and other mammals show unconditioned preference for select sweet stimuli. Such preference is poised to influence diet selection and, in turn, nutritional status, which underscores the importance of delineating the physiological mechanisms for sweet taste with respect to their influence on human health. Advances in our knowledge of the biology of sweet taste in humans have arisen in part through studies on mechanisms of gustatory processing in rodent models. Along this line, recent work has revealed there are operational parallels in neural systems for sweet taste between mice and humans, as indexed by similarities in the effects of temperature on central neurophysiological and psychophysical responses to sucrose in these species. Such association strengthens the postulate that rodents can serve as effective models of particular mechanisms of appetitive taste processing. Data supporting this link are discussed here, as are rodent and human data that shed light on relationships between mechanisms for sweet taste and ingestive disorders, such as alcohol abuse.
Results and Conclusions
Rodent models have utility for understanding mechanisms of taste processing that may pertain to human flavor perception. Importantly, there are limitations to generalizing data from rodents, albeit parallels across species do exist.
Similar content being viewed by others
References
Avena NM, Rada P, Moise N, Hoebel BG (2006) Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 139:813–820
Bachmanov AA, Reed DR, Ninomiya Y, Inoue M, Tordoff MG, Price RA, Beauchamp GK (1997) Sucrose consumption in mice: major influence of two genetic loci affecting peripheral sensory responses. Mamm Genome 8:545–548
Bachmanov AA et al (2001a) Positional cloning of the mouse saccharin preference (Sac) locus. Chem Senses 26:925–933
Bachmanov AA, Tordoff MG, Beauchamp GK (2001b) Sweetener preference of C57BL/6ByJ and 129P3/J mice. Chem Senses 26:905–913
Bachmanov AA, Reed DR, Li X, Li S, Beauchamp GK, Tordoff MG (2002) Voluntary ethanol consumption by mice: genome-wide analysis of quantitative trait loci and their interactions in a C57BL/6ByJ x 129P3/JF2 intercross. Genome Res 12:1257–1268
Bartoshuk LM, Rennert K, Rodin J, Stevens JC (1982) Effects of temperature on the perceived sweetness of sucrose. Physiol Behav 28:905–910
Belknap JK, Crabbe JC, Young ER (1993) Voluntary consumption of ethanol in 15 inbred mouse strains. Psychopharmacology (Berl) 112:503–510
Bertino M, Beauchamp GK, Engelman K (1986) Increasing dietary salt alters salt taste preference. Physiol Behav 38:203–213
Blednov YA, Walker D, Martinez M, Levine M, Damak S, Margolskee RF (2008) Perception of sweet taste is important for voluntary alcohol consumption in mice. Genes Brain Behav 7:1–13
Blizard DA, Kotlus B, Frank ME (1999) Quantitative trait loci associated with short-term intake of sucrose, saccharin and quinine solutions in laboratory mice. Chem Senses 24:373–385
Brasser SM, Norman MB, Lemon CH (2010) T1r3 taste receptor involvement in gustatory neural responses to ethanol and oral ethanol preference. Physiol Genomics 41:232–243
Brasser SM, Silbaugh BC, Ketchum MJ, Olney JJ, Lemon CH (2012) Chemosensory responsiveness to ethanol and its individual sensory components in alcohol-preferring, alcohol-nonpreferring and genetically heterogeneous rats. Addict Biol 17:423–436
Brasser SM, Castro N, Feretic B (2014) Alcohol sensory processing and its relevance for ingestion. Physiol Behav. doi:10.1016/j.physbeh.2014.09.004
Breza JM, Curtis KS, Contreras RJ (2006) Temperature modulates taste responsiveness and stimulates gustatory neurons in the rat geniculate ganglion. J Neurophysiol 95:674–685
Calvino AM (1986) Perception of sweetness: the effects of concentration and temperature. Physiol Behav 36:1021–1028
Crook C (1978) Taste perception in the newborn infant. Infant Behav Dev 1:52–69
Damak S et al (2003) Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301:850–853
Doyon WM, York JL, Diaz LM, Samson HH, Czachowski CL, Gonzales RA (2003) Dopamine activity in the nucleus accumbens during consummatory phases of oral ethanol self-administration. Alcohol Clin Exp Res 27:1573–1582
Dudley R (2000) Evolutionary origins of human alcoholism in primate frugivory. Q Rev Biol 75:3–15
Feigin MB, Sclafani A, Sunday SR (1987) Species differences in polysaccharide and sugar taste preferences. Neurosci Biobehav Rev 11:231–240
Fuller JL (1974) Single-locus control of saccharin preference in mice. J Hered 65:33–36
Fushan AA, Simons CT, Slack JP, Manichaikul A, Drayna D (2009) Allelic polymorphism within the TAS1R3 promoter is associated with human taste sensitivity to sucrose. Curr Biol 19:1288–1293
Green BG, Frankmann SP (1987) The effect of cooling the tongue on the perceived intensity of taste. Chem Senses 12:609–619
Green BG, Frankmann SP (1988) The effect of cooling on the perception of carbohydrate and intensive sweeteners. Physiol Behav 43:515–519
Green BG, Nachtigal D (2012) Somatosensory factors in taste perception: effects of active tasting and solution temperature. Physiol Behav 107:488–495
Hajnal A, Smith GP, Norgren R (2004) Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 286:R31–R37
Jiang P et al (2014) The bamboo-eating giant panda (Ailuropoda melanoleuca) has a sweet tooth: behavioral and molecular responses to compounds that taste sweet to humans. PLoS One 9:e93043
Kampov-Polevoy A, Garbutt JC, Janowsky D (1997) Evidence of preference for a high-concentration sucrose solution in alcoholic men. Am J Psychiatry 154:269–270
Kampov-Polevoy AB, Garbutt JC, Davis CE, Janowsky DS (1998) Preference for higher sugar concentrations and Tridimensional Personality Questionnaire scores in alcoholic and nonalcoholic men. Alcohol Clin Exp Res 22:610–614
Kampov-Polevoy AB, Garbutt JC, Khalitov E (2003a) Family history of alcoholism and response to sweets. Alcohol Clin Exp Res 27:1743–1749
Kampov-Polevoy AB et al (2003b) Association between sweet preference and paternal history of alcoholism in psychiatric and substance abuse patients. Alcohol Clin Exp Res 27:1929–1936
Kareken DA, Dzemidzic M, Oberlin BG, Eiler WJ 2nd (2013) A preliminary study of the human brain response to oral sucrose and its association with recent drinking. Alcohol Clin Exp Res 37:2058–2065
Kawai K, Sugimoto K, Nakashima K, Miura H, Ninomiya Y (2000) Leptin as a modulator of sweet taste sensitivities in mice. Proc Natl Acad Sci U S A 97:11044–11049
Kitagawa M, Kusakabe Y, Miura H, Ninomiya Y, Hino A (2001) Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun 283:236–242
LaMotte RH, Campbell JN (1978) Comparison of responses of warm and nociceptive C-fiber afferents in monkey with human judgments of thermal pain. J Neurophysiol 41:509–528
Lemon CH, Brasser SM, Smith DV (2004) Alcohol activates a sucrose-responsive gustatory neural pathway. J Neurophysiol 92:536–544
Lemon CH, Wilson DM, Brasser SM (2011) Differential neural representation of oral ethanol by central taste-sensitive neurons in ethanol-preferring and genetically heterogeneous rats. J Neurophysiol 106:3145–3156
Liu B, Ha M, Meng XY, Khaleduzzaman M, Zhang Z, Li X, Cui M (2012) Functional characterization of the heterodimeric sweet taste receptor T1R2 and T1R3 from a New World monkey species (squirrel monkey) and its response to sweet-tasting proteins. Biochem Biophys Res Commun 427:431–437
Lu B, Breza JM, Nikonov AA, Paedae AB, Contreras RJ (2012) Leptin increases temperature-dependent chorda tympani nerve responses to sucrose in mice. Physiol Behav 107:533–539
Lush IE (1989) The genetics of tasting in mice. VI. Saccharin, acesulfame, dulcin and sucrose. Genet Res 53:95–99
Lush IE, Hornigold N, King P, Stoye JP (1995) The genetics of tasting in mice. VII. Glycine revisited, and the chromosomal location of Sac and Soa. Genet Res 66:167–174
Max M et al (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28:58–63
Mennella JA, Lukasewycz LD, Griffith JW, Beauchamp GK (2011) Evaluation of the Monell forced-choice, paired-comparison tracking procedure for determining sweet taste preferences across the lifespan. Chem Senses 36:345–355
Mennella JA, Finkbeiner S, Reed DR (2012) The proof is in the pudding: children prefer lower fat but higher sugar than do mothers. Int J Obes 36:1285–1291
Montmayeur JP, Liberles SD, Matsunami H, Buck LB (2001) A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 4:492–498
Nakamura Y et al (2008) Diurnal variation of human sweet taste recognition thresholds is correlated with plasma leptin levels. Diabetes 57:2661–2665
Newsome WT, Britten KH, Movshon JA (1989) Neuronal correlates of a perceptual decision. Nature 341:52–54
Nicola SM (2010) The flexible approach hypothesis: unification of effort and cue-responding hypotheses for the role of nucleus accumbens dopamine in the activation of reward-seeking behavior. J Neurosci 30:16585–16600
Nowlis GH, Kessen W (1976) Human newborns differentiate differing concentrations of sucrose and glucose. Science 191:865–866
Perez CA et al (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169–1176
Reed DR et al (2004) Polymorphisms in the taste receptor gene (Tas1r3) region are associated with saccharin preference in 30 mouse strains. J Neurosci 24:938–946
Sainz E, Korley JN, Battey JF, Sullivan SL (2001) Identification of a novel member of the T1R family of putative taste receptors. J Neurochem 77:896–903
Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology (Berl) 191:461–482
Samuelsen CL, Gardner MP, Fontanini A (2012) Effects of cue-triggered expectation on cortical processing of taste. Neuron 74:410–422
Sclafani A, Abrams M (1986) Rats show only a weak preference for the artificial sweetener aspartame. Physiol Behav 37:253–256
Sclafani A, Clare RA (2004) Female rats show a bimodal preference response to the artificial sweetener sucralose. Chem Senses 29:523–528
Small DM, Green BG (2012) A proposed model of a flavor modality. In: Murray MM, Wallace MT (eds) The neural bases of multisensory processes. Frontiers in Neuroscience, Boca Raton
Small DM, Jones-Gotman M, Dagher A (2003) Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage 19:1709–1715
Smith DV, Ye MK, Li CS (2005) Medullary taste responses are modulated by the bed nucleus of the stria terminalis. Chem Senses 30:421–434
Steiner JE (1979) Human facial expressions in response to taste and smell stimulation. Adv Child Dev Behav 13:257–295
Talavera K et al (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–1025
Treesukosol Y, Spector AC (2012) Orosensory detection of sucrose, maltose, and glucose is severely impaired in mice lacking T1R2 or T1R3, but polycose sensitivity remains relatively normal. Am J Physiol Regul Integr Comp Physiol 303:R218–R235
Wilson DM, Lemon CH (2013) Modulation of central gustatory coding by temperature. J Neurophysiol 110:1117–1129
Wilson DM, Lemon CH (2014) Temperature systematically modifies neural activity for sweet taste. J Neurophysiol 112:1667–1677
Yamashita S, Sato M (1965) The effects of temperature on gustatory response of rats. J Cell Compar Physl 66:1–18
Zhang Y et al (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301
Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255–266
Compliance with Ethics Requirements
ᅟ
Conflict of Interest
The author declares no conflict of interest.
Funding
This work was supported in part by the National Institutes of Health grant DC-011579 to C.H.L.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lemon, C.H. Perceptual and Neural Responses to Sweet Taste in Humans and Rodents. Chem. Percept. 8, 46–52 (2015). https://doi.org/10.1007/s12078-015-9177-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12078-015-9177-8