Korean J Physiol Pharmacol.  2021 Nov;25(6):603-611. 10.4196/kjpp.2021.25.6.603.

Influences of ethanol and temperature on sucrose-evoked response of gustatory neurons in the hamster solitary nucleus

Affiliations
  • 1Department of Anatomy, School of Medicine, Southern Illinois University, Carbondale, IL 62901, USA
  • 2Department of Physiology and Neuroscience, College of Dentistry and Research Institute of Oral Science, Gangneung-Wonju National University, Gangneung 25457, Korea

Abstract

Taste-responsive neurons in the nucleus of the solitary tract (NST), the first gustatory nucleus, often respond to thermal or mechanical stimulation. Alcohol, not a typical taste modality, is a rewarding stimulus. In this study, we aimed to investigate the effects of ethanol (EtOH) and/or temperature as stimuli to the tongue on the activity of taste-responsive neurons in hamster NST. In the first set of experiments, we recorded the activity of 113 gustatory NST neurons in urethane-anesthetized hamsters and evaluated responses to four basic taste stimuli, 25% EtOH, and 40°C and 4°C distilled water (dH2O). Sixty cells responded to 25% EtOH, with most of them also being sucrose sensitive. The response to 25% EtOH was significantly correlated with the sucrose-evoked response. A significant correlation was also observed between sucrose- and 40°C dH2O- and between 25% EtOH- and 40°C dH2O-evoked firings. In a subset of the cells, we evaluated neuronal activities in response to a series of EtOH concentrations, alone and in combination with 32 mM sucrose (EtOH/Suc) at room temperature (RT, 22°C–23°C), 40°C, and 4°C. Neuronal responses to EtOH at RT and 40°C increased as the concentrations increased. The firing rates to EtOH/Suc were greater than those to EtOH or sucrose alone. The responses were enhanced when solutions were applied at 40°C but diminished at 4°C. In summary, EtOH activates most sucrose-responsive NST gustatory cells, and the concomitant presence of sucrose or warm temperatures enhance this response. Our findings may contribute to elucidate the neural mechanisms underlying appetitive alcohol consumption.

Keyword

Electrophysiology; Ethanol; In vivo; Solitary nucleus; Sucrose

Figure

  • Fig. 1 Stimulus-evoked firings (impulses/s) of 113 nucleus of the solitary tract (NST) neurons, in response to four basic taste stimuli, 25% ethanol (EtOH), and distilled water (dH2O) at 40°C and 4°C in order from top to bottom panels. The last panel shows the mean number of spikes during 5 sec of dH2O at a room temperature (baseline activity) before taste stimulus. Net taste responses, unaffected by somatosensory or thermal aspects of the test solutions, were calculated as a mean number of spikes during the first 5 sec of each taste stimulus minus the baseline activity of same neuron. Each neuron was classified according to the taste stimulus that was the most effective in causing it to respond (best stimulus) and cells are arranged along the abscissa according to their best stimulus, with cells 1–33 being sucrose-best (Sb: red), 34–51 NaCl-best (Nb: blue), 52–54 citric acid-best (Cb: yellow), and 55–60 QHCl-best (Qb: green) in EtOH-responsive groups (A). Similarly, 53 cells are arranged: 3 Sb, 16 Nb, 15 Cb, and 19 Qb are arranged in EtOH-non-responsive groups (B). Within each best-stimulus group, cells are arranged according to the magnitude of the response to their best stimulus. The response profile for any one cell in the figure can be read from top to bottom.

  • Fig. 2 Comparison of the mean firing rate (× SE) of nucleus of the solitary tract (NST) neurons in response to four taste stimuli, 25% ethanol (EtOH), and distilled water (dH2O) at 40°C (40) and 4°C (4) between EtOH-responsive and EtOH-non-responsive neurons. The last bars on the right of the figure indicate the baseline activities at room temperature. The solid bars indicate mean responses of EtOH-responsive neurons and open bars represent those of EtOH-non-responsive cells. For sucrose (S), 25% EtOH (E), and 40°C dH2O stimulus, net responses in EtOH-responsive neurons were significantly larger than those in EtOH-non-responsive cells (*p < 0.001, t-test). In comparison, citric acid (C)-, and QHCl (Q)-evoked firings were significantly larger in EtOH-non-responsive group (**p < 0.005, t-test). There were no differences across taste stimuli between EtOH-responsive and EtOH-non-responsive cells for NaCl (N) and 4°C dH2O stimuli.

  • Fig. 3 Response profiles for various stimuli of a typical QHCl-best neuron (NST43Q) belonging to ethanol (EtOH)-non-responsive cells. Neuronal firings for each tastant during the 10-sec stimulus are shown in filled bars, and the pre- and post-rinse periods with distilled water (dH2O) for 5 sec are shown in open bars. The stimuli applied to the anterior tongue were sucrose (S), NaCl (N), citric acid (C), QHCl (Q), 3, 5, 10, 15, 25, and 40% of EtOH, and dH2O at 40°C and 4°C. This neuron only responded to 32 mM QHCl as a taste stimulation.

  • Fig. 4 A representative peri-stimulus time histogram (1-ms bins) of the impulses in a sucrose-best neuron (NST95S) in ethanol (EtOH)-responsive cells. Taste stimuli are a series of EtOH (A) and a mixture of EtOH and 32 mM sucrose (EtOH/Suc) (B). Evoked firings were increased in a dose-dependent manner for the stimulations with EtOH or EtOH/Suc. The stimulation with EtOH/Suc produced larger responses than with EtOH alone. (C) Mean responses (± SE) of 15 nucleus of the solitary tract (NST) gustatory neurons to a series of 6 concentrations of EtOH (open circle) and EtOH/Suc (solid circle) stimulations at room temperature. Stimulus-evoked firings were increased in a dose-dependent manner. Responses to EtOH/Suc stimulation were greater than those to EtOH alone.

  • Fig. 5 Mean responses (× SE) of 3 nucleus of the solitary tract (NST) gustatory neurons to a series of 6 concentrations of ethanol (EtOH) (open symbol) and EtOH/Suc (solid symbol) at 40°C (circle) and 4°C (rectangle). Neuronal responses to serial concentrations of EtOH alone or with sucrose stimulation at 40°C were similar to those shown at room temperature. However, this trend at 40°C was not shown at 4°C.


Reference

1. Lundy RF Jr. Paxinos G, editor. 2004. Gustatory system. The rat nervous system. 3rd ed. Elsevier Academic Press;Cambridge: p. 891–921. DOI: 10.1016/B978-012547638-6/50029-8.
Article
2. Smith DV, Margolskee RF. 2001; Making sense of taste. Sci Am. 284:32–39. DOI: 10.1038/scientificamerican0301-32. PMID: 11234504.
Article
3. Rolls ET. 2004; Smell, taste, texture, and temperature multimodal representations in the brain, and their relevance to the control of appetite. Nutr Rev. 62(11 Pt 2):S193–S204. discussion S224–S241. DOI: 10.1301/nr.2004.nov.S193-S204. PMID: 15630935.
Article
4. Rogers PJ, Hardman CA. 2015; Food reward. What it is and how to measure it. Appetite. 90:1–15. DOI: 10.1016/j.appet.2015.02.032. PMID: 25728883.
Article
5. Rolls ET. 1999. The brain and emotion. Oxford University Press;New York:
6. Saper CB, Chou TC, Elmquist JK. 2002; The need to feed: homeostatic and hedonic control of eating. Neuron. 36:199–211. DOI: 10.1016/S0896-6273(02)00969-8. PMID: 12383777.
7. Giza BK, Deems RO, Vanderweele DA, Scott TR. 1993; Pancreatic glucagon suppresses gustatory responsiveness to glucose. Am J Physiol. 265(6 Pt 2):R1231–R1237. DOI: 10.1152/ajpregu.1993.265.6.R1231. PMID: 8285262.
Article
8. Giza BK, Scott TR. 1983; Blood glucose selectively affects taste-evoked activity in rat nucleus tractus solitarius. Physiol Behav. 31:643–650. PMID: 6665054.
9. Giza BK, Scott TR. 1987; Intravenous insulin infusions in rats decrease gustatory-evoked responses to sugars. Am J Physiol. 252(5 Pt 2):R994–R1002. DOI: 10.1152/ajpregu.1987.252.5.R994. PMID: 3555122.
Article
10. Whitehead MC. 1988; Neuronal architecture of the nucleus of the solitary tract in the hamster. J Comp Neurol. 276:547–572. DOI: 10.1002/cne.902760409. PMID: 2461969.
Article
11. Chang FC, Scott TR. 1984; Conditioned taste aversions modify neural responses in the rat nucleus tractus solitarius. J Neurosci. 4:1850–1862. DOI: 10.1523/JNEUROSCI.04-07-01850.1984. PMID: 6737042. PMCID: PMC6564891.
Article
12. Giza BK, Ackroff K, McCaughey SA, Sclafani A, Scott TR. 1997; Preference conditioning alters taste responses in the nucleus of the solitary tract of the rat. Am J Physiol. 273:R1230–R1240. DOI: 10.1152/ajpregu.1997.273.4.R1230. PMID: 9362285.
13. Brasser SM, Castro N, Feretic B. 2015; Alcohol sensory processing and its relevance for ingestion. Physiol Behav. 148:65–70. DOI: 10.1016/j.physbeh.2014.09.004. PMID: 25304192. PMCID: PMC4388769.
Article
14. Bachmanov AA, Kiefer SW, Molina JC, Tordoff MG, Duffy VB, Bartoshuk LM, Mennella JA. 2003; Chemosensory factors influencing alcohol perception, preferences, and consumption. Alcohol Clin Exp Res. 27:220–231. DOI: 10.1097/01.ALC.0000051021.99641.19. PMID: 12605071. PMCID: PMC1940064.
Article
15. Mattes RD, DiMeglio D. 2001; Ethanol perception and ingestion. Physiol Behav. 72:217–229. DOI: 10.1016/S0031-9384(00)00397-8. PMID: 11240000.
Article
16. Kiefer SW, Morrow NS, Metzler CW. 1988; Alcohol aversion generalization in rats: specific disruption of taste and odor cues with gustatory neocortex or olfactory bulb ablations. Behav Neurosci. 102:733–739. DOI: 10.1037/0735-7044.102.5.733. PMID: 2848538.
Article
17. Kampov-Polevoy AB, Garbutt JC, Janowsky DS. 1999; Association between preference for sweets and excessive alcohol intake: a review of animal and human studies. Alcohol Alcohol. 34:386–395. DOI: 10.1093/alcalc/34.3.386. PMID: 10414615.
Article
18. Hellekant G, Danilova V, Roberts T, Ninomiya Y. 1997; The taste of ethanol in a primate model: I. Chorda tympani nerve response in Macaca mulatta. Alcohol. 14:473–484. DOI: 10.1016/S0741-8329(96)00215-7. PMID: 9305463.
Article
19. Sako N, Yamamoto T. 1999; Electrophysiological and behavioral studies on taste effectiveness of alcohols in rats. Am J Physiol. 276:R388–R396. DOI: 10.1152/ajpregu.1999.276.2.R388. PMID: 9950916.
Article
20. Lemon CH, Brasser SM, Smith DV. 2004; Alcohol activates a sucrose-responsive gustatory neural pathway. J Neurophysiol. 92:536–544. DOI: 10.1152/jn.00097.2004. PMID: 14985409.
Article
21. 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. DOI: 10.1152/jn.00580.2011. PMID: 21918002. PMCID: PMC3234093.
Article
22. Cho YK. 2007; Relationship between alcohol and sucrose/thermal stimulation in pontine taste neurons in the hamster. Exp Neurobiol. 16:79–87.
23. Cruz A, Green BG. 2000; Thermal stimulation of taste. Nature. 403:889–892. DOI: 10.1038/35002581. PMID: 10706285.
Article
24. Bartoshuk LM, Rennert K, Rodin J, Stevens JC. 1982; Effects of temperature on the perceived sweetness of sucrose. Physiol Behav. 28:905–910. DOI: 10.1016/0031-9384(82)90212-8. PMID: 7100291.
Article
25. Green BG, Frankmann SP. 1988; The effect of cooling on the perception of carbohydrate and intensive sweeteners. Physiol Behav. 43:515–519. DOI: 10.1016/0031-9384(88)90127-8. PMID: 3194473.
Article
26. Cho YK, Li CS, Smith DV. 2002; Gustatory projections from the nucleus of the solitary tract to the parabrachial nuclei in the hamster. Chem Senses. 27:81–90. DOI: 10.1093/chemse/27.1.81. PMID: 11751472.
Article
27. Cho YK, Li CS, Smith DV. 2002; Taste responses of neurons of the hamster solitary nucleus are enhanced by lateral hypothalamic stimulation. J Neurophysiol. 87:1981–1992. DOI: 10.1152/jn.00765.2001. PMID: 11929917.
Article
28. Li CS, Lu DP, Cho YK. 2015; Descending projections from the nucleus accumbens shell excite activity of taste-responsive neurons in the nucleus of the solitary tract in the hamster. J Neurophysiol. 113:3778–3786. DOI: 10.1152/jn.00362.2014. PMID: 25744880. PMCID: PMC4468968.
Article
29. Duncan HJ, Smith DV. 1992; Concentration-response functions for thirty chemical stimuli in the hamster solitary nucleus. Chem Senses. 17:616.
30. Smith DV, Travers JB. 1979; A metric for the breadth of tuning of gustatory neurons. Chem Senses. 4:215–229. DOI: 10.1093/chemse/4.3.215.
Article
31. McPheeters M, Hettinger TP, Nuding SC, Savoy LD, Whitehead MC, Frank ME. 1990; Taste-responsive neurons and their locations in the solitary nucleus of the hamster. Neuroscience. 34:745–758. DOI: 10.1016/0306-4522(90)90179-8. PMID: 2352650.
Article
32. Di Lorenzo PM, Kiefer SW, Rice AG, Garcia J. 1986; Neural and behavioral responsivity to ethyl alcohol as a tastant. Alcohol. 3:55–61. DOI: 10.1016/0741-8329(86)90071-6. PMID: 3964438.
Article
33. Danilova V, Hellekant G. 2000; The taste of ethanol in a primate model. II. Glossopharyngeal nerve response in Macaca mulatta. Alcohol. 21:259–269. DOI: 10.1016/S0741-8329(00)00094-X. PMID: 11091030.
34. Hellekant G. 1965; Electrophysiological investigation of the gustatory effect of ethyl alcohol. II. A single fibre analysis in the cat. Acta Physiol Scand. 64:398–406. DOI: 10.1111/j.1748-1716.1965.tb04197.x. PMID: 5853033.
Article
35. Lemon CH, Imoto T, Smith DV. 2003; Differential gurmarin suppression of sweet taste responses in rat solitary nucleus neurons. J Neurophysiol. 90:911–923. DOI: 10.1152/jn.00215.2003. PMID: 12702710.
36. Kampov-Polevoy AB, Kasheffskaya OP, Sinclair JD. 1990; Initial acceptance of ethanol: gustatory factors and patterns of alcohol drinking. Alcohol. 7:83–85. DOI: 10.1016/0741-8329(90)90065-K. PMID: 2328091.
Article
37. Kampov-Polevoy AB, Overstreet DH, Rezvani AH, Janowsky DS. 1995; Saccharin-induced increase in daily fluid intake as a predictor of voluntary alcohol intake in alcohol-preferring rats. Physiol Behav. 57:791–795. DOI: 10.1016/0031-9384(94)00389-0. PMID: 7777619.
Article
38. Berridge KC. 2003; Pleasures of the brain. Brain Cogn. 52:106–128. DOI: 10.1016/S0278-2626(03)00014-9. PMID: 12812810.
Article
39. Levine AS, Kotz CM, Gosnell BA. 2003; Sugars: hedonic aspects, neuroregulation, and energy balance. Am J Clin Nutr. 78:834S–842S. DOI: 10.1093/ajcn/78.4.834S. PMID: 14522747.
Article
40. 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. DOI: 10.1152/ajpregu.00282.2003. PMID: 12933362.
Article
41. Norgren R, Hajnal A, Mungarndee SS. 2006; Gustatory reward and the nucleus accumbens. Physiol Behav. 89:531–535. DOI: 10.1016/j.physbeh.2006.05.024. PMID: 16822531. PMCID: PMC3114426.
Article
42. Smith GP. 2004; Accumbens dopamine mediates the rewarding effect of orosensory stimulation by sucrose. Appetite. 43:11–13. DOI: 10.1016/j.appet.2004.02.006. PMID: 15262012.
Article
43. Weiss F, Lorang MT, Bloom FE, Koob GF. 1993; Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J Pharmacol Exp Ther. 267:250–258. PMID: 8229752.
44. Zhang M, Kelley AE. 2002; Intake of saccharin, salt, and ethanol solutions is increased by infusion of a mu opioid agonist into the nucleus accumbens. Psychopharmacology (Berl). 159:415–423. DOI: 10.1007/s00213-001-0932-y. PMID: 11823894.
Article
45. Loriaux AL, Roitman JD, Roitman MF. 2011; Nucleus accumbens shell, but not core, tracks motivational value of salt. J Neurophysiol. 106:1537–1544. DOI: 10.1152/jn.00153.2011. PMID: 21697439. PMCID: PMC3174809.
Article
46. Li CS, Chung S, Lu DP, Cho YK. 2012; Descending projections from the nucleus accumbens shell suppress activity of taste-responsive neurons in the hamster parabrachial nuclei. J Neurophysiol. 108:1288–1298. DOI: 10.1152/jn.00121.2012. PMID: 22696536.
Article
47. Hayama T, Ito S, Ogawa H. 1985; Responses of solitary tract nucleus neurons to taste and mechanical stimulations of the oral cavity in decerebrate rats. Exp Brain Res. 60:235–242. DOI: 10.1007/BF00235918. PMID: 4054268.
Article
48. Ogawa H, Hayama T, Yamashita Y. 1988; Thermal sensitivity of neurons in a rostral part of the rat solitary tract nucleus. Brain Res. 454:321–331. DOI: 10.1016/0006-8993(88)90833-5. PMID: 3409015.
Article
49. Ogawa H, Imoto T, Hayama T. 1984; Responsiveness of solitario-parabrachial relay neurons to taste and mechanical stimulation applied to the oral cavity in rats. Exp Brain Res. 54:349–358. DOI: 10.1007/BF00236236. PMID: 6723854.
Article
50. Travers SP, Norgren R. 1995; Organization of orosensory responses in the nucleus of the solitary tract of rat. J Neurophysiol. 73:2144–2162. DOI: 10.1152/jn.1995.73.6.2144. PMID: 7666129.
Article
51. Green BG, George P. 2004; 'Thermal taste' predicts higher responsiveness to chemical taste and flavor. Chem Senses. 2:617–628. DOI: 10.1093/chemse/bjh065. PMID: 15337686.
Article
52. Ogawa H, Sato M, Yamashita S. 1968; Multiple sensitivity of chordat typani fibres of the rat and hamster to gustatory and thermal stimuli. J Physiol. 199:223–240. DOI: 10.1113/jphysiol.1968.sp008650. PMID: 5684036. PMCID: PMC1365355.
53. Lundy RF Jr, Contreras RJ. 1997; Temperature and amiloride alter taste nerve responses to Na+, K+, and NH4+salts in rats. Brain Res. 744:309–317. DOI: 10.1016/S0006-8993(96)01118-3.
54. Li J, Lemon CH. 2015; Influence of stimulus and oral adaptation temperature on gustatory responses in central taste-sensitive neurons. J Neurophysiol. 113:2700–2712. DOI: 10.1152/jn.00736.2014. PMID: 25673737. PMCID: PMC4416558.
Article
55. Wilson DM, Lemon CH. 2014; Temperature systematically modifies neural activity for sweet taste. J Neurophysiol. 112:1667–1677. DOI: 10.1152/jn.00368.2014. PMID: 24966301. PMCID: PMC4157175.
Article
56. 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. DOI: 10.1152/jn.00793.2005. PMID: 16267112.
Article
57. Cho YK, Smith ME, Norgren R. 2004; Low-dose furosemide modulates taste responses in the nucleus of the solitary tract of the rat. Am J Physiol Regul Integr Comp Physiol. 287:R706–R714. DOI: 10.1152/ajpregu.00090.2004. PMID: 15155275.
Article
58. Cho YK, Mao L, Li CS. 2008; Modulation of solitary taste neurons by electrical stimulation of the ventroposteromedial nucleus of the thalamus in the hamster. Brain Res. 1221:67–79. DOI: 10.1016/j.brainres.2008.05.006. PMID: 18565498.
Article
59. Li CS, Cho YK, Smith DV. 2002; Taste responses of neurons in the hamster solitary nucleus are modulated by the central nucleus of the amygdala. J Neurophysiol. 88:2979–2992. DOI: 10.1152/jn.00239.2002. PMID: 12466423.
Article
Full Text Links
  • KJPP
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr