Sweet taste and chorda tympani transection alter capsaicin-induced lingual pain perception in adult human subjects

Physiology and Behavior

Volumn 107, Issue 3, 2012, Pages 368-373

  Schobel N ^a,b   Kyereme, J ^a   Minovi, A ^c   Dazert, S ^c   Bartoshuk, L ^d   Hatt, H ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b LEIBNIZ RESEARCH CENTRE FOR WORKING ENVIRONMENT AND HUMAN FACTORS   (Germany)

^c St Elisabeth Hospital Bochum   (Germany)

^d UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

Author keywords

GLMS; Hedonics; Hemiageusia; Oral pain; Pain suppression; Sweet taste

Indexed keywords

CAPSAICIN; QUININE; SUCROSE;

ADULT; ANALGESIA; ARTICLE; BURNING SENSATION; CHORDA TYMPANI; CONTROLLED STUDY; FEMALE; FOOD INTAKE; HUMAN; MALE; MIDDLE EAR SURGERY; MOUTH PAIN; NOCICEPTION; NORMAL HUMAN; PAIN RECEPTOR; PRIORITY JOURNAL; SWEETNESS; TRIGEMINUS NEURALGIA;

EID: 84867201550     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2012.09.004     Document Type: Article

References (65)

1. Anseloni V, Weng H, Terayama R, Letizia D, Davis B, Ren K, et al. Age-dependency of analgesia elicited by intraoral sucrose in acute and persistent pain models. Pain 2002;97:93-103
2. Blass E, Shide D. Some comparisons among the calming and pain-relieving effects of sucrose, glucose, fructose and lactose in infant rats. Chem Senses 1994;19:239-49
3. Shide DJ, Blass EM. Opioid mediation of odor preferences induced by sugar and fat in 6-day-old rats. Physiol Behav 1991;50:961-6
4. Blass E, Shah A. Pain-reducing properties of sucrose in human newborns. Chem Senses 1995;20:29-35
5. Blass E, Hoffmeyer L. Sucrose as an analgesic for newborn infants. Pediatrics 1991;87:215-8
6. Overgaard C, Knudsen A. Pain-relieving effect of sucrose in newborns during heel prick. Biol Neonate 1999;75:279-84
7. Taddio A, Shah V, Katz J. Reduced infant response to a routine care procedure after sucrose analgesia. Pediatrics 2009;123:e425-9
8. Ramenghi L, Evans D, Levene M. "Sucrose analgesia": absorptive mechanism or taste perception? Arch Dis Child Fetal Neonatal Ed 1999;80:F146-7
9. Blass E, Fitzgerald E, Kehoe P. Interactions between sucrose, pain and isolation distress. Pharmacol Biochem Behav 1987;26:483-9
10. Blass E, Fitzgerald E. Milk-induced analgesia and comforting in 10-day-old rats: opioid mediation. Pharmacol Biochem Behav 1988;29:9-13
11. Shide D, Blass E. Opioidlike effects of intraoral infusions of corn oil and polycose on stress reactions in 10-day-old rats. Behav Neurosci 1989;103:1168-75
12. Lewkowski MD, Young SN, Ghosh S, Ditto B. Effects of opioid blockade on the modulation of pain and mood by sweet taste and blood pressure in young adults. Pain 2008;135:75-81
13. Peciña S. Opioid reward 'liking' and 'wanting' in the nucleus accumbens. Physiol Behav 2008;94:675-80
14. Gebhart G. Descending modulation of pain. Neurosci Biobehav Rev 2004;27: 729-37
15. Heinricher M, Tavares I, Leith J, Lumb B. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 2009;60:214-25
16. Anseloni V, Ren K, Dubner R, Ennis M. A brainstem substrate for analgesia elicited by intraoral sucrose. Neuroscience 2005;133:231-43
17. Behbehani M, Park M, Clement M. Interactions between the lateral hypothalamus and the periaqueductal gray. J Neurosci 1988;8:2780-7
18. Behbehani M. Functional characteristics of the midbrain periaqueductal gray. Prog Neurobiol 1995;46:575-605
19. Rizvi T, Ennis M, Behbehani M, Shipley M. Connections between the central nucleus of the amygdala and themidbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 1991;303:121-31
20. Krukoff T, Harris K, Jhamandas J. Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res Bull 1993;30:163-72
21. Hermann D, Luppi P, Peyron C, Hinckel P, Jouvet M. Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars alpha demonstrated by iontophoretic application of choleratoxin (subunit b). J Chem Neuroanat 1997;13:1-21
22. Foo H, Mason P. Sensory suppression during feeding. Proc Natl Acad Sci U S A 2005;102:16865-9
23. Mercer ME, Holder MD. Antinociceptive effects of palatable sweet ingesta on human responsivity to pressure pain. Physiol Behav 1997;61:311-8
24. Lewkowski MD, Ditto B, Roussos M, Young SN. Sweet taste and blood pressure-related analgesia. Pain 2003;106:181-6
25. Pepino M, Mennella J. Sucrose-induced analgesia is related to sweet preferences in children but not adults. Pain 2005;119:210-8
26. Caterina M, Schumacher M, Tominaga M, Rosen T, Levine J, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997;389: 816-24
27. Nasrawi C, Pangborn R. The influence of tastants on oral irritation by capsaicin. J Sens Stud 1988;3:287-94
28. Stevens DA, Lawless HT. Putting out the fire: effects of tastants on oral chemical irritation. Percept Psychophys 1986;39:346-50
29. Sizer F, Harris N. The influence of common food additives and temperature on threshold perception of capsaicin. Chem Senses 1985;10:279-86
30. Knight YE, Goadsby PJ. The periaqueductal grey mattermodulates trigeminovascular input: a role in migraine? Neuroscience 2001;106:793-800
31. Tashiro T, Ruda MA, Satoda T, Matsushima R, Mizuno N. Convergence of serotonin-, enkephalin- and substance P-like immunoreactive afferent fibers onto cat medullary dorsal horn projection neurons: a triple immunocytochemical staining technique combined with the retrograde HRP-tracing method. Brain Res 1989;491:360-5
32. Basbaum A, Fields H. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 1984;7:309-38
33. Meng I, Hu J, Bereiter D. Parabrachial area and nucleus raphe magnus inhibition of corneal units in rostral and caudal portions of trigeminal subnucleus caudalis in the rat. Pain 2000;87:241-51
34. Lambert GA, Hoskin KL, Zagami AS. Cortico-NRM influences on trigeminal neuronal sensation. Cephalalgia 2008;28:640-52
35. Schwartz SR JT, Kveton J, Green BG, Bartoshuk LM. Alteration in lingual somatosensation as a result of transection of the chorda tympani nerve (VII). Chem Senses 1998;23:560
36. Bartoshuk L, Duffy V, Green B, Hoffman H, Ko C, Lucchina L, et al. Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching. Physiol Behav 2004;82:109-14
37. Bartoshuk L, Duffy V, Hayes J, Moskowitz H, Snyder D. Psychophysics of sweet and fat perception in obesity: problems, solutions and new perspectives. Philos Trans R Soc Lond B Biol Sci 2006;361:1137-48
38. Bartoshuk LM, Catalanotto F, Hoffman H, Logan H, Snyder DJ. Taste damage (otitis media, tonsillectomy and head and neck cancer), oral sensations and BMI. Physiol Behav (in press), http://dx.doi.org/10.1016/j.physbeh.2012.06.013
39. Green B. Sensory interactions between capsaicin and temperature in the oral cavity. Chemical Senses; 1986. p. 371-82
40. Nasrawi CW, Pangborn RM. Temporal effectiveness of mouth-rinsing on capsaicin mouth-burn. Physiol Behav 1990;47:617-23
41. Foo H, Mason P. Analgesia accompanying food consumption requires ingestion of hedonic foods. J Neurosci 2009;29:13053-62
42. Foo H, Crabtree K, Thrasher A, Mason P. Eating is a protected behavior even in the face of persistent pain in male rats. Physiol Behav 2009;97:426-9
43. Mason P, Foo H. Food consumption inhibits pain-related behaviors. Ann N Y Acad Sci 2009;1170:399-402
44. Anseloni V, Ren K, Dubner R, Ennis M. Ontogeny of analgesia elicited by nonnutritive suckling in acute and persistent neonatal rat pain models. Pain 2004;109:507-13
45. Wylie L, Gentle M. Feeding-induced tonic pain suppression in the chicken: reversal by naloxone. Physiol Behav 1998;64:27-30
46. Berteretche M, Eloit C, Dumas H, Talmain G, Herman P, Tran Ba Huy P, et al. Taste deficits after middle ear surgery for otosclerosis: taste somatosensory interactions. Eur J Oral Sci 2008;116:394-404
47. Tie K, Fast K, Kveton J, Cohen Z, Duffy V, Green B, et al. Anesthesia of the chorda tympani nerve and effect on oral pain (abstract). Chem Senses 1999;24:609
48. Fillingim R.B., Maixner W., Bunting S, Silva S. Resting blood pressure and thermal pain responses among females: effects on pain unpleasantness but not pain intensity. Int J Psychophysiol 1998;30:313-8
49. Tominaga M, Caterina M, Malmberg A, Rosen T, Gilbert H, Skinner K, et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998;21:531-43
50. Liu L, Simon S. Responses of cultured rat trigeminal ganglion neurons to bitter tastants. Chem Senses 1998;23:125-30
51. Schwartz H, Weddel G. Observations on pathways transmitting sensation of taste. Brain 1938;61:99-115
52. Lewis D, Dandy W. The course of the nerve fibers transmitting sensation of taste. Arch Surg; 1930. p. 249-88
53. Perez R, Fuoco G, Dorion JM, Ho PH, Chen JM. Does the chorda tympani nerve confer general sensation from the tongue? Otolaryngol Head Neck Surg 2006;135:368-73
54. Wang Y, Erickson R, Simon S. Modulation of rat chorda tympani nerve activity by lingual nerve stimulation. J Neurophysiol 1995;73:1468-83
55. Felizardo R, Boucher Y, Braud A, Carstens E, Dauvergne C, Zerari-Mailly F. Trigeminal projections on gustatory neurons of the nucleus of the solitary tract: a double-label strategy using electrical stimulation of the chorda tympani and tracer injection in the lingual nerve. Brain Res 2009;1288:60-8
56. Hsieh ST, Lin WM. Modulation of keratinocyte proliferation by skin innervation. J Invest Dermatol 1999;113:579-86
57. Huang IT, LinWM, Shun CT, Hsieh ST. Influence of cutaneous nerves on keratinocyte proliferation and epidermal thickness in mice. Neuroscience 1999;94:965-73
58. Finger T. Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallate papilla of the rat. Chem Senses 1986;11:135-44
59. Bartoshuk L, Cunningham K, Dabrila G, Duffy V, Etter L, Fast K, et al. From sweets to hot peppers: genetic variation in taste, oral pain, and oral touch. In: Bell G, Watson A, editors. Tastes and Aromas. The Chemical Senses in Science and Industry. Sydney: UNSW Press; 1999. p. 12-22
60. Formaker B, Frank M. Taste function in patients with oral burning. Chem Senses 2000;25:575-81
61. Grushka M, Sessle B, Howley T. Psychophysical evidence of taste dysfunction in burning mouth syndrome. Chem Senses 1986;11:485-98
62. Bartoshuk L, Snyder D, Grushka M, Berger A, Duffy V, Kveton J. Taste damage: previously unsuspected consequences. Chem Senses 2005;30(Suppl. 1):i218-9
63. Grushka M, Bartoshuk L. Burning mouth syndrome and oral dysthesias. Can J Diagn 2000:99-109
64. Grushka M, Sessle B, Howley T. Psychophysical assessment of tactile, pain and thermal sensory functions in burning mouth syndrome. Pain 1987;28:169-84
65. Grushka M, Ching V, Epstein J. Burning mouth syndrome. Adv Otorhinolaryngol 2006;63:278-87