Can age-related CNS taste differences be detected as early as middle age? Evidence from fMRI

Neuroscience

Volumn 232, Issue , 2013, Pages 194-203

  Green, E ^a   Jacobson, A ^a   Haase, L ^a   Murphy, C ^a,b,c  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; FMRI; Gustatory; Reward value; Taste

Indexed keywords

CAFFEINE; SUCROSE; SUGAR INTAKE;

ADULT; AGE; ANTERIOR CINGULATE; ARTICLE; BITTER TASTE; BODY MASS; BRAIN DEPTH STIMULATION; BRAIN REGION; CAUDATE NUCLEUS; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; MIDDLE FRONTAL GYRUS; NEUROIMAGING; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PUTAMEN; SWEETNESS; TASTE DISCRIMINATION; ADMINISTRATION AND DOSAGE; AGING; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; IMAGE PROCESSING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOPHYSICS; STIMULATION; SUGAR INTAKE; TASTE; YOUNG ADULT;

ADULT; AGING; ANALYSIS OF VARIANCE; BODY MASS INDEX; BRAIN; BRAIN MAPPING; CAFFEINE; DIETARY SUCROSE; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PHYSICAL STIMULATION; PSYCHOPHYSICS; TASTE; TASTE PERCEPTION; YOUNG ADULT;

EID: 84892483787     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.11.027     Document Type: Article

References (66)

1. Antonini A., Leenders K., Reist H., Thomann R., Beer H., Locher J. Effect of age on D2 dopamine receptors in normal human brain measured by positron emission tomography and 11C-raclopride. Arch Neurol 1993, 50(5):474-480.
2. Arey L.B., Tremaine M.J., Monzingo F.L. The numerical and topographical relations of taste buds to human circumvallate papillae throughout the life span. Anat Rec 1935, 64:9-25.
3. Arvidson K. Location and variation in number of taste buds in human fungiform papillae. Scand J Dent Res 1979, 87:435-442.
4. Bäckman L., Farde L. The role of dopamine systems in cognitive aging. Cognitive neuroscience of aging: linking cognitive and cerebral aging 2005, 58-84. Oxford University Press, New York. R. Cabeza, L. Nyberg, D.C. Park (Eds.).
5. Balleine B.W., Delgado M.R., Hikosaka O. The role of the dorsal striatum in reward and decision-making. J Neurosci 2007, 27:8161-8165.
6. Bartoshuk L.M., Duffy V.B., Green B.G., Hoffman H.J., Ko C.W., Lucchina L.A., Marks L.E., Snyder D.J., Weiffenbach J.M. Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching. Physiol Behav 2004, 82:109-114.
7. Baumgarter R.N., Heymsfield S.B., Roche A.F. Human body composition and the epidemiology of chronic disease. Obes Res 1995, 3:73-95.
8. Berthoud H.-R., Morrison C. The brain, appetite, and obesity. Annu Rev Psychol 2008, 59:55-92.
9. Boesveldt S., Lindau S.T., McClintock M.K., Hummel T., Lundstrom J.N. Gustatory and olfactory dysfunction in older adults: a national probability study. Rhinology 2011, 49:324-330.
10. Boling W., Reutens D.C., Olivier A. Functional topography of the low postcentral area. J Neurosurg 2002, 97(2):388-395.
11. Bradley R.M., Stedman H.M., Mistretta M. Age does not affect numbers of taste buds and papillae in adult rhesus monkeys. Anat Rec 1985, 212:246-249.
12. Cabanac M. Physiological role of pleasure. Science 1971, 173:1101-1107.
13. Cerf-Ducastel B., Haase L., Murphy C. Effects of magnitude estimation of pleasantness and intensity on fMRI activation to taste. Chemosens Percept 2012, 5:100-109.
14. Cowdrey F.A., Park R.J., Harmer C.J., McCabe C. Increased neural processing of rewarding and aversive stimuli in recovered anorexia nervosa. Biol Psychiatry 2011, 70:736-743.
15. Cox R.W. AFNI: software analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996, 29:162-173.
16. Delgado M.R. Reward-related response in the human striatum. Ann NY Acad Sci 2007, 1104:70-88.
17. Drewnowski A. Energy density, palatability, and satiety: implications for weight control. Nutr Rev 1998, 56:347-353.
18. Faurion A., Kobayakawa T., Cerf-Ducastel B. Cerebral imaging in taste. Chem Senses 2005, 30(Suppl. 1):i230-i231.
19. Felsted J.A., Xueying R., Chouinard-Decorte F., Small D. Genetically determined differences in brain response to a primary food reward. J Neurosci 2010, 30:2429-2432.
20. Folsom A.R., Kushi L.H., Anderson K.E., Mink P.J., Olsen J.E., Hong C.P., Sellers T.A., Lazovich D., Prineas R.J. Associations of general and abdominal obesity with multiple health outcomes in older women. Arch Intern Med 2000, 160:2117-2128.
21. Gilmore M.M., Murphy C. Aging is associated with increased Weber ratios for caffeine, but not for sucrose. Percept Psychophys 1989, 46:555-559.
22. Green B.G., Dalton P., Cowart B., Shaffer G., Rankin K., Higgins J. Evaluating the "labeled magnitude scale" for measuring sensations of taste and smell. Chem Senses 1996, 21:323-334.
23. Green B.G., Shaffer G.S., Gilmore M.M. Derivation and evaluation of a semantic scale of oral sensation magnitude with apparent ratio properties. Chem Senses 1993, 18:683-702.
24. Green E., Jacobson A., Haase L., Murphy C. Reduced nucleus accumbens and caudate nucleus activation to a pleasant taste is associated with obesity in older adults. Brain Res 2011, 1386:109-117.
25. Green E., Murphy C. Altered processing of sweet taste in the brain of diet soda drinkers. Physiol Behav 2012, 107(4):560-567.
26. Haase L., Cerf-Ducastel B., Buracas G., Murphy C. On-line psychophysical data acquisition and event-related fMRI protocol optimized for the investigation of brain activation in response to gustatory stimuli. J Neurosci Methods 2007, 159:98-107.
27. Haase L., Cerf-Ducastel B., Murphy C. Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety. NeuroImage 2009, 44(1008):21.
28. Haber S.N., Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010, 35:4-26.
29. Jacobson A., Green E., Murphy C. Age-related functional changes in gustatory and reward processing regions: an fMRI study. NeuroImage 2010, 53:602-610.
30. Jensen G.L., Rogers J. Obesity in older persons. J Am Diet Assoc 1998, 98:1301-1311.
31. Kobayakawa T., Endo H., Ayabe-Kanamura S., Kumagai T., Yamaguchi Y., Kikuchi Y., et al. The primary gustatory area in human cerebral cortex studied by magnetoencephalography. Neurosci Lett 1996, 212:155-158.
32. Kringelbach M.L., O'Doherty J., Rolls E.T., Andrews C. Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cereb Cortex 2003, 13:1064-1071.
33. Ledikwe J.H., Ello-Martin J.A., Rolls B.J. Portion sizes and the obesity epidemic. J Nutr 2005, 135(4):905-909.
34. McCabe C., Cowen P.J., Harmer C.J. Neural representation of reward in recovered depressed patients. Psychopharmacology 2009, 205:667-677.
35. Miller I. Human taste bud density across adult age groups. J Gerontol 1988, 43:B26-B30.
36. Mulderink T.A., Gitelman D.R., Mesulam M.M., Parrish T.B. On the use of caffeine as a contrast booster for BOLD fMRI studies. NeuroImage 2002, 15:37-44.
37. Muller D.C., Elahi D., Tobin J.D., Andres R. The effect of age on insulin resistance and secretion: a review. Semin Nephrol 1996, 16:289-298.
38. Murphy C. The effects of age on taste sensitivity. Special senses in aging 1979, 21-33. Institute of Gerontology, University of Ann Arbor, Ann Arbor, MI. D.S. Han, D.H. Coon (Eds.).
39. Murphy C. Nutrition and chemosensory perception in the elderly. Crit Rev Food Sci Nutr 1993, 33(1):3-15.
40. Murphy C., Gilmore M.M., Seery C.S., Salmon D.P., Lasker B.R. Olfactory thresholds are associated with degree of dementia in Alzheimer's disease. Neurobiol Aging 1990, 11:465-469.
41. Murphy C., Schubert C.R., Cruickshanks K.J., Klein B.E.K., Klein R., et al. Prevalence of olfactory impairment in older adults. J Am Med Assoc 2002, 288:2307-2312.
42. Nordin S., Bramerson A., Bringlov E., Kobal G., Hummel T., Bende M. Substance and tongue-region specific loss in basic taste-quality identification in elderly adults. Eur Arch Otorhinolaryngol 2007, 264:285-289.
43. Nordin S., Razani J., Markison S., Murphy C. Age-associated increases in intensity discrimination for taste. Exp Aging Res 2003, 29:371-381.
44. Ogawa H., Wakita M., Hasegawa K., Kobayakawa T., Sakai N., Hirai T., et al. Functional MRI detection of activation in the primary gustatory cortices in humans. Chem Senses 2005, 30:583-592.
45. Ogden C.L., Carroll M.D., Curtin L.R., McDowell M., Tabak C., et al. Prevalence of overweight and obesity in the United States, 1999-2004. J Am Med Assoc 2006, 295:1549-1555.
46. Pepino M.Y., Finkbeiner S., Beauchamp G.K., Mennella J.A. Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women. Obesity 2010, 18:959-965.
47. Rolls E.T., Sienkiewicz Z.J., Yaxley S. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur J Neurosci 1989, 1:53-60.
48. Schiffman S.S., Gatlin C. Clinical physiology of taste and smell. Annu Rev Nutr 1993, 13:435-436.
49. Schiffman S.S., Graham B.G. Taste and smell perception affect appetite and immunity in the elderly. Eur J Clin Nutr 2000, 54(Suppl. 3):54-63.
50. Schiffman S.S. Effects of aging on the human taste system. Ann N Y Acad Sci 2009, 1170:725-729.
51. Schimizu Y. A histomorphometric study of the age-related changes of the human taste buds in circumvallate papillae. Oral Med Pathol 1997, 2:17-24.
52. Scott T.R., Plata-Salaman C.R. Taste in the monkey cortex. Physiol Behav 1999, 67(4):489-511.
53. Scott T.R., Verhagen J.V. Taste as a factor in the management of nutrition. Nutrition 2000, 16(10):874-885.
54. Sherwood N.E., Jeffery R.W., French S.A., Hannan P.J., Murray D.M. Predictors of weight gain in the pound of prevention study. Int J Obes Relat Metab Disord 2000, 24:395-403.
55. Ship J.A., Weiffenbach J.M. Age, gender, medical treatment, and medication effects on smell identification. J Gerontol 1993, 48:26-32.
56. Small D.M., Zatorre R.J., Dagher A., Evans A.C., Jones-Gotman M. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 2001, 124:1720-1733.
57. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T., et al. Advances in functional and structural MR image analysis and implementation in FSL. NeuroImage 2004, 23:8208-8219.
58. Stevens J.C., Cruz L.A., Hoffman J.M., Patterson M.Q. Taste sensitivity and aging: high incidence of decline revealed by repeated threshold measures. Chem Senses 1995, 20:451-459.
59. Stice E., Spoor S., Ng J., Zald D. Relation of obesity to consummatory and anticipatory food reward. Physiol Behav 2009, 97:551-560.
60. Stunkard A.J., Messick S. The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res 1985, 1985(29):71-83.
61. Veldhuizen M.G., Albrecht J., Zelano C., Boesveldt S., Breslin P., Lundström J.N. Identification of human gustatory cortex by activation likelihood estimation. Hum Brain Mapp 2011, 32:2256-2266.
62. Volkow N.D., Wang G.J., Fowler J.S., Telang F. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci 2008, 363:3191-3200.
63. Vul E., Harris C., Winkielman P., Pashler H. Puzzingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect Psychol Sci 2009, 4:274-290.
64. Whitmer R.A., Gunderson E.P., Barrett-Connor E., Quesenberry C.P., Yaffe K. Obesity in middle age and future risk of dementia: a 27 year longitudinal based study. Br Med J 2005, 330:1360.
65. Yaxley S., Rolls E.T., Sienkiewicz Z.J. Gustatory responses of single neurons in the insula of the macaque monkey. J Neurophysiol 1990, 63(4):689-700.
66. Yaxley S., Rolls E.T., Sienkiewicz Z.J., Scott T.R. Satiety does not affect gustatory activity in the nucleus of the solitary tract of the alert monkey. Brain Res 1985, 347(1):85-93.