Affective value, intensity and quality of liquid tastants/food discernment in the human brain: An activation likelihood estimation meta-analysis

NeuroImage

Volumn 169, Issue , 2018, Pages 189-199

  Yeung, Andy Wai Kan ^a   Goto, Tazuko K ^a,b   Leung, W Keung ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b TOKYO DENTAL COLLEGE   (Japan)

Author keywords

Affection; Functional magnetic resonance imaging; Intensity; Meta analysis; Quality; Taste

Indexed keywords

ADULT; ARTICLE; BODY MASS; BOLD SIGNAL; CAUDATE NUCLEUS; CONTROLLED STUDY; FEMALE; FOOD; FOOD DISCERNMENT; FOOD INTAKE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSULA; LIQUID FOOD; MALE; NORMAL HUMAN; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; TASTE ACUITY; TASTE AFFECTIVE VALUE; TASTE INTENSITY; TASTE QUALITY; THALAMUS; AFFECT; BRAIN CORTEX; BRAIN MAPPING; DIAGNOSTIC IMAGING; META ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; STATISTICAL MODEL; TASTE; YOUNG ADULT;

ADULT; AFFECT; BRAIN MAPPING; CEREBRAL CORTEX; HUMANS; LIKELIHOOD FUNCTIONS; MAGNETIC RESONANCE IMAGING; TASTE PERCEPTION; YOUNG ADULT;

EID: 85041440258     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2017.12.034     Document Type: Article

References (82)

1. Bender, G., Veldhuizen, M.G., Meltzer, J.A., Gitelman, D.R., Small, D.M., Neural correlates of evaluative compared with passive tasting. Eur. J. Neurosci. 30 (2009), 327–338.
2. Breslin, P.A.S., An evolutionary perspective on food and human taste. Curr. Biol. 23 (2013), R409–R418.
3. Burger, K.S., Stice, E., Neural responsivity during soft drink intake, anticipation, and advertisement exposure in habitually comsuming youth. Obesity 22 (2014), 441–450.
4. Chandrashekar, J., Hoon, M.A., Ryba, N.J.P., Zuker, C.S., The receptors and cells for mammalian taste. Nature 444 (2006), 288–294.
5. Cloutman, L.L., Binney, R.J., Drakesmith, M., Parker, G.J., Ralph, M.A.L., The variation of function across the human insula mirrors its patterns of structural connectivity: evidence from in vivo probabilistic tractography. NeuroImage 59 (2012), 3514–3521.
6. Crouzet, S.M., Busch, N.A., Ohla, K., Taste quality decoding parallels taste sensations. Curr. Biol. 25 (2015), 890–896.
7. Dalenberg, J.R., Hoogeveen, H.R., Renken, R.J., Langers, D.R., ter Horst, G.J., Functional specialization of the male insula during taste perception. NeuroImage 119 (2015), 210–220.
8. de Araujo, I.E., Rolls, E.T., Representation in the human brain of food texture and oral fat. J. Neurosci. 24 (2004), 3086–3093.
9. de Araujo, I.E., Rolls, E.T., Kringelbach, M.L., McGlone, F., Phillips, N., Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur. J. Neurosci. 18 (2003), 2059–2068.
10. Ebisch, S.J., Bello, A., Spitoni, G.F., Perrucci, M.G., Gallese, V., Committeri, G., Pastorelli, C., Pizzamiglio, L., Emotional susceptibility trait modulates insula responses and functional connectivity in flavor processing. Front. Behav. Neurosci., 9, 2015, 297.
11. Eickhoff, S.B., Laird, A.R., Grefkes, C., Wang, L.E., Zilles, K., Fox, P.T., Coordinate-based ALE meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum. Brain Mapp. 30 (2009), 2907–2926.
12. Eickhoff, S.B., Bzdok, D., Laird, A.R., Kurth, F., Fox, P.T., Activation likelihood estimation meta-analysis revisited. NeuroImage 59 (2012), 2349–2361.
13. Eickhoff, S.B., Nichols, T.E., Laird, A.R., Hoffstaedter, F., Amunts, K., Fox, P.T., Bzdok, D., Eickhoff, C.R., Behavior, sensitivity, and power of activation likelihood estimation characterized by massive empirical simulation. NeuroImage 137 (2016), 70–85.
14. Eldeghaidy, S., Marciani, L., Pfeiffer, J.C., Hort, J., Head, K., Taylor, A.J., Spiller, R.C., Gowland, P.A., Francis, S., Use of an immediate swallow protocol to assess taste and aroma integration in fMRI studies. Chemosens Percept 4 (2011), 163–174.
15. Frost, R., Quiñones, I., Veldhuizen, M., Alava, J.-I., Small, D., Carreiras, M., Basic taste processing recruits bilateral anteroventral and middle dorsal insulae: an activation likelihood estimation meta-analysis of fMRI studies. PLoS One, 10, 2015, e0119220.
16. Goto, T.K., Yeung, A.W.K., Suen, J.L.K., Fong, B.S.K., Ninomiya, Y., High resolution time–intensity recording with synchronized solution delivery system for the human dynamic taste perception. J. Neurosci. Meth. 245 (2015), 147–155.
17. Goto, T.K., Yeung, A.W.K., Tanabe, H.C., Ito, Y., Jung, H.-S., Ninomiya, Y., Enhancement of combined umami and salty taste by glutathione in the human tongue and brain. Chem. Senses 41 (2016), 623–630.
18. Grabenhorst, F., Rolls, E.T., Selective attention to affective value alters how the brain processes taste stimuli. Eur. J. Neurosci. 27 (2008), 723–729.
19. Grabenhorst, F., Rolls, E.T., Bilderbeck, A., How cognition modulates affective responses to taste and flavor: top-down influences on the orbitofrontal and pregenual cingulate cortices. Cereb Cortex 18 (2008), 1549–1559.
20. Green, E., Jacobson, A., Haase, L., Murphy, C., Can age-related CNS taste differences be detected as early as middle age? Evidence from fMRI. Neuroscience 232 (2013), 194–203.
21. 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. Meth. 159 (2007), 98–107.
22. Haase, L., Cerf-Ducastel, B., Murphy, C., Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety. NeuroImage 44 (2009), 1008–1021.
23. Haase, L., Green, E., Murphy, C., Males and females show differential brain activation to taste when hungry and sated in gustatory and reward areas. Appetite 57 (2011), 421–434.
24. Holmes, C.J., Hoge, R., Collins, L., Woods, R., Toga, A.W., Evans, A.C., Enhancement of MR images using registration for signal averaging. J. Comput. Assist. Tomogr. 22 (1998), 324–333.
25. Huerta, C.I., Sarkar, P.R., Duong, T.Q., Laird, A.R., Fox, P.T., Neural bases of food perception: coordinate-based meta-analyses of neuroimaging studies in multiple modalities. Obesity 22 (2014), 1439–1446.
26. Iannilli, E., Bult, J.H., Roudnitzky, N., Gerber, J., de Wijk, R.A., Hummel, T., Oral texture influences the neural processing of ortho-and retronasal odors in humans. Brain Res. 1587 (2014), 77–87.
27. Jacobson, A., Green, E., Murphy, C., Age-related functional changes in gustatory and reward processing regions: an fMRI study. NeuroImage 53 (2010), 602–610.
28. Kawakami, S., Sato, H., Sasaki, A.T., Tanabe, H.C., Yoshida, Y., Saito, M., Toyoda, H., Sadato, N., Kang, Y., The brain mechanisms underlying the perception of pungent taste of capsaicin and the subsequent autonomic responses. Front. Hum. Neurosci., 9, 2016, 720.
29. Kim, S.Y., Park, J.E., Lee, Y.J., Seo, H.J., Sheen, S.S., Hahn, S., Jang, B.H., Son, H.J., Testing a tool for assessing the risk of bias for nonrandomized studies showed moderate reliability and promising validity. J. Clin. Epidemiol. 66 (2013), 408–414.
30. Kobayashi, M., Takeda, M., Hattori, N., Fukunaga, M., Sasabe, T., Inoue, N., Nagai, Y., Sawada, T., Sadato, N., Watanabe, Y., Functional imaging of gustatory perception and imagery: “top-down” processing of gustatory signals. NeuroImage 23 (2004), 1271–1282.
31. Kurth, F., Zilles, K., Fox, P.T., Laird, A.R., Eickhoff, S.B., A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 214 (2010), 519–534.
32. Lancaster, J.L., Tordesillas-Gutiérrez, D., Martinez, M., Salinas, F., Evans, A., Zilles, K., Mazziotta, J.C., Fox, P.T., Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum. Brain Mapp. 28 (2007), 1194–1205.
33. Mai, J.K., Majtanik, M., Paxinos, G., Atlas of the Human Brain. fourth ed., 2016, Academic Press, Cambridge, Massachusetts.
34. McCabe, C., Rocha-Rego, V., Investigating the predictive value of functional MRI to appetitive and aversive stimuli: a pattern classification approach. PLoS One, 11, 2016, e0165295.
35. McCabe, C., Huber, A., Harmer, C.J., Cowen, P.J., The D2 antagonist sulpiride modulates the neural processing of both rewarding and aversive stimuli in healthy volunteers. Psychopharmacology (Berl) 217 (2011), 271–278.
36. McCabe, C., Woffindale, C., Harmer, C.J., Cowen, P.J., Neural processing of reward and punishment in young people at increased familial risk of depression. Biol. Psychiatr. 72 (2012), 588–594.
37. McCabe, C., Harwood, J., Brouwer, S., Harmer, C.J., Cowen, P.J., Effects of pramipexole on the processing of rewarding and aversive taste stimuli. Psychopharmacology (Berl) 228 (2013), 283–290.
38. Menon, V., Uddin, L.Q., Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214 (2010), 655–667.
39. Molenberghs, P., Johnson, H., Henry, J.D., Mattingley, J.B., Understanding the minds of others: a neuroimaging meta-analysis. Neurosci. Biobehav. Rev. 65 (2016), 276–291.
40. Moskowitz, H.R., Arabie, P., Taste intensity as a function of stimulus concentration and solvent viscosity. J. Texture Stud. 1 (1970), 502–510.
41. Mufson, E.J., Mesulam, M., Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus. J. Comp. Neurol. 227 (1984), 109–120.
42. Murray, E., Brouwer, S., McCutcheon, R., Harmer, C.J., Cowen, P.J., McCabe, C., Opposing neural effects of naltrexone on food reward and aversion: implications for the treatment of obesity. Psychopharmacology (Berl) 231 (2014), 4323–4335.
43. Nakamura, Y., Goto, T.K., Tokumori, K., Yoshiura, T., Kobayashi, K., Nakamura, Y., Honda, H., Ninomiya, Y., Yoshiura, K., Localization of brain activation by umami taste in humans. Brain Res. 1406 (2011), 18–29.
44. Nakamura, Y., Goto, T.K., Tokumori, K., Yoshiura, T., Kobayashi, K., Nakamura, Y., Honda, H., Ninomiya, Y., Yoshiura, K., The temporal change in the cortical activations due to salty and sweet tastes in humans: fMRI and time–intensity sensory evaluation. NeuroReport 23 (2012), 400–404.
45. Nakamura, Y., Tokumori, K., Tanabe, H.C., Yoshiura, T., Kobayashi, K., Nakamura, Y., Honda, H., Yoshiura, K., Goto, T.K., Localization of the primary taste cortex by contrasting passive and attentive conditions. Exp. Brain Res. 227 (2013), 185–197.
46. Nitschke, J.B., Dixon, G.E., Sarinopoulos, I., Short, S.J., Cohen, J.D., Smith, E.E., Kosslyn, S.M., Rose, R.M., Davidson, R.J., Altering expectancy dampens neural response to aversive taste in primary taste cortex. Nat. Neurosci. 9 (2006), 435–442.
47. Oberndorfer, T.A., Frank, G.K., Simmons, A.N., Wagner, A., McCurdy, D., Fudge, J.L., Yang, T.T., Paulus, M.P., Kaye, W.H., Altered insula response to sweet taste processing after recovery from anorexia and bulimia nervosa. Am. J. Psychiatr. 170 (2013), 1143–1151.
48. Ohla, K., Toepel, U., le Coutre, J., Hudry, J., Electrical neuroimaging reveals intensity-dependent activation of human cortical gustatory and somatosensory areas by electric taste. Biol. Psychol. 85 (2010), 446–455.
49. Ohla, K., Toepel, U., le Coutre, J., Hudry, J., Visual-gustatory interaction: orbitofrontal and insular cortices mediate the effect of high-calorie visual food cues on taste pleasantness. PLoS One, 7, 2012, e32434.
50. Pangborn, R.M., Individual variation in affective responses to taste stimuli. Psychon Sci 21 (1970), 125–126.
51. Pazart, L., Comte, A., Magnin, E., Millot, J.-L., Moulin, T., An fMRI study on the influence of sommeliers’ expertise on the integration of flavor. Front. Behav. Neurosci., 8, 2014, 358.
52. Pritchard, T., Hamilton, R., Morse, J., Norgren, R., Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J. Comp. Neurol. 244 (1986), 213–228.
53. Reed, D.R., Tanaka, T., McDaniel, A.H., Diverse tastes: genetics of sweet and bitter perception. Physiol. Behav. 88 (2006), 215–226.
54. Research Imaging Institute, User Manual for GingerALE 2.3. Retrieved 6 December, 2016, from http://www.brainmap.org/ale/manual.pdf, 2013.
55. Research Imaging Institute, GingerALE Version 2.3.6. Retrieved 6 December, 2016, from http://www.brainmap.org/ale/, 2016.
56. Rolls, E.T., McCabe, C., Enhanced affective brain representations of chocolate in cravers vs. non-cravers. Eur. J. Neurosci. 26 (2007), 1067–1076.
57. Rudenga, K., Green, B., Nachtigal, D., Small, D., Evidence for an integrated oral sensory module in the human anterior ventral insula. Chem. Senses 35 (2010), 693–703.
58. Sawyer, K., The cognitive neuroscience of creativity: a critical review. Creativ. Res. J. 23 (2011), 137–154.
59. Scott, T.R., Plata-Salamán, C.R., Taste in the monkey cortex. Physiol. Behav. 67 (1999), 489–511.
60. Small, D.M., Taste representation in the human insula. Brain Struct. Funct. 214 (2010), 551–561.
61. Small, D.M., Zald, D.H., Jones-Gotman, M., Zatorre, R.J., Pardo, J.V., Frey, S., Petrides, M., Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10 (1999), 7–14.
62. Small, D.M., Gregory, M.D., Mak, Y.E., Gitelman, D., Mesulam, M.M., Parrish, T., Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39 (2003), 701–711.
63. Spetter, M., Smeets, P., de Graaf, C., Viergever, M., Representation of sweet and salty taste intensity in the brain. Chem. Senses 35 (2010), 831–840.
64. Stice, E., Yokum, S., Burger, K., Epstein, L., Smolen, A., Multilocus genetic composite reflecting dopamie signaling capacity predicts reward circuitry responsivity. J. Neurosci. 32 (2012), 10093–10100.
65. Stice, E., Burger, K.S., Yokum, S., Relative ability of fat and sugar tastes to activate reward, gustatory, and somatosensory regions. Am. J. Clin. Nutr. 98 (2013), 1377–1384.
66. Tudge, L., Williams, C., Cowen, P.J., McCabe, C., Neural effects of cannabinoid CB1 neutral antagonist tetrahydrocannabivarin on food reward and aversion in healthy volunteers. Int. J. Neuropsychopharmacol., 18, 2015 pyu094.
67. Turkeltaub, P.E., Eden, G.F., Jones, K.M., Zeffiro, T.A., Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. NeuroImage 16 (2002), 765–780.
68. Turkeltaub, P.E., Eickhoff, S.B., Laird, A.R., Fox, M., Wiener, M., Fox, P., Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum. Brain Mapp. 33 (2012), 1–13.
69. Tzieropoulos, H., Rytz, A., Hudry, J., le Coutre, J., Dietary fat induces sustained reward response in the human brain without primary taste cortex discrimination. Front. Hum. Neurosci., 7, 2013, 36.
70. Research Imaging Institute, UTHSCSA, Mango for the Desktop. Retrieved 6 December, 2016, from http://rii.uthscsa.edu/mango/mango.html, 2016.
71. van der Laan, L.N., Smeets, P.A., You are what you eat: a neuroscience perspective on consumers’ personality characteristics as determinants of eating behavior. Current Opinion in Food Science 3 (2015), 11–18.
72. van der Laan, L.N., de Ridder, D.T., Viergever, M.A., Smeets, P.A., The first taste is always with the eyes: a meta-analysis on the neural correlates of processing visual food cues. NeuroImage 55 (2011), 296–303.
73. van Meer, F., van der Laan, L.N., Adan, R.A., Viergever, M.A., Smeets, P.A., What you see is what you eat: an ALE meta-analysis of the neural correlates of food viewing in children and adolescents. NeuroImage 104 (2015), 35–43.
74. Veldhuizen, M.G., Small, D.M., Modality-specific neural effects of selective attention to taste and odor. Chem. Senses 36 (2011), 747–760.
75. Veldhuizen, M.G., Bender, G., Constable, R.T., Small, D.M., Trying to detect taste in a tasteless solution: modulation of early gustatory cortex by attention to taste. Chem. Senses 32 (2007), 569–581.
76. 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. 32 (2011), 2256–2266.
77. Verhagen, J.V., Engelen, L., The neurocognitive bases of human multimodal food perception: sensory integration. Neurosci. Biobehav. Rev. 30 (2006), 613–650.
78. Wang, Y., Monteiro, C., Popkin, B.M., Trends of obesity and underweight in older children and adolescents in the United States, Brazil, China, and Russia. Am. J. Clin. Nutr. 75 (2002), 971–977.
79. Woods, A.T., Lloyd, D.M., Kuenzel, J., Poliakoff, E., Dijksterhuis, G.B., Thomas, A., Expected taste intensity affects response to sweet drinks in primary taste cortex. NeuroReport 22 (2011), 365–369.
80. World Health Organization, BMI Classification. Retrieved 27 January, 2017, from http://apps.who.int/bmi/index.jsp?introPage=intro_3.html, 2006.
81. Yeung, A.W.K., Tanabe, H.C., Suen, J.L.K., Goto, T.K., Taste intensity modulates effective connectivity from the insular cortex to the thalamus in humans. NeuroImage 135 (2016), 214–222.
82. Yeung, A.W.K., Goto, T.K., Leung, W.K., Basic taste processing recruits bilateral anteroventral and middle dorsal insulae: an activation likelihood estimation meta-analysis of fMRI studies. Brain Behav, 7, 2017, e00655.