Food labels promote healthy choices by a decision bias in the amygdala

NeuroImage

Volumn 74, Issue , 2013, Pages 152-163

  Grabenhorst, Fabian ^a,b   Schulte, Frank P ^b,c   Maderwald, Stefan ^b   Brand, Matthias ^b,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ERWIN L HAHN INSTITUTE FOR MAGNETIC RESONANCE IMAGING   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Amygdala; Decision; Emotion; Food; Obesity; Reward

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; CONSUMER HEALTH INFORMATION; CONTROLLED STUDY; DECISION MAKING; FEMALE; FOOD PACKAGING; FOOD PREFERENCE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEALTH FOOD; HUMAN; HUMAN EXPERIMENT; MALE; NEUROIMAGING; NEUROMODULATION; NORMAL HUMAN; PRIORITY JOURNAL; TASTE;

ADULT; AMYGDALA; BRAIN MAPPING; CHOICE BEHAVIOR; EMOTIONS; FEMALE; FOOD LABELING; HEALTH BEHAVIOR; HEALTH POLICY; HEALTH PROMOTION; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; YOUNG ADULT;

EID: 84874997957     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.02.012     Document Type: Article

References (102)

1. Adolphs R. What does the amygdala contribute to social cognition?. Ann. N. Y. Acad. Sci. 2010, 1191:42-61.
2. Adolphs R., Tranel D., Damasio H., Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 1994, 372:669-672.
3. Andrade A., Paradis A.L., Rouquette S., Poline J.B. Ambiguous results in functional neuroimaging data analysis due to covariate correlation. Neuroimage 1999, 10:483-486.
4. Arana F.S., Parkinson J.A., Hinton E., Holland A.J., Owen A.M., Roberts A.C. Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection. J. Neurosci. 2003, 23:9632-9638.
5. Balleine B.W., Killcross S. Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci. 2006, 29:272-279.
6. Bargh J.A., Morsella E. The unconscious mind. Perspect. Psychol. Sci. 2008, 3:73-79.
7. Basten U., Biele G., Heekeren H.R., Fiebach C.J. How the brain integrates costs and benefits during decision making. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21767-21772.
8. Bechara A., Damasio H., Damasio A.R., Lee G.P. Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J. Neurosci. 1999, 19:5473-5481.
9. Bechara A., Damasio H., Damasio A.R. Role of the amygdala in decision-making. Ann. N. Y. Acad. Sci. 2003, 985:356-369.
10. Behrens T.E., Hunt L.T., Woolrich M.W., Rushworth M.F. Associative learning of social value. Nature 2008, 456:245-249.
11. 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. 2009, 30:327-338.
12. Bermudez M.A., Schultz W. Reward magnitude coding in primate amygdala neurons. J. Neurophysiol. 2010, 104:3424.
13. Berwick R.C., Chomsky N. The biolinguistic program: the current state of its development. The Biolinguistic Enterprise: New Perspectives on the Evolution and Nature of the Human Language Faculty 2011, 19-41. Oxford University Press, Oxford. A.M. Di Sciullo, C. Boeckx (Eds.).
14. Bollinger B., Leslie P., Sorensen A. Calorie posting in chain restaurants. Am. Econ. J. Econ. Policy 2011, 3:91-128.
15. Brand M., Grabenhorst F., Starcke K., Vandekerckhove M.M., Markowitsch H.J. Role of the amygdala in decisions under ambiguity and decisions under risk: evidence from patients with Urbach-Wiethe disease. Neuropsychologia 2007, 45:1305-1317.
16. Christopoulos G.I., Tobler P.N., Bossaerts P., Dolan R.J., Schultz W. Neural correlates of value, risk, and risk aversion contributing to decision making under risk. J. Neurosci. 2009, 29:12574-12583.
17. Davis M., Whalen P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 2001, 6:13-34.
18. de Araujo I.E.T., 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. 2003, 18:2059-2068.
19. de Araujo I.E.T., Rolls E.T., Velazco M.I., Margot C., Cayeux I. Cognitive modulation of olfactory processing. Neuron 2005, 46:671-679.
20. de Araujo I.E., Gutierrez R., Oliveira-Maia A.J., Pereira A., Nicolelis M.A., Simon S.A. Neural ensemble coding of satiety states. Neuron 2006, 51:483-494.
21. De Martino B., Kumaran D., Seymour B., Dolan R.J. Frames, biases, and rational decision-making in the human brain. Science 2006, 313:684-687.
22. Deco G., Scarano L., Soto-Faraco S. Weber's law in decision making: integrating behavioral data in humans with a neurophysiological model. J. Neurosci. 2007, 27:11192-11200.
23. Dolan R.J. The human amygdala and orbital prefrontal cortex in behavioural regulation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2007, 362:787-799.
24. Downs J.S., Loewenstein G., Wisdom J. Strategies for Promoting Healthier Food Choices. Am. Econ. Rev. 2009, 99:159-164.
25. Draper N.R., Smith H. Applied Regression Analysis 1998, Wiley-Interscience. Third Edition.
26. Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E.T., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997, 6:218-229.
27. Fuhrer D., Zysset S., Stumvoll M. Brain activity in hunger and satiety: an exploratory visually stimulated FMRI study. Obesity (Silver Spring) 2008, 16:945-950.
28. Gitelman D.R., Penny W.D., Ashburner J., Friston K.J. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 2003, 19:200-207.
29. Gottfried J.A., O'Doherty J., Dolan R.J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 2003, 301:1104-1107.
30. Grabenhorst F., Rolls E.T. Selective attention to affective value alters how the brain processes taste stimuli. Eur. J. Neurosci. 2008, 27:723-729.
31. Grabenhorst F., Rolls E.T. Different representations of relative and absolute value in the human brain. Neuroimage 2009, 48:258-268.
32. Grabenhorst F., Rolls E.T. Value, pleasure and choice in the ventral prefrontal cortex. Trends Cogn. Sci. 2011, 15:56-67.
33. Grabenhorst F., Rolls E.T., Margot C., da Silva M.A.A.P., Velazco M.I. How pleasant and unpleasant stimuli combine in different brain regions: odor mixtures. J. Neurosci. 2007, 27:13532-13540.
34. 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 2008, 18:1549-1559.
35. Grabenhorst F., Rolls E.T., Parris B.A. From affective value to decision-making in the prefrontal cortex. Eur. J. Neurosci. 2008, 28:1930-1939.
36. Grabenhorst F., D'Souza A., Parris B.A., Rolls E.T., Passingham R.E. A common neural scale for the subjective pleasantness of different primary rewards. Neuroimage 2010, 51:1265-1274.
37. Grabenhorst F., Rolls E.T., Parris B.A., D'Souza A. How the brain represents the reward value of fat in the mouth. Cereb. Cortex 2010, 20:1082-1091.
38. Grabenhorst F., Hernadi I., Schultz W. Prediction of economic choice by primate amygdala neurons. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:18950-18955.
39. Griswold M.A., Jakob P.M., Heidemann R.M., Nittka M., Jellus V., Wang J., Kiefer B., Haase A. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn. Reson. Med. 2002, 47:1202-1210.
40. Hare T.A., Camerer C.F., Rangel A. Self-control in decision-making involves modulation of the vmPFC valuation system. Science 2009, 324:646-648.
41. Hare T.A., Camerer C.F., Knoepfle D.T., Rangel A. Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J. Neurosci. 2010, 30:583-590.
42. Hare T.A., Malmaud J., Rangel A. Focusing attention on the health aspects of foods changes value signals in vmPFC and improves dietary choice. J. Neurosci. 2011, 31:11077-11087.
43. Harris J.L., Brownell K.D., Bargh J.A. The food marketing defense model: integrating psychological research to protect youth and inform public policy. Soc. Issues Policy Rev. 2009, 3:211-271.
44. Heekeren H.R., Marrett S., Bandettini P.A., Ungerleider L.G. A general mechanism for perceptual decision-making in the human brain. Nature 2004, 431:859-862.
45. Heekeren H.R., Marrett S., Ruff D.A., Bandettini P.A., Ungerleider L.G. Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10023-10028.
46. Hilbert A., Tuschen-Caffier B. Eating Disorder Examination Questionnaire - Deutschsprachige Uebersetzung [German Translation] 2006, Verlag fuer Psychotherapie, Muenster.
47. Hunt L.T., Kolling N., Soltani A., Woolrich M.W., Rushworth M.F., Behrens T.E. Mechanisms underlying cortical activity during value-guided choice. Nat. Neurosci. 2012, 15(470-476):S471-S473.
48. Insabato A., Pannunzi M., Rolls E.T., Deco G. Confidence-related decision-making. J. Neurophysiol. 2010, 104:539-547.
49. Jackendoff R. Foundations of Language 2002, Oxford University Press, Oxford.
50. Jenison R.L., Rangel A., Oya H., Kawasaki H., Howard M.A. Value encoding in single neurons in the human amygdala during decision making. J. Neurosci. 2011, 31:331-338.
51. Just D.R., Payne C.R. Obesity: can behavioral economics help?. Ann. Behav. Med. 2009, 38(Suppl. 1):S47-S55.
52. Kable J.W., Glimcher P.W. The neural correlates of subjective value during intertemporal choice. Nat. Neurosci. 2007, 10:1625-1633.
53. Kadohisa M., Rolls E.T., Verhagen J.V. The primate amygdala: neuronal representations of the viscosity, fat texture, temperature, grittiness and taste of foods. Neuroscience 2005, 132:33-48.
54. Kahneman D., Tversky A. Choices, values, and frames. Am. Psychol. 1984, 4:341-350.
55. Kiesel K., McCluskey J.J., Villas-Boas S.B. Nutritional labeling and consumer choices. Ann. Rev. Resour. Econ. 2011, 3.
56. Kim J.N., Shadlen M.N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat. Neurosci. 1999, 2:176-185.
57. 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.
58. Linder N.S., Uhl G., Fliessbach K., Trautner P., Elger C.E., Weber B. Organic labeling influences food valuation and choice. Neuroimage 2010, 53:215-220.
59. Loewenstein G., Brennan T., Volpp K.G. Asymmetric paternalism to improve health behaviors. JAMA 2007, 298:2415-2417.
60. McCabe C., Rolls E.T. Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain. Eur. J. Neurosci. 2007, 25:1855-1864.
61. McCabe C., Rolls E.T., Bilderbeck A., McGlone F. Cognitive influences on the affective representation of touch and the sight of touch in the human brain. Soc. Cogn. Affect. Neurosci. 2008, 3:97-108.
62. McClure S.M., Li J., Tomlin D., Cypert K.S., Montague L.M., Montague P.R. Neural correlates of behavioral preference for culturally familiar drinks. Neuron 2004, 44:379-387.
63. Murawski C., Harris P.G., Bode S., Dominguez D.J., Egan G.F. Led into temptation? Rewarding brand logos bias the neural encoding of incidental economic decisions. PLoS One 2012, 7:e34155.
64. Ng J., Stice E., Yokum S., Bohon C. An fMRI study of obesity, food reward, and perceived caloric density. Does a low-fat label make food less appealing?. Appetite 2011, 57:65-72.
65. O'Doherty J., Rolls E.T., Francis S., Bowtell R., McGlone F. The representation of pleasant and aversive taste in the human brain. J. Neurophysiol. 2001, 85:1315-1321.
66. Orzada S., Kraff O., Schaefer L.C., Brote I., Bahr A., Bolz T., Maderwald S., Ladd M.E. 8-Channel transmit/receive head coil for 7 T human imaging using intrinsically decoupled strip line elements with meanders. Proceedings of the 17th Annual Meeting of ISMRM 2009, (Honolulu, HI: Abstract 3010).
67. Padoa-Schioppa C. Neurobiology of economic choice: a good-based model. Annu. Rev. Neurosci. 2011, 34:333-359.
68. Paton J.J., Belova M.A., Morrison S.E., Salzman C.D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 2006, 439:865-870.
69. Pessoa L., Adolphs R. Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat. Rev. Neurosci. 2010, 11:773-783.
70. Phelps E.A. Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 2006, 57:27-53.
71. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
72. Plassmann H., O'Doherty J., Shiv B., Rangel A. Marketing actions can modulate neural representations of experienced pleasantness. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1050-1054.
73. Poser B.A., Norris D.G. Investigating the benefits of multi-echo EPI for fMRI at 7T. Neuroimage 2009, 45:1162-1172.
74. Roiser J.P., de Martino B., Tan G.C., Kumaran D., Seymour B., Wood N.W., Dolan R.J. A genetically mediated bias in decision making driven by failure of amygdala control. J. Neurosci. 2009, 29:5985-5991.
75. Rolls E.T. Neurophysiology and functions of the primate amygdala, and the neural basis of emotion. The Amygdala: a Functional Analysis 2000, 447-478. Oxford University Press, Oxford. J.P. Aggleton (Ed.).
76. Rolls E.T. Sensory processing in the brain related to the control of food intake. Proc. Nutr. Soc. 2007, 66:96-112.
77. Rolls E.T., Grabenhorst F., Deco G. Choice, difficulty, and confidence in the brain. Neuroimage 2010, 53:694-706.
78. Rolls E.T., Grabenhorst F., Deco G. Decision-making, errors, and confidence in the brain. J. Neurophysiol. 2010, 104:2359-2374.
79. Rolls E.T., Grabenhorst F., Parris B.A. Neural systems underlying decisions about affective odors. J. Cogn. Neurosci. 2010, 22:1069-1082.
80. Ruff D.A., Marrett S., Heekeren H.R., Bandettini P.A., Ungerleider L.G. Complementary roles of systems representing sensory evidence and systems detecting task difficulty during perceptual decision making. Front. Neurosci. 2010, 4:190.
81. Schultz W. Potential vulnerabilities of neuronal reward, risk, and decision mechanisms to addictive drugs. Neuron 2011, 69:603-617.
82. Seymour B., Dolan R. Emotion, decision making, and the amygdala. Neuron 2008, 58:662-671.
83. Sharot T. The optimism bias. Curr. Biol. 2011, 21:R941-R945.
84. Sharot T., Riccardi A.M., Raio C.M., Phelps E.A. Neural mechanisms mediating optimism bias. Nature 2007, 450:102-105.
85. Sharot T., De Martino B., Dolan R.J. How choice reveals and shapes expected hedonic outcome. J. Neurosci. 2009, 29:3760-3765.
86. Sharot T., Shiner T., Dolan R.J. Experience and choice shape expected aversive outcomes. J. Neurosci. 2010, 30:9209-9215.
87. Siep N., Roefs A., Roebroeck A., Havermans R., Bonte M.L., Jansen A. Hunger is the best spice: an fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex. Behav. Brain Res. 2009, 198:149-158.
88. Small D.M. Individual differences in the neurophysiology of reward and the obesity epidemic. Int. J. Obes. (Lond) 2009, 33(Suppl. 2):S44-S48.
89. 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 2003, 39:701-711.
90. Small D.M., Gerber J.C., Mak Y.E., Hummel T. Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 2005, 47:593-605.
91. Small D.M., Veldhuizen M.G., Felsted J., Mak Y.E., McGlone F. Separable substrates for anticipatory and consummatory food chemosensation. Neuron 2008, 57:786-797.
92. Smeets P.A., Weijzen P., de Graaf C., Viergever M.A. Consumption of caloric and non-caloric versions of a soft drink differentially affects brain activation during tasting. Neuroimage 2011, 54:1367-1374.
93. Thaler R.H., Sunstein C.R. Nudge: Improving Decisions about Health, Wealth and Happiness 2008, Yale University Press, New Haven, CT.
94. Vickers D. Decision Processes in Visual Perception 1979, Academic Press, New York.
95. Vickers D., Packer J. Effects of alternating set for speed or accuracy on response time, accuracy and confidence in a unidimensional discrimination task. Acta Psychol. 1982, 50:179-197.
96. Volkow N.D., Wang G.J., Baler R.D. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn. Sci. 2011, 15:37-46.
97. Wang X.J. Probabilistic decision making by slow reverberation in cortical circuits. Neuron 2002, 36:955-968.
98. Wang X.J. Decision making in recurrent neuronal circuits. Neuron 2008, 60:215-234.
99. Wunderlich K., Rangel A., O'Doherty J.P. Economic choices can be made using only stimulus values. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15005-15010.
100. Yan J., Scott T.R. The effect of satiety on responses of gustatory neurons in the amygdala of alert cynomolgus macaques. Brain Res. Brain Res. Rev. 1996, 740:193-200.
101. Zald D.H. The human amygdala and the emotional evaluation of sensory stimuli. Brain Res. Brain Res. Rev. 2003, 41:88-123.
102. Zimmerman F.J. Using marketing muscle to sell fat: the rise of obesity in the modern economy. Annu. Rev. Public Health 2011, 32:285-306.