Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion

Acta Physiologica Hungarica

Volumn 95, Issue 2, 2008, Pages 131-164

  Rolls, E T ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Appetite; Cingulate cortex; Emotion; fMRI; Neuronal activity; Olfaction; Orbitofrontal cortex; Taste

Indexed keywords

ANIMAL; APPETITE; BRAIN MAPPING; CINGULATE GYRUS; CYTOLOGY; EMOTION; FRONTAL LOBE; HUMAN; NERVE CELL; NERVE TRACT; ODOR; PHYSIOLOGY; PSYCHOPHYSIOLOGY; REVIEW; TASTE;

ANIMALS; APPETITE; BRAIN MAPPING; EMOTIONS; FRONTAL LOBE; GYRUS CINGULI; HUMANS; NEURAL PATHWAYS; NEURONS; SATIETY RESPONSE; SMELL; TASTE;

EID: 44649167641     PISSN: 0231424X     EISSN: 15882683     Source Type: Journal    
DOI: 10.1556/APhysiol.95.2008.2.1     Document Type: Review

References (121)

1. Rolls ET (2005): Emotion Explained. Oxford: Oxford, University Press
2. Scott TR, Yaxley S, Sienkiewicz ZJ, Rolls ET: Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. J. of Neurophysiology 56, 876-890 (1986)
3. Yaxley S, Rolls ET, Sienkiewicz ZJ: Gustatory responses of single neurons in the insula of the macaque monkey. J. of Neurophysiology 63, 689-700 (1990)
4. Rolls ET, Scott TR (2003): Central taste anatomy and neurophysiology. In: Handbook of Olfaction and Gustation. 2 nd ed. (Ed.: Doty RL), New York, Dekker, pp. 679-705
5. Baylis LL, Rolls ET: Responses of neurons in the primate taste cortex to glutamate. Physiology and Behavior 49, 973-979 (1991)
6. Rolls ET, Critchley H, Wakeman EA, Mason R: Responses of neurons in the primate taste cortex to the glutamate ion and to inosine 5′-monophosphate. Physiology and Behavior 59, 991-1000 (1996)
7. Verhagen JV, Kadohisa M, Rolls ET: The primate insular/opercular taste cortex: neuronal representations of the viscosity, fat texture, grittiness, temperature and taste of foods. J. of Neurophysiology 92, 1685-1699 (2004)
8. Rolls ET, Scott TR, Sienkiewicz ZJ, Yaxley S: The responsiveness of neurones in the frontal opercular gustatory cortex of the macaque monkey is independent of hunger. J. of Physiol. 397, 1-12 (1988)
9. Yaxley S, Rolls ET, Sienkiewicz ZJ: The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiology and Behavior 42, 223-229 (1988)
10. Rolls ET, Yaxley S, Sienkiewicz ZJ: Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J. of Neurophysiology 64, 1055-1066 (1990)
11. Rolls ET: Taste and olfactory processing in the brain and its relation to the control of eating. Critical Reviews in Neurobiology 11, 263-287 (1997)
12. Zhao GQ, Zhang Y, Hoon MA, et al.: The receptors for mammalian sweet and umami taste. Cell 115(3), 255-266 (2003)
13. Rolls ET, Critchley HD, Browning A, Hernadi I: The neurophysiology of taste and olfaction in primates, and umami flavor. Annals of the New York Academy of Sciences 855, 426-437 (1998)
14. McCabe C, Rolls ET: Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain. Europ. J. of Neurosci. 25, 1855-1864 (2007)
15. Critchley HD, Rolls ET: Responses of primate taste cortex neurons to the astringent tastant tannic acid. Chemical Senses 21, 135-145 (1996)
16. Rolls ET, Verhagen JV, Kadohisa M: Representations of the texture of food in the primate orbitofrontal cortex: neurons responding to viscosity, grittiness and capsaicin. J. of Neurophysiology 90, 3711-3724 (2003)
17. Kadohisa M, Rolls ET, Verhagen JV: Orbitofrontal cortex neuronal representation of temperature and capsaicin in the mouth. Neuroscience 127, 207-221 (2004)
18. Rolls ET (1999): The Brain and Emotion. Oxford, Oxford University Press
19. Yaxley S, Rolls ET, Sienkiewicz ZJ, Scott TR: Satiety does not affect gustatory activity in the nucleus of the solitary tract of the alert monkey. Brain Research 347, 85-93 (1985)
20. Rolls ET, Sienkiewicz ZJ, Yaxley S: Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Europ. J. of Neurosci. 1, 53-60 (1989)
21. Critchley HD, Rolls ET: Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. J. of Neurophysiology 75, 1673-1686 (1996)
22. Cabanac M: Physiological role of pleasure. Science 173, 1103-1107 (1971)
23. Rolls BJ, Rolls ET, Rowe EA, Sweeney K: Sensory specific satiety in man. Physiology and Behavior 27, 137-142 (1981)
24. Rolls BJ, Rowe EA, Rolls ET, et al.: Variety in a meal enhances food intake in man. Physiology and Behavior 26, 215-221 (1981)
25. Rolls BJ, Rowe EA, Rolls ET: How sensory properties of foods affect human feeding behavior. Physiology and Behavior 29, 409-417 (1982)
26. Rolls ET, Rolls BJ (1977): Activity of neurones in sensory, hypothalamic and motor areas during feeding in the monkey. In: Food Intake and Chemical Senses. Eds: Katsuki Y, Sato M, Takagi S, Oomura Y. Tokyo, University of Tokyo Press, pp. 525-549
27. Rolls ET, Rolls BJ (1982): Brain mechanisms involved in feeding. In: Psychobiology of Human Food Selection. Ed.: Barker LM. Westport, Connecticut, AVI Publishing Company, pp. 33-62
28. Rolls BJ, Rolls ET, Rowe EA: Body fat control and obesity. Behavioral and Brain Sciences 4, 744-745 (1983)
29. Rolls ET, Rolls BJ, Rowe EA: Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man. Physiology and Behavior 30, 185-192 (1983)
30. Rolls ET, Murzi E, Yaxley S, Thorpe SJ, Simpson SJ: Sensory-specific satiety: food-specific reduction in responsiveness of ventral forebrain neurons after feeding in the monkey. Brain Research 368, 79-86 (1986)
31. Critchley HD, Rolls ET: Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task. J. of Neurophysiol. 75, 1659-1672 (1996)
32. Rolls ET: The orbitofrontal cortex. Philosophical Transactions of the Royal Society of London B 351, 1433-1444 (1996)
33. Rolls ET: The orbitofrontal cortex and reward. Cerebral Cortex 10, 284-294 (2000)
34. Rolls ET (2000): Taste, olfactory, visual and somatosensory representations of the sensory properties of foods in the brain, and their relation to the control of food intake. In: Neural and Metabolic Control of Macronutrient Intake. Eds: Berthoud H-R, Seeley RJ. Boca-Raton, Florida, CRC Press, pp. 247-262
35. Scott TR, Yan J, Rolls ET: Brain mechanisms of satiety and taste in macaques. Neurobiology 3, 281-292 (1995)
36. Zatorre RJ, Jones-Gotman M, Evans AC, Meyer E: Functional localization of human olfactory cortex. Nature 360, 339-340 (1992)
37. Francis S, Rolls ET, Bowtell R, et al.: The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport 10, 453-459 (1999)
38. O'Doherty J, Rolls ET, Francis S, et al.: Sensory-specific satiety related olfactory activation of the human orbitofrontal cortex. Neuroreport 11, 893-897 (2000)
39. Rolls ET, Kringelbach ML, de Araujo IET: Different representations of pleasant and unpleasant odors in the human brain. Europ. J. of Neurosci. 18, 695-703 (2003)
40. de Araujo IET, Rolls ET, Velazco MI, Margot C, Cayeux I: Cognitive modulation of olfactory processing. Neuron 46, 671-679 (2005)
41. de Araujo IET, Rolls ET, Kringelbach ML, McGlone F, Phillips N: Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Europ. J. of Neurosci. 18, 2374-2390 (2003)
42. de Araujo IET, Kringelbach ML, Rolls ET, Hobden P: The representation of umami taste in the human brain. J. of Neurophysiol. 90, 313-319 (2003)
43. de Araujo IET, Rolls ET: The representation in the human brain of food texture and oral fat. J. of Neurosci. 24, 3086-3093 (2004)
44. Li W, Luxenberg E, Parrish T, Gottfried JA: Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron 52(6), 1097-1108 (2006)
45. Gottfried JA, Small DM, Zald DH (2006): The chemical senses. In: The Orbitofrontal Cortex. Eds: Zald DH, Rauch SL. Oxford, Oxford University Press, pp. 125-171
46. Rolls ET, McCabe C: Enhanced affective brain representations of chocolate in cravers vs non-cravers. Europ. J. of Neurosci. 26, 1067-1076 (2007)
47. Kringelbach ML, Rolls ET: The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Progress in Neurobiology 72, 341-372 (2004)
48. Rolls ET, Verhagen JV, Gabbott PL, Kadohisa M: Taste and texture representations in the primate pregenual cingulate and medial orbitofrontal cortices. In preparation (2008)
49. Baylis LL, Rolls ET, Baylis GC: Afferent connections of the orbitofrontal cortex taste area of the primate. Neuroscience 64, 801-812(1995)
50. Rolls ET, Baylis LL: Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J. of Neurosci. 14, 5437-5452 (1994)
51. Pritchard TC, Edwards EM, Smith CA, et al.: Gustatory neural responses in the medial orbitofrontal cortex of the old world monkey. J. Neurosci. 25, 6047-6056 (2005)
52. Carmichael ST, Price JL: Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J. of Comparative Neurology 346, 366-402 (1994)
53. Ongur D, Ferry AT, Price JL: Architectonic division of the human orbital and medial prefrontal cortex. J. of Comparative Neurology 460, 425-449 (2003)
54. Ongur D, Price JL: The organisation of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10, 206-219 (2000)
55. Petrides M, Pandya DN: Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Europ. J. of Neurosci. 16, 291-310 (2001)
56. Rolls ET: Brain mechanisms underlying flavour and appetite. Philosophical Transactions of the Royal Society London B 361, 1123-1136 (2006)
57. Verhagen JV, Rolls ET, Kadohisa M: Neurons in the primate orbitofrontal cortex respond to fat texture independently of viscosity. J. of Neurophysiol. 90, 1514-1525 (2003)
58. Kadohisa M, Rolls ET, Verhagen JV: Neuronal representations of stimuli in the mouth: the primate insular taste cortex, orbitofrontal cortex, and amygdala. Chemical Senses 30, 401-419 (2005)
59. Rolls ET, Critchley HD, Browning AS, Hernadi A, Lenard L: Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J. of Neurosci. 19, 1532-1540 (1999)
60. Rolls ET, Critchley HD, Treves A: The representation of olfactory information in the primate orbitofrontal cortex. J. of Neurophysiol. 75, 1982-1996 (1996)
61. Rolls ET, Critchley HD, Mason R, Wakeman EA: Orbitofrontal cortex neurons: role in olfactory and visual association learning. J. of Neurophysiol. 75, 1970-1981 (1996)
62. Pritchard TC, Hamilton RB, Morse JR, Norgren R: Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J. of Comparative Neurology 244, 213-228 (1986)
63. Carmichael ST, Price JL: Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J. of Comparative Neurology 371, 179-207 (1996)
64. Scott TR, Edwards EM, Smith CA, et al.: Medial orbitofrontal cortex: its role in mediating satiety in the macaque. Chem. Senses 30(Suppl 1), i190 (2005)
65. Rolls ET: Sensory processing in the brain related to the control of food intake. Proceedings of the Nutrition Society 66, 96-112 (2007)
66. Goldman-Rakic PS: The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Philosophical Transactions of the Royal Society B 351, 1445-1453 (1996)
67. Rolls ET, Deco G (2002): Computational Neuroscience of Vision. Oxford. Oxford University Press
68. Deco G, Rolls ET: Attention, short-term memory, and action selection: a unifying theory. Progress in Neurobiology 76, 236-256 (2005)
69. Rolls ET (2008): The anterior and midcingulate cortices and reward. In: Cingulate Neurobiology & Disease. Ed: Vogt BA. Oxford, Oxford University Press
70. Amiez C, Joseph JP, Procyk E: Reward encoding in the monkey anterior cingulate cortex. Cerebral Cortex 16, 1040-1055 (2006)
71. Rushworth MF, Walton ME, Kennerley SW, Bannerman DM: Action sets and decisions in the medial frontal cortex. Trends in Cognitive Sciences 8, 410-417 (2004)
72. Hornak J, Bramham J, Rolls ET, et al.: Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. Brain 126, 1691-1712 (2003)
73. Mayberg HS: Positron emission tomography imaging in depression: a neural systems perspective: Neuroimaging Clin. N. Am. 13(4), 805-815 (2003)
74. Fisher RA (1932): Statistical Methods for Research Workers. London, Oliver and Boyd
75. Littell RC, Folks JL: Asymptotic optimality of Fisher's method of combining independent tests. J. Am. Stat. Assoc. 66, 802-806 (1971)
76. Zaykin DV, Zhivotovsky LA, Westfall PH, Weir BS: Truncated product method for combining P-values. Genet. Epidemiol. 22, 170-185 (2002)
77. Rolls ET, O'Doherty J, Kringelbach ML, et al.: Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cerebral Cortex 13, 308-317 (2003)
78. Zald DH, Lee JT, Fluegel KW, Pardo JV: Aversive gustatory stimulation activates limbic circuits in humans. Brain 121, 1143-1154 (1998)
79. Ito S, Stuphorn V, Brown JW, Schall JD: Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120-122 (2003)
80. Vogt BA Ed. (2008): Cingulate Neurobiology & Disease. Oxford. Oxford University Press
81. Rolls ET (2008): Memory, Attention, and Decision-Making: A Unifying Computational Neuroscience Approach. Oxford, Oxford University Press
82. Rolls ET: The rules of formation of the olfactory representations found in the orbitofrontal cortex olfactory areas in primates. Chemical Senses 26, 595-604 (2001)
83. Rolls ET (2002): The cortical representation of taste and smell. In: Olfaction, Taste and Cognition. Eds: Rouby G, Schaal B, Dubois D, Gervais R, Holley A. New York, Cambridge University Press, pp. 367-388
84. Rolls ET (2002): The functions of the orbitofrontal cortex. In: Principles of Frontal Lobe Function. Eds: Stuss DT, Knight RT. New York, Oxford University Press, Chap. 23, pp. 354-375
85. Rolls ET: Central nervous mechanisms related to feeding and appetite. British Medical Bulletin 37, 131-134 (1981)
86. Rolls BJ, Van Duijvenvoorde PM, Rolls ET: Pleasantness changes and food intake in a varied fourcourse meal. Appetite 5, 337-348 (1984)
87. Rolls BJ (1990): The role of sensory-specific satiety in food intake and food selection. In: Taste, Experience, and Feeding. Eds: Capaldi ED, Powley TL, Washington DC, American Psychological Association, pp. 197-209
88. Cabanac M, Fantino M: Origin of olfacto-gustatory alliesthesia: Intestinal sensitivity to carbohydrate concentration? Physiology and Behavior 10, 1039-1045 (1977)
89. Cabanac M, Duclaux R: Specificity of internal signals in producing satiety for taste stimuli. Nature 227, 966-967 (1970)
90. Rolls ET, Rolls JH: Olfactory sensory-specific satiety in humans. Physiology and Behavior 61, 461-473 (1997)
91. Rolls ET: Understanding the mechanisms of food intake and obesity. Obesity Reviews 8(Suppl. 1), 67-72 (2007)
92. Rolls BJ, Van Duijenvoorde PM, Rowe EA: Variety in the diet enhances intake in a meal and contributes to the development of obesity in the rat. Physiology and Behavior 31, 21-27 (1983)
93. Rolls BJ, Hetherington M (1989): The role of variety in eating and body weight regulation. In: Handbook of the Psychophysiology of Human Eating. Ed: Shepherd R. Chichester, Wiley, pp. 57-84
94. Thorpe SJ, Rolls ET, Maddison S: Neuronal activity in the orbitofrontal cortex of the behaving monkey. Experimental Brain Research 49, 93-115 (1983)
95. Rolls ET: Taste and olfactory processing in the brain, and its relation to the control of eating. Frontiers of Oral Biology 9, 40-75 (1998)
96. Kadohisa M, Rolls ET, Verhagen JV: The primate amygdala: neuronal representations of the viscosity, fat texture, grittiness and taste of foods. Neuroscience 132, 33-48 (2005)
97. Rolls ET (2000): Neurophysiology and functions of the primate amygdala, and the neural basis of emotion. In: The Amygdala: A Functional Analysis. Ed.: Aggleton JP Second Edition. Oxford, Oxford University Press, pp. 447-478
98. Sanghera MK, Rolls ET, Roper-Hall A: Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Experimental Neurology 63, 610-626 (1979)
99. Deco G, Rolls ET: Synaptic and spiking dynamics underlying reward reversal in orbitofrontal cortex. Cerebral Cortex 15, 15-30 (2005)
100. O'Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F: The representation of pleasant and aversive taste in the human brain. Journal of Neurophysiology 85, 1315-1321 (2001)
101. de Araujo IET, Kringelbach ML, Rolls ET, McGlone F: Human cortical responses to water in the mouth, and the effects of thirst. J. of Neurophysiol. 90, 1865-1876 (2003)
102. Poellinger A, Thomas R, Lio P, et al.: Activation and habituation in olfaction - an fMRI study. NeuroImage 13, 547-560 (2001)
103. Sobel N, Prabkakaran V, Zhao Z, et al.: Time course of odorant-induced activation in the human primary olfactory cortex. J. of Neurophysiol. 83, 537-551 (2000)
104. Zald DH, Pardo JV: Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proceedings of the National Academy of Sciences USA 94, 4119-4124 (1997)
105. Small DM, Voss J, Mak YE, et al.: Experience-dependent neural integration of taste and smell in the human brain. J. of Neurophysiol. 92, 1892-1903 (2004)
106. Small DM, Prescott J: Odor/taste integration and the perception of flavor. Experimental Brain Research 166, 345-357 (2005)
107. Kringelbach ML, O'Doherty J, Rolls ET, Andrews C: Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cerebral Cortex 13, 1064-1071 (2003)
108. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ: Neural responses during anticipation of a primary taste reward. Neuron 33, 815-826 (2002)
109. Simmons WK, Martin A, Barsalou LW: Pictures of appetizing foods activate gustatory cortices for taste and reward. Cerebral Cortex 15, 1602-1608 (2005)
110. Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD: Images of desire: food-craving activation during fMRI. NeuroImage 23, 1486-1493 (2004)
111. Wang GJ, Volkow ND, Telang F, et al.: Exposure to appetitive food stimuli markedly activates the human brain. NeuroImage 21, 1790-1797 (2004)
112. Grabenhorst F, Rolls ET, Bilderbeck A: How cognition modulates affective responses to taste and flavor: top down influences on the orbitofrontal and pregenual cingulate cortices. Cerebral Cortex (in press 2007)
113. McCabe C, Rolls ET, Bilderbeck A, McGlone F: Cognitive influences on the representation of touch in the human brain. In preparation (2008)
114. Wilson FAW, Rolls ET: The primate amygdala and reinforcement: a dissociation between rule-based and associatively-mediated memory revealed in amygdala neuronal activity. Neuroscience 133, 1061-1072 (2005)
115. Garrow JS (1988): Obesity and Related Diseases. London, Churchill Livingstone
116. Barsh GS, Schwartz MW: Genetic approaches to studying energy balance: perception and integration. Nature Reviews Genetics 3, 589-600 (2002)
117. Cummings DE, Schwartz MW: Genetics and pathophysiology of human obesity. Annual Reviews of Medicine 54, 453-471 (2003)
118. Schwartz MW, Porte D: Diabetes, obesity, and the brain. Science 307, 375-379 (2005)
119. Brownell KD, Fairburn C (1995): Eating Disorders and Obesity: a Comprehensive Handbook. New York, Guildford Press
120. Horvath TL: The hardship of obesity: a soft-wired hypothalamus. Nature Neuroscience 8, 561-565 (2005)
121. Rolls ET: Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiology and Behavior 85, 45-56 (2005)