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  • Review Article
  • Published:

The human orbitofrontal cortex: linking reward to hedonic experience

Nature Reviews Neuroscience volume 6, pages 691–702 (2005)Cite this article

Key Points

  • The prefrontal cortex seems to be essential for the control and organization of behaviour. In particular, it has been linked to the relative cognitive sophistication that has been reached by higher primates, especially humans. However, the functions of one of its constituent regions, the orbitofrontal cortex, have remained enigmatic.

  • In terms of neuroanatomical connectivity, the primate orbitofrontal cortex is uniquely placed to integrate sensory and autonomic information to modulate behaviour through both visceral and motor systems.

  • Recent neuroimaging studies in humans have confirmed the role of the human orbitofrontal cortex as a nexus for sensory integration, modulation of visceral reactions, and participation in learning, prediction and decision making for emotional and reward-related behaviours. But these studies have also shown that the human orbitofrontal cortex is a highly heterogeneous brain region that encompasses many different functions.

  • In particular, the human orbitofrontal cortex has been found to represent not only the reward value and expected reward value of foods and other reinforcers, but also their subjective pleasantness. This link to subjective hedonic processing could provide a basis for further exploration of the brain systems involved in the conscious experience of pleasure and reward, and, as such, offer a unique method for studying the hedonic quality of human experience.

  • Based on the available evidence from neuroimaging and neuropsychology, a tentative new model of the functional neuroanatomy of the orbitofrontal cortex is offered with medial–lateral and posterior–anterior distinctions, in which the implicit reward value is assigned early on in the hierarchy for each type of reinforcer, with a further progression up the processing hierarchy (reflecting the effects of combinations of stimuli) towards areas that are connected to brain regions necessary for conscious hedonic processing.

  • At present, little is known about the functional and structural development of the human orbitofrontal cortex in children and adolescents. However, further investigation of the link to hedonic processing could potentially lead to a better understanding of and novel treatments for disorders linked to anhedonia, such as depression, obesity and eating disorders.

Abstract

Hedonic experience is arguably at the heart of what makes us human. In recent neuroimaging studies of the cortical networks that mediate hedonic experience in the human brain, the orbitofrontal cortex has emerged as the strongest candidate for linking food and other types of reward to hedonic experience. The orbitofrontal cortex is among the least understood regions of the human brain, but has been proposed to be involved in sensory integration, in representing the affective value of reinforcers, and in decision making and expectation. Here, the functional neuroanatomy of the human orbitofrontal cortex is described and a new integrated model of its functions proposed, including a possible role in the mediation of hedonic experience.

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Figure 1: Cytoarchitectonic maps of human and monkey orbitofrontal cortices.
Figure 2: Anatomy, variability and development of the human orbitofrontal cortex.
Figure 3: Meta-analysis of the functions of the orbitofrontal cortex.
Figure 5: Hedonic processing.
Figure 4: Co-activation of the lateral orbitofrontal and anterior cingulate cortices.
Figure 6: A model of orbitofrontal cortex function.

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References

  1. Holland, P. C. & Gallagher, M. Amygdala–frontal interactions and reward expectancy. Curr. Opin. Neurobiol. 14, 148–155 (2004). An excellent recent review of the converging evidence from mammals indicating that reinforcer expectancy is encoded through the interconnections between the basolateral complex of the amygdala and the orbitofrontal cortex.

    CAS  PubMed  Google Scholar 

  2. Cardinal, R. N., Parkinson, J. A., Hall, J. & Everitt, B. J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352 (2002).

    PubMed  Google Scholar 

  3. O'Doherty, J. et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11, 893–897 (2000).

    CAS  PubMed  Google Scholar 

  4. Gottfried, J. A., O'Doherty, J. & Dolan, R. J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104–1107 (2003). A demonstration of how predictive reward value is encoded in the human brain in the orbitofrontal cortex and amygdala.

    CAS  PubMed  Google Scholar 

  5. 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 13, 1064–1071 (2003). A clear demonstration that neural activity in the orbitofrontal cortex is correlated with hedonic experience.

    CAS  PubMed  Google Scholar 

  6. Fuster, J. M. The Prefrontal Cortex (Raven, New York, USA, 1997).

    Google Scholar 

  7. Pandya, D. N. & Yeterian, E. H. Comparison of prefrontal architecture and connections. Phil. Trans. R. Soc. Lond. B 351, 1423–1432 (1996).

    CAS  Google Scholar 

  8. Brodmann, K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues (Barth, Leipzig, Germany, 1909).

    Google Scholar 

  9. Walker, A. E. A cytoarchitectural study of the prefrontal area of the macaque monkey. J. Comp. Neurol. 73, 59–86 (1940).

    Google Scholar 

  10. Petrides, M. & Pandya, D. N. in Handbook of Neuropsychology Vol. 9 (eds Boller, F. & Grafman, J.) 17–58 (Elsevier, Amsterdam, 1994).

    Google Scholar 

  11. Carmichael, S. T. & Price, J. L. Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J. Comp. Neurol. 346, 366–402 (1994).

    CAS  PubMed  Google Scholar 

  12. Chiavaras, M. M. & Petrides, M. Orbitofrontal sulci of the human and macaque monkey brain. J. Comp. Neurol. 422, 35–54 (2000).

    CAS  PubMed  Google Scholar 

  13. Chiavaras, M. M. & Petrides, M. Three-dimensional probabilistic atlas of the human orbitofrontal sulci in standardized stereotaxic space. Neuroimage 13, 479–496 (2001).

    CAS  PubMed  Google Scholar 

  14. Carmichael, S. T. & Price, J. L. Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol. 363, 642–664 (1995).

    CAS  PubMed  Google Scholar 

  15. Barbas, H. Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J. Comp. Neurol. 276, 313–342 (1988).

    CAS  PubMed  Google Scholar 

  16. Amaral, D. G. & Price, J. L. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230, 465–496 (1984).

    CAS  PubMed  Google Scholar 

  17. Carmichael, S. T. & Price, J. L. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 363, 615–641 (1995).

    CAS  PubMed  Google Scholar 

  18. Van Hoesen, G. W., Morecraft, R. J. & Vogt, B. A. in The Neurobiology of the Cingulate Cortex and Limbic Thalamus: A Comprehensive Handbook (eds Vogt, B. A. & Gabriel, M.) 249–284 (Birkhäuser, Boston, USA, 1993).

    Google Scholar 

  19. Öngür, D. & Price, J. L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10, 206–219 (2000).

    PubMed  Google Scholar 

  20. Mesulam, M. -M. & Mufson, E. J. Insula of the old world monkey. III Efferent cortical output and comments on function. J. Comp. Neurol. 212, 38–52 (1982).

    CAS  PubMed  Google Scholar 

  21. Rempel-Clower, N. L. & Barbas, H. Topographic organization of connections between the hypothalamus and prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 398, 393–419 (1998).

    CAS  PubMed  Google Scholar 

  22. Cavada, C., Company, T., Tejedor, J., Cruz Rizzolo, R. J. & Reinoso Suarez, F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb. Cortex 10, 220–242 (2000).

    CAS  PubMed  Google Scholar 

  23. Eblen, F. & Graybiel, A. M. Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J. Neurosci. 15, 5999–6013 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Barbas, H. & Pandya, D. N. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286, 353–375 (1989).

    CAS  PubMed  Google Scholar 

  25. Nauta, W. J. The problem of the frontal lobe: a reinterpretation. J. Psychiatr. Res. 8, 167–187 (1971).

    CAS  PubMed  Google Scholar 

  26. Rolls, E. T. The Brain and Emotion (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  27. Bechara, A., Damasio, A. R., Damasio, H. & Anderson, S. W. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15 (1994). A classic paper showing that patients with lesions to the orbitofrontal and medial prefrontal cortices are impaired at real-life decision making, although they retain otherwise normal intellectual functions.

    CAS  PubMed  Google Scholar 

  28. Kringelbach, M. L. & Rolls, E. T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 72, 341–372 (2004). A review of the functions of the human orbitofrontal cortex, including a large meta-analysis of neuroimaging studies showing that different subregions of the orbitofrontal cortex have different functions.

    PubMed  Google Scholar 

  29. Elliott, R., Dolan, R. J. & Frith, C. D. Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb. Cortex 10, 308–317 (2000).

    CAS  PubMed  Google Scholar 

  30. Dias, R., Robbins, T. & Roberts, A. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69–72 (1996).

    CAS  PubMed  Google Scholar 

  31. Rolls, E. T., Hornak, J., Wade, D. & McGrath, J. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J. Neurol. Neurosurg. Psychiatry 57, 1518–1524 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Iversen, S. D. & Mishkin, M. Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Exp. Brain Res. 11, 376–386 (1970). A classic lesioning study that showed the importance of the lateral orbitofrontal cortex in reversal learning in monkeys.

    CAS  PubMed  Google Scholar 

  33. Hornak, J. et al. Reward-related reversal learning after surgical excisions in orbitofrontal and dorsolateral prefrontal cortex in humans. J. Cogn. Neurosci. 16, 463–478 (2004).

    CAS  PubMed  Google Scholar 

  34. Damasio, A. R. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Phil. Trans. R. Soc. Lond. B 351, 1413–1420 (1996).

    CAS  Google Scholar 

  35. James, W. The Principles of Psychology (Henry Holt, New York, USA, 1890).

    Google Scholar 

  36. Lange, C. G. Über Gemüstbewegungen. (Org. Om Sindsbevægelser) (Theodor Thomas, Leipzig, Germany, 1887).

    Google Scholar 

  37. Cannon, W. B. The James–Lange theory of emotion. Am. J. Psychol. 39, 106–124 (1927).

    Google Scholar 

  38. Craig, A. D. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Rev. Neurosci. 3, 655–666 (2002).

    CAS  Google Scholar 

  39. Wilson, J. et al. Fast, fully automated global and local magnetic field optimization for fMRI of the human brain. Neuroimage 17, 967–976 (2002).

    PubMed  Google Scholar 

  40. Deichmann, R., Josephs, O., Hutton, C., Corfield, D. R. & Turner, R. Compensation of susceptibility-induced BOLD sensitivity losses in echo-planar fMRI imaging. Neuroimage 15, 120–135 (2002).

    CAS  PubMed  Google Scholar 

  41. Frey, S., Kostopoulos, P. & Petrides, M. Orbitofrontal involvement in the processing of unpleasant auditory information. Eur. J. Neurosci. 12, 3709–3712 (2000).

    CAS  PubMed  Google Scholar 

  42. Small, D. M. et al. Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10, 7–14 (1999).

    CAS  PubMed  Google Scholar 

  43. Zatorre, R. J., Jones-Gotman, M., Evans, A. C. & Meyer, E. Functional localization and lateralization of human olfactory cortex. Nature 360, 339–340 (1992).

    CAS  PubMed  Google Scholar 

  44. Rolls, E. T. et al. Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cereb. Cortex 13, 308–317 (2003).

    CAS  PubMed  Google Scholar 

  45. Aharon, I. et al. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 32, 537–551 (2001).

    CAS  PubMed  Google Scholar 

  46. Critchley, H. D., Mathias, C. J. & Dolan, R. J. Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron 33, 653–663 (2002).

    CAS  PubMed  Google Scholar 

  47. Thut, G. et al. Activation of the human brain by monetary reward. Neuroreport 8, 1225–1228 (1997).

    CAS  PubMed  Google Scholar 

  48. O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J. & Andrews, C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nature Neurosci. 4, 95–102 (2001).

    CAS  PubMed  Google Scholar 

  49. Small, D. M., Jones-Gotman, M., Zatorre, R. J., Petrides, M. & Evans, A. C. Flavor processing: more than the sum of its parts. Neuroreport 8, 3913–3917 (1997).

    CAS  PubMed  Google Scholar 

  50. 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. 18, 2059–2068 (2003).

    PubMed  Google Scholar 

  51. Rolls, B. J., Rolls, E. T., Rowe, E. A. & Sweeney, K. Sensory specific satiety in man. Physiol. Behav. 27, 137–142 (1981).

    CAS  PubMed  Google Scholar 

  52. Butter, C. M., Mishkin, M. & Rosvold, H. E. Conditioning and extinction of a food-rewarded response after selective ablations of frontal cortex in rhesus monkeys. Exp. Neurol. 7, 65–75 (1963).

    CAS  PubMed  Google Scholar 

  53. Baylis, L. L. & Gaffan, D. Amygdalectomy and ventromedial prefrontal ablation produce similar deficits in food choice and in simple object discrimination learning for an unseen reward. Exp. Brain Res. 86, 617–622 (1991).

    CAS  PubMed  Google Scholar 

  54. Baxter, M. G., Parker, A., Lindner, C. C., Izquierdo, A. D. & Murray, E. A. Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. J. Neurosci. 20, 4311–4319 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Rahman, S., Sahakian, B. J., Hodges, J. R., Rogers, R. D. & Robbins, T. W. Specific cognitive deficits in mild frontal variant frontotemporal dementia. Brain 122, 1469–1493 (1999).

    PubMed  Google Scholar 

  56. Farrow, T. F. et al. Investigating the functional anatomy of empathy and forgiveness. Neuroreport 12, 2433–2438 (2001).

    CAS  PubMed  Google Scholar 

  57. Blood, A. J., Zatorre, R. J., Bermudez, P. & Evans, A. C. Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nature Neurosci. 2, 382–387 (1999).

    CAS  PubMed  Google Scholar 

  58. Rozin, P. in International Encyclopedia of the Social & Behavioral Sciences (eds Smelser, N. J. & Baltes, P. B.) 5719–5722 (Elsevier, Amsterdam, 2001).

    Google Scholar 

  59. Harlow, J. M. Passage of an iron rod through the head. Boston Med. Surg. J. 39, 389–393 (1848).

    Google Scholar 

  60. Macmillan, M. An Odd Kind of Fame: Stories of Phineas Gage (MIT Press, Cambridge, Massachusetts, 2000).

    Google Scholar 

  61. Blair, R. J. & Cipolotti, L. Impaired social response reversal. A case of 'acquired sociopathy'. Brain 123, 1122–1141 (2000).

    PubMed  Google Scholar 

  62. Anderson, S. W., Bechara, A., Damasio, H., Tranel, D. & Damasio, A. R. Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nature Neurosci. 2, 1032–1037 (1999).

    CAS  PubMed  Google Scholar 

  63. Hornak, J. et al. Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. Brain 126, 1671–1712 (2003). Strong evidence from surgically circumscribed lesions in humans showing that the orbitofrontal and medial prefrontal cortices are involved in emotion identification, social behaviour and subjective emotional state.

    Google Scholar 

  64. Hornak, J., Rolls, E. T. & Wade, D. Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia 34, 247–261 (1996).

    CAS  PubMed  Google Scholar 

  65. Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).

    CAS  PubMed  Google Scholar 

  66. Bechara, A., Damasio, H., Tranel, D. & Anderson, S. W. Dissociation of working memory from decision making within the human prefrontal cortex. J. Neurosci. 18, 428–437 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Maia, T. V. & McLelland, J. L. A reexamination of the evidence for the somatic marker hypothesis: what participants really know in the Iowa gambling task. Proc. Natl Acad. Sci. USA 101, 16075–16080 (2004).

    CAS  PubMed  Google Scholar 

  68. Rogers, R. D. et al. Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J. Neurosci. 19, 9029–9038 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Rolls, E. T., Kringelbach, M. L. & de Araujo, I. E. T. Different representations of pleasant and unpleasant odors in the human brain. Eur. J. Neurosci. 18, 695–703 (2003).

    PubMed  Google Scholar 

  70. Anderson, A. K. et al. Dissociated neural representations of intensity and valence in human olfaction. Nature Neurosci. 6, 196–202 (2003).

    CAS  PubMed  Google Scholar 

  71. Small, D. M. et al. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39, 701–711 (2003).

    CAS  PubMed  Google Scholar 

  72. Schnider, A. & Ptak, R. Spontaneous confabulators fail to suppress currently irrelevant memory traces. Nature Neurosci. 2, 677–681 (1999).

    CAS  PubMed  Google Scholar 

  73. Schnider, A. Spontaneous confabulation and the adaptation of thought to ongoing reality. Nature Rev. Neurosci. 4, 662–671 (2003). A fascinating review article that links the medial orbitofrontal cortex to spontaneous confabulation in patients and proposes that this region might serve to adapt to ongoing reality.

    CAS  Google Scholar 

  74. Schnider, A., Treyer, V. & Buck, A. The human orbitofrontal cortex monitors outcomes even when no reward is at stake. Neuropsychologia 43, 316–323 (2005).

    PubMed  Google Scholar 

  75. Petrovic, P., Kalso, E., Petersson, K. M. & Ingvar, M. Placebo and opioid analgesia — imaging a shared neuronal network. Science 295, 1737–1740 (2002). An elegant demonstration of placebo mechanisms in the human brain in which the pain relief in placebo-responders is correlated with activity in lateral orbitofrontal and anterior cingulate cortices.

    CAS  PubMed  Google Scholar 

  76. Petrovic, P. & Ingvar, M. Imaging cognitive modulation of pain processing. Pain 95, 1–5 (2002).

    PubMed  Google Scholar 

  77. Nobre, A. C., Coull, J. T., Frith, C. D. & Mesulam, M. M. Orbitofrontal cortex is activated during breaches of expectation in tasks of visual attention. Nature Neurosci. 2, 11–12 (1999).

    CAS  PubMed  Google Scholar 

  78. Kringelbach, M. L. & Rolls, E. T. Neural correlates of rapid context-dependent reversal learning in a simple model of human social interaction. Neuroimage 20, 1371–1383 (2003).

    PubMed  Google Scholar 

  79. Kringelbach, M. L. Learning to change. PLoS Biol. 2, E140 (2004).

    PubMed  PubMed Central  Google Scholar 

  80. Blair, R. J., Morris, J. S., Frith, C. D., Perrett, D. I. & Dolan, R. J. Dissociable neural responses to facial expressions of sadness and anger. Brain 122, 883–893 (1999).

    PubMed  Google Scholar 

  81. Walton, M. E., Devlin, J. T. & Rushworth, M. F. Interactions between decision making and performance monitoring within prefrontal cortex. Nature Neurosci. 7, 1259–1265 (2004). An important paper that demonstrates the central role played by the orbitofrontal and anterior cingulate cortices in decision making.

    CAS  PubMed  Google Scholar 

  82. Ullsperger, M. & von Cramon, D. Y. Decision making, performance and outcome monitoring in frontal cortical areas. Nature Neurosci. 7, 1173–1174 (2004).

    CAS  PubMed  Google Scholar 

  83. Chalmers, D. Facing up to the problem of consciousness. J. Conscious. Stud. 2, 200–219 (1995).

    Google Scholar 

  84. Hull, C. L. Essentials of Behavior (Yale Univ. Press, New Haven, Connecticut, USA, 1951).

    Google Scholar 

  85. Bindra, D. How adaptive behavior is produced: a perceptual–motivational alternative to response-reinforcement. Behav. Brain Sci. 1, 41–91 (1978).

    Google Scholar 

  86. Cabanac, M. Physiological role of pleasure. Science 173, 1103–1107 (1971).

    CAS  PubMed  Google Scholar 

  87. Berridge, K. C. Food reward: brain substrates of wanting and liking. Neurosci. Biobehav. Rev. 20, 1–25 (1996).

    CAS  PubMed  Google Scholar 

  88. Berridge, K. C. & Robinson, T. E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. 28, 309–369 (1998).

    CAS  PubMed  Google Scholar 

  89. Kringelbach, M. L. Food for thought: hedonic experience beyond homeostasis in the human brain. Neuroscience 126, 807–819 (2004).

    CAS  PubMed  Google Scholar 

  90. Saper, C. B., Chou, T. C. & Elmquist, J. K. The need to feed: homeostatic and hedonic control of eating. Neuron 36, 199–211 (2002).

    CAS  PubMed  Google Scholar 

  91. 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 13, 1064–1071 (2003).

    CAS  PubMed  Google Scholar 

  92. Hinton, E. C. et al. Neural contributions to the motivational control of appetite in humans. Eur. J. Neurosci. 20, 1411–1418 (2004). Demonstrates that the extrinsic incentive value of foods is located in mid-anterior parts of the orbitofrontal cortex.

    PubMed  Google Scholar 

  93. De Araujo, I. E. T., Kringelbach, M. L., Rolls, E. T. & Hobden, P. The representation of umami taste in the human brain. J. Neurophysiol. 90, 313–319 (2003). Shows that the subjective synergistic enhancement of umami taste is represented in mid-anterior parts of the orbitofrontal cortex.

    CAS  PubMed  Google Scholar 

  94. De Araujo, I. E. T., Kringelbach, M. L., Rolls, E. T. & McGlone, F. Human cortical responses to water in the mouth, and the effects of thirst. J. Neurophysiol. 90, 1865–1876 (2003).

    PubMed  Google Scholar 

  95. 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 124, 1720–1733 (2001).

    CAS  PubMed  Google Scholar 

  96. De Araujo, I. E. & Rolls, E. T. Representation in the human brain of food texture and oral fat. J. Neurosci. 24, 3086–3093 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Craig, A. D., Chen, K., Bandy, D. & Reiman, E. M. Thermosensory activation of insular cortex. Nature Neurosci. 3, 184–190 (2000).

    CAS  PubMed  Google Scholar 

  98. Völlm, B. A. et al. Methamphetamine activates reward circuitry in drug naïve human subjects. Neuropsychopharmacology 29, 1715–1722 (2004).

    PubMed  Google Scholar 

  99. Blood, A. J. & Zatorre, R. J. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc. Natl Acad. Sci. USA 98, 11818–11823 (2001).

    CAS  PubMed  Google Scholar 

  100. Hornak, J. et al. Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. Brain 126, 1671–1712 (2003).

    Google Scholar 

  101. Drevets, W. C. Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders. Curr. Opin. Neurobiol. 11, 240–249 (2001).

    CAS  PubMed  Google Scholar 

  102. Volkow, N. D. & Li, T. K. Drug addiction: the neurobiology of behaviour gone awry. Nature Rev. Neurosci. 5, 963–970 (2004).

    CAS  Google Scholar 

  103. Dehaene, S., Kerszberg, M. & Changeux, J. P. A neuronal model of a global workspace in effortful cognitive tasks. Proc. Natl Acad. Sci. USA 95, 14529–14534 (1998).

    CAS  PubMed  Google Scholar 

  104. Gusnard, D. A. & Raichle, M. E. Searching for a baseline: functional imaging and the resting human brain. Nature Rev. Neurosci. 2, 685–694 (2001).

    CAS  Google Scholar 

  105. Granger, C. W. J. Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37, 424–438 (1969).

    Google Scholar 

  106. Dehaene, S. et al. Cerebral mechanisms of word masking and unconscious repetition priming. Nature Neurosci. 4, 752–758 (2001).

    CAS  PubMed  Google Scholar 

  107. Eslinger, P. J., Flaherty-Craig, C. V. & Benton, A. L. Developmental outcomes after early prefrontal cortex damage. Brain Cogn. 55, 84–103 (2004).

    PubMed  Google Scholar 

  108. Uylings, H. B. & van Eden, C. G. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog. Brain Res. 85, 31–62 (1990).

    CAS  PubMed  Google Scholar 

  109. Öngür, D. & Price, J. L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10, 206–219 (2000). An important paper proposing that, on neuroanatomical grounds, the orbitofrontal cortex should be considered along with the medial prefrontal cortex as a crucial sensory–visceromotor link for consummatory behaviours.

    PubMed  Google Scholar 

  110. Papez, J. Comparative Neurology (Crowell, New York, 1929).

    Google Scholar 

  111. Brodmann, K. Neue Ergebnisse ueber die Vergleichende histologische Localisation der Grosshirnfinde mit besonderer Berucksichtigung des Stirnhirns. Anat. Anz. Suppl. 41, 157–216 (1912).

    Google Scholar 

  112. Passingham, R. E. The Human Primate (W. H. Freeman, Oxford, 1982).

    Google Scholar 

  113. Schoenbaum, G. & Setlow, B. Integrating orbitofrontal cortex into prefrontal theory: common processing themes across species and subdivisions. Learn. Mem. 8, 134–147 (2001).

    CAS  PubMed  Google Scholar 

  114. Darwin, C. The Expression of the Emotions in Man and Animals (Univ. Chicago Press, Chicago, 1872).

    Google Scholar 

  115. Kringelbach, M. L. in The Oxford Companion to the Mind 2nd edn (ed. Gregory, R. L.) 287–290 (Oxford Univ. Press, Oxford, 2004).

    Google Scholar 

  116. Weiskrantz, L. in Analysis of Behavioural Change (ed. Weiskrantz, L.) 50–90 (Harper and Row, New York/London, 1968).

    Google Scholar 

  117. Gogtay, N. et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl Acad. Sci. USA 101, 8174–8179 (2004).

    CAS  PubMed  Google Scholar 

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Acknowledgements

This research is supported by the Wellcome Trust and the Medical Research Council (to the Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB)).

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Authors and Affiliations

  1. University of Oxford, University Laboratory of Physiology, Parks Road, Oxford, OX1 3PT, UK

    Morten L. Kringelbach

  2. FMRIB, Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, John Radcliffe Hospital, Headley Way, Oxford, OX3 9DU, UK

    Morten L. Kringelbach

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FURTHER INFORMATION

Kringelbach's homepage

Glossary

REINFORCERS

Positive reinforcers (rewards) increase the frequency of behaviour that leads to their acquisition. Negative reinforcers (punishers) decrease the frequency of behaviour that leads to their encounter and increase the frequency of behaviour that leads to their avoidance.

BRODMANN'S AREAS

(BA). Korbinian Brodmann (1868–1918) was an anatomist who divided the cerebral cortex into numbered subdivisions on the basis of cell arrangements, types and staining properties (for example, the dorsolateral prefrontal cortex contains several subdivisions, including BA 46 and BA 9). Modern derivatives of Brodmann's maps are commonly used as the reference system for the discussion of brain-imaging findings.

GOAL-DIRECTED BEHAVIOUR

Behaviour directed towards the attainment of a future state (for example, obtaining the next meal).

VENTROMEDIAL PREFRONTAL CORTEX

An anatomical term that refers to most of the medial orbitofrontal cortex and areas on the medial wall, but not to more central and lateral regions of the orbitofrontal cortex.

RESPONSE INHIBITION

Lack of control and general perseveration are symptoms that commonly follow damage to the frontal lobes, and have often been ascribed to a lack of inhibitory control over the appropriate responses.

REVERSAL LEARNING

Describes a task in which participants are trained to respond differentially to two stimuli under conditions of reward and punishment (or non-reward), and subsequently have to learn to change their behaviour when the reward values are reversed (that is, when the previously rewarded stimulus is no longer rewarded, and vice versa).

JAMES–LANGE THEORY

Two nineteenth-century scholars, William James and Carl Lange, independently proposed that emotions arise as a result of bodily physiological events, such as increases in heart rate, rather than being the cause of them

SELECTIVE SATIETY

A form of reinforcer devaluation in which participants that have been fed to satiety on one food still find other foods rewarding, and will eat some of these other foods. Selective satiety is particularly useful for studying affective representation in the brain, because it provides a means of altering the affective value of a stimulus without modifying its physical attributes, allowing a change in reward value to be detected.

CO-ACTIVATION

The presence, in a neuroimaging experiment, of significant activity in two brain structures in the same subtraction.

TRUE TASTE SYNERGISM

The combined effect of two taste stimuli, when greater than the sum of the effects of each one present alone.

MULTIMODAL INTEGRATION

The process of combining information from different sensory modalities.

MAGNETOENCEPHALOGRAPHY

(MEG). A non-invasive technique that allows the detection of the changing magnetic fields that are associated with brain activity on the timescale of milliseconds.

GRANGER CAUSALITY

A technique for determining whether one time series is useful in predicting another.

ANHEDONIA

Loss of interest or pleasure in almost all activities.

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Kringelbach, M. The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 6, 691–702 (2005). https://doi.org/10.1038/nrn1747

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