Disgust: Sensory affect or primary emotional system?

Cognition and Emotion

Volumn 21, Issue 8, 2007, Pages 1799-1818

  Toronchuk, Judith A ^a   Ellis, George F R ^b  

^a TRINITY WESTERN UNIVERSITY   (Canada)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

AROUSAL; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BEHAVIOR; BRAIN FUNCTION; COGNITION; ELECTROSTIMULATION; EMOTION; HUMAN; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SENSORY SYSTEM; STIMULUS RESPONSE; TASTE AVERSION; THEORY;

EID: 36248970644     PISSN: 02699931     EISSN: 14640600     Source Type: Journal    
DOI: 10.1080/02699930701298515     Document Type: Article

References (107)

1. Adolphs, R., Tranel, D., Koenigs, M. and Damasio, A. R. (2005) Preferring one taste over another without recognising either. Nature Neuroscience, 8, pp. 860-861.
2. Alvarez-Borda, B., Ramirez-Amaya, V., Perez-Montfort, R. and Bermudez-Rattoni, F. (1995) Enhancement of antibody production by a learning paradigm. Neurobiology of Learning & Memory, 64:2, pp. 103-105.
3. Bechara, A. and Damasio, A. (2005) The somatic marker hypothesis: A neural theory of economic decision. Games and Economic Behavior, 52, pp. 336-372.
4. Berman, D. E., Hazvi, S., Neduva, V. and Dudai, Y. (2000) The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: Activation of ERK1-2 and formation of a memory trace. The Journal of Neuroscience, 20, pp. 7017-7023.
5. Bermudez-Rattoni, F. (2004) Molecular mechanisms of taste recognition memory. Nature Reviews: Neuroscience, 5, pp. 209-217.
6. Bermudez-Rattoni, F., Grijalva, C. V., Kiefer, S. W. and Garcia, J. &. (1986) Flavor-illness aversions: The role of the amygdala in the acquisition of taste-potentiated odor aversions. Physiological Behavior, 384, pp. 503-508.
7. Bernstein, I. L. (1999) Taste aversion learning: A contemporary perspective. Nutrition, 15, pp. 229-234.
8. Burgdorf, J. and Panksepp, J. P. (2006) The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews, 30, pp. 173-187.
9. Calder, A. J., Keane, J., Manes, F., Antoun, N. and Young, A. W. (2000) Impaired recognition and experience of disgust following brain injury. Nature Neuroscience, 3, pp. 1077-1078.
10. Carew, T. J. and Sahley, C. L. (1986) Invertebrate learning and memory: From behaviour to molecules. Annual Review of Neuroscience, 9, pp. 435-487.
11. Cechetto, D. F. and Saper, C. B. (1987) Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. Journal of Comparative Neurology, 262, pp. 27-45.
12. Craig, A. D. (2002) How do you feel? Interoception: The sense of the physiological condition of the body. Nature Reviews: Neuroscience, 3, pp. 655-666.
13. Craig, A. D. (2003) Interoception: The sense of the physiological condition of the body. Current Opinion in Neurobiology, 13, pp. 500-505.
14. Craig, A. D. (2005) Forebrain emotional asymmetry: A neuroanatomical basis?. Trends in Cognitive Sciences, 9, pp. 566-571.
15. Critchley, H. D. and Rolls, E. T. (1996) Olfactory neural responses in the primate orbitofrontal cortex: Analysis in an olfactory discrimination task. Journal of Neurophysiology, 75, pp. 1659-1672.
16. Critchley, H. D., Rotshtein, P., Nagai, Y., O'Doherty, J., Mathias, C. J. and Dolan, R. J. (2005) Activity in the human brain predicting differential heart rate responses to emotional facial expressions. NeuroImage, 24, pp. 751-762.
17. Critchley, H. D., Wiens, S., Rotshtein, P., Öhman, A. and Dolan, R. J. (2004) Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, pp. 189-195.
18. Curtis, V., Aunger, R. and Rabie, T. (2004) Evidence that disgust evolved to protect from risk of disease. Proceedings of the Royal Society of London. Series B. Biological Sciences, 271, pp. 131-133.
19. Curtis, V. A. and Biran, A. (2001) Dirt, disgust and disease: Is hygiene in our genes?. Perspectives in Biology and Medicine, 44, pp. 17-31.
20. Damasio, A. R. (1999) The feeling of what happens: Body and emotion in the making of consciousness, Harcourt, New York
21. Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto, L. L. and Parvizi, J. (2000) Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience, 3, pp. 1049-1056.
22. de Araujo, I. E. T., Rolls, E. T., Kringelbach, M. L., McGlone, F. and Phillips, N. (2003) Taste-olfactory convergence and the representation of the pleasantness of flavour, in the human brain. European Journal of Neuroscience, 18, pp. 2059-2068.
23. Domjan, M. (2005) Pavlovian conditioning: A functional perspective. Annual Review of Psychology, 56, pp. 179-206.
24. Dunn, B. D., Dalgleish, T. and Lawrence, A. D. (2006) The somatic marker hypothesis: A critical evaluation. Neuroscience & Biobehavioral Reviews, 30, pp. 239-271.
25. Egan, G., Silk, T., Zamarripa, F., Williams, J., Federico, P. and Cunnington, R. (2003) Neural correlates of the emergence of consciousness of thirst. Proceedings of the National Academy of Science, USA, 100, pp. 15241-15246.
26. Ekman, P. and Friesen, W. V. (1986) A new pan-cultural facial expression of emotion. Motivation and Emotion, 10, pp. 159-168.
27. Ellis, G. F. R. and Toronchuk, J. A. (2005) Neural development: Affective and immune system influences. Consciousness and emotion: Agency, conscious choice and selective perception, pp. 81-119. John Benjamins, Philadelphia, PA
28. Fitzgerald, D. A., Posse, S., Moore, G. J., Tancer, M. E., Nathan, P. J. and Phan, K. L. (2004) Neural correlates of internally generated disgust via autobiographical recall: A functional magnetic resonance imaging investigation. Neuroscience Letters, 370, pp. 91-96.
29. Flynn, F. G., Benson, D. F. and Ardila, A. (1999) Anatomy of the insula - Functional and clinical correlates. Aphasiology, 13, pp. 55-78.
30. Galati, D., Scherer, K. R. and Ricci-Bitti, P. E. (1997) Voluntary facial expression of emotion: Comparing congenitally blind with normally sighted encoders. Journal of Personality and Social Psychology, 73, pp. 1363-1379.
31. Gallese, V., Keysers, C. and Rizzolatti, G. (2004) A unifying view of the basis of social cognition. Trends in Cognitive Science, 8, pp. 396-404.
32. Garcia, J., Hankins, W. G. and Rusiniak, K. W. (1974) Behavioral regulation of the milieu interne in man and rat. Science, 185, pp. 824-831.
33. Garcia, J., Quick, D. F. and White, B. (1984) Conditioning disgust and fear from mollusk to monkey. Primary neural substrates of learning and behavioral change, pp. 47-61. Cambridge University Press, Cambridge, UK
34. Goldman, A. I. and Sripada, C. S. (2005) Simulationist models of face-based emotion recognition. Cognition, 94, pp. 193-213.
35. Gottfried, J. A. and Zald, D. H. (2005) On the scent of human olfactory orbitofrontal cortex: Meta-analysis and comparison to non-primates. Brain Research Reviews, 50, pp. 287-304.
36. Heimer, L. and Van Hoesen, G. W. (2006) The limbic lobe and its output channels: Implications for emotional functions and adaptive behaviour. Neuroscience and Biobehavioral Reviews, 30, pp. 126-147.
37. Hennenlotter, A., Schroeder, U., Erhard, P., Haslinger, B., Stahl, R. and Weindl, A. (2004) Neural correlates associated with impaired disgust processing in pre-symptomatic Huntington's disease. Brain, 127, pp. 1446-1453.
38. Hornby, P. J. (2001) Central neurocircuitry associated with emesis. The American Journal of Medicine, 111, p. 106S.
39. Horton, J. and Ratcliffe, N. A. (2001) Immunology, Mosby, Toronto, Canada
40. Hosie, J. A., Gray, C. D., Russell, P. A., Scott, C. and Hunter, N. (1998) The matching of facial expressions by deaf and hearing children and their production and comprehension of emotion labels. Motivation and Emotion, 22, pp. 293-313.
41. Kiefer, S. W. and Orr, M. R. (1992) Taste avoidance, but not aversion, learning in rats lacking gustatory cortex. Behavioral Neuroscience, 106, pp. 140-146.
42. Koh, M. T. and Bernstein, I. L. (2005) Mapping conditioned taste aversion associations using c-Fos reveals a dynamic role for insular cortex. Behavioral Neuroscience, 1192, pp. 388-398.
43. Krolak-Salmon, P., Henaff, M. -A., Isnard, J., Tallon-Baudry, C., Guenot, M. and Vighetto, A. (2003) An attention modulated response to disgust in human ventral anterior insula. Annuals of Neurology, 53, pp. 446-453.
44. Lane, R. D., Reiman, E. M., Ahern, G. L., Schwartz, G. E. and Davidson, R. J. (1997) Neuroanatomical correlates of happiness, sadness, and disgust. The American Journal of Psychiatry, 154, pp. 926-933.
45. Lasiter, P. S., Deems, D. A., Oetting, R. L. and Garcia, J. (1985) Taste discriminations in rats lacking anterior insular gustatory neocortex. Physiological Behavior, 352, pp. 277-285.
46. Lawes, I. N. (1990) The origin of the vomiting response: A neuroanatomical hypothesis. Canadian Journal of Physiological Pharmacology, 682, pp. 254-259.
47. Lawrence, A. D. and Calder, A. J. (2004) Homologizing human emotions. Emotion, evolution and rationality, pp. 15-47. Oxford University Press, Oxford, UK
48. Lazar, S. W., Kerr, C. E., Wasserman, R. H., Gray, J. R., Greved, G. N. and Treadway, M. T. (2005) Meditation experience is associated with increased cortical thickness. Neuroreport, 16, pp. 1893-1897.
49. Levenson, R. W., Ekman, P. and Friesen, W. V. (1990) Voluntary facial action generates emotion-specific autonomic nervous system activity. Psychophysiology, 27, pp. 363-384.
50. Liotti, M., Mayberg, H. S., Brannan, S. K., McGinnis, S., Jerabek, P. and Fox, P. T. (2000) Differential limbic-cortical correlates of sadness and anxiety in healthy subjects: Implications for affective disorders. Biological Psychiatry, 48, pp. 30-42.
51. Lundy, R. F. and Norgren, R. (2004) Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. Journal of Neurophysiology, 91, pp. 1143-1157.
52. Mesulam, M. -M. and Mufson, E. J. (1982) Insula of the old world monkey. III: Efferent cortical output and comments on function. Journal of Comparative Neurology, 212, pp. 38-52.
53. Miller, S. B. (2004) Disgust: The gatekeeper emotion, Atlantic Press, Hillsdale, NJ
54. Miller, W. I. (1997) The anatomy of disgust, Harvard University Press, Cambridge, MA
55. Miranda, M. I., Ferreira, G., Ramirez-Lugo, L. and Bermudez-Rattoni, F. (2002) Glutamatergic activity in the amygdala signals visceral input during taste memory formation. Proceeding of the National Academy of Science, USA, 99, pp. 11417-11422.
56. Moll, J., Oliveira-Souza, R., Eslinger, P. J., Bramati, I. E., Mourao-Miranda, J. and Andreiuolo, P. A. (2002) The neural correlates of moral sensitivity: A functional magnetic resonance imaging investigation of basic and moral emotions. The Journal of Neuroscience, 22, pp. 2730-2736.
57. Morris, J. S., Friston, K. J., Büchel, C., Frith, C. D., Young, A. W. and Calder, A. J. (1998) A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain, 121, pp. 47-57.
58. Mufson, E. J., Mesulam, M. M. and Pandya, D. N. (1981) Insular interconnections with the amygdala in the Rhesus monkey. Neuroscience, 6, pp. 1231-1248.
59. Nimchinsky, E. A., Gilissen, E., Allman, J. M., Perl, D. P., Erwin, J. M. and Hof, P. R. (1999) A neuronal morphologic type unique to humans and great apes. Proceeding of the National Academy of Sciences, USA, 96, pp. 5268-5273.
60. O'Doherty, J., Rolls, E. T., Francis, S., Bowtell, R. and McGlone, F. (2001) The representation of pleasant and aversive taste in the human brain. Journal of Neurophysiology, 85, pp. 1315-1321.
61. Öhman, A. and Mineka, S. (2001) Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychological Review, 108, pp. 483-522.
62. Ortony, A. and Turner, T. J. (1990) What's basic about basic emotions?. Psychological Review, 97, pp. 315-331.
63. Pacheco-López, G., Niemi, M. -B., Kou, W., Härting, M., Rey, A. Del and Besedovsky, H. O. (2004) Behavioral endocrine immune conditioned response is induced by taste and superantigen pairing. Neuroscience, 129, pp. 555-562.
64. Panksepp, J. (1998) Affective neuroscience: The foundations of human and animal emotions, Oxford University Press, London
65. Panksepp, J. (2000) The handbook of emotions, pp. 137-156. Guilford Press, New York
66. Panksepp, J. (2005) Affective consciousness: Core emotional feelings in animals and humans. Consciousness and Cognition, 14, pp. 30-80.
67. Parker, L. A. (2003) Taste avoidance and taste aversion: Evidence for two different processes. Learning & Behavior, 312, pp. 165-172.
68. Paulus, M. P., Rogalsky, C., Simmons, A., Feinstein, J. S. and Stein, M. B. (2003) Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. NeuroImage, 19, pp. 1439-1448.
69. Pelchat, M. L., Grill, H. J., Rozin, P. and Jacobs, J. (1983) Quality of acquired responses to tastes by Rattus norvegicus depends on types of associated discomfort. Journal of Comparative Psychology, 97, pp. 140-153.
70. Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrew, C. and Calder, A. J. (1997) A specific neural substrate for perceiving facial expressions of disgust. Nature, 389, pp. 495-498.
71. Ramirez-Amaya, V., Alvarez-Borda, B. and Bermudez-Rattoni, F. (1998) Differential effects of NMDA-induced lesions into the insular cortex and amygdala on the acquisition and evocation of conditioned immunosuppression. Brain, Behavior, and Immunity, 12, pp. 149-160.
72. Ramirez-Amaya, V. and Bermudez-Rattoni, F. (1999) Conditioned enhancement of antibody production is disrupted by insular cortex and amygdala but not hippocampal lesions. Brain, Behavior, and Immunity, 13, pp. 46-60.
73. Ritz, T., Thons, M., Fahrenkrug, S. and Dahme, B. (2005) Airways, respiration, and respiratory sinus arrhythmia during picture viewing. Psychophysiology, 42, pp. 568-578.
74. Rolls, E. T. (1989) Information processing in the taste system of primates. Journal of Experimental Biology, 146, pp. 141-164.
75. Rolls, E. T. (2005) Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiology & Behavior, 85, pp. 45-56.
76. Rolls, E. T. (2005) Emotions explained, Oxford University Press, Oxford, UK
77. Royet, J. -P., Plailly, J., Delon-Martin, C., Kareken, D. A. and Segebarth, C. (2003) fMRI of emotional responses to odors: Influence of hedonic valence and judgment, handedness, and gender. NeuroImage, 20, pp. 713-728.
78. Rozin, P. and Fallon, A. E. (1987) A perspective on disgust. Psychological Review, 94, pp. 23-41.
79. Rozin, P., Haidt, J. and McCauley, C. R. (1999) The handbook of cognition and emotion, pp. 429-445. Wiley, Chichester, UK
80. Rozin, P. and Kalat, J. W. (1971) Specific hungers and poison avoidance as adaptive specializations of learning. Psychological Review, 78, pp. 459-486.
81. Rubio-Godoy, M., Aunger, R. and Curtis, V. (2007) Serotonin - A link between disgust and immunity?. Medical Hypotheses, 68, pp. 61-66.
82. Sanfey, A. G., Rilling, J. K., Aronson, J. A., Nystrom, L. E. and Cohen, J. D. (2003) The neural basis of economic decision-making in the ultimatum game. Science, 300, pp. 1755-1758.
83. Saper, C. B. (2002) The central autonomic nervous system: Conscious visceral perception and autonomic pattern generation. Annual Review of Neuroscience, 25, pp. 433-469.
84. Schafer, A., Schienle, A. and Vaitl, D. (2005) Stimulus type and design influence hemodynamic responses towards visual disgust and fear elicitors. International Journal of Psychophysiology, 57, pp. 53-59.
85. Schienle, A., Schafer, A., Stark, R., Walter, B. and Vaitl, D. (2005) Relationship between disgust sensitivity, trait anxiety and brain activity during disgust induction. Neuropsychobiology, 51, pp. 86-92.
86. Schienle, A., Stark, R., Walter, B., Blecker, C., Ott, U. and Kirsch, P. (2002) The insula is not specifically involved in disgust processing: An fMRI study. Neuroreport, 13, pp. 2023-2026.
87. Shapira, N. A., Liu, Y., He, A. G., Bradley, M. M., Lessig, M. C. and James, G. A. (2003) Brain activation by disgust-inducing pictures in obsessive-compulsive disorder. Biological Psychiatry, 54, pp. 751-756.
88. Simmons, A., Mathews, S. C., Stein, M. B. and Paulus, M. P. (2004) Anticipation of emotionally aversive visual stimuli activates right insula. Neuroreport, 15, pp. 2261-2265.
89. Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J. and Frith, C. D. (2004) Empathy for pain involves the affective but not sensory components of pain. Science, 303, pp. 1157-1162.
90. Singer, T., Seymour, B., O'Doherty, J. P., Stephan, K. E., Dolan, R. J. and Frith, C. D. (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature, 439, pp. 466-469.
91. Small, D. M., Gregory, M. D., Mak, Y. E., Gitelman, D., Mesulam, M. M. and Parrish, T. (2003) Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron, 39, pp. 701-711.
92. Small, D. M., Zarotte, R. J., Dagher, A., Evans, A. C. and Jones-Gotman, M. (2001) Changes in brain activity related to eating chocolate: From pleasure to aversion. Brain, 124, pp. 1720-1733.
93. Spector, A. C. (2000) Linking gustatory neurobiology to behavior in vertebrates. Neuroscience and Biobehavioral Reviews, 24, pp. 391-416.
94. Sprengelmeyer, R., Young, A. W., Calder, A. J., Karnat, A., Lange, H. and Hömberg, V. (1996) Loss of disgust: Perception of faces and emotions in Huntington's disease. Brain: A Journal of Neurology, 119, pp. 1647-1665.
95. Sprengelmeyer, R., Young, A. W., Mahn, K., Schroeder, U., Woitalla, D. and Büttner, T. (2003) Facial expression recognition in people with medicated and unmedicated Parkinson's disease. Neuropsychologia, 41, pp. 1047-1057.
96. Sprengelmeyer, R., Young, A. W., Pundt, I., Sprengelmeyer, A., Calder, A. J. and Berrios, G. (1997) Disgust implicated in obsessive-compulsive disorder. Proceedings of the Royal Society of London. Series B. Biological Sciences, 264, pp. 1767-1773.
97. Stark, R., Walter, B., Schienle, A. and Vaitl, D. (2005) Psychophysiological correlates of disgust and disgust sensitivity. Journal of Psychophysiology, 19, pp. 50-60.
98. Steiner, J. E., Glaser, D., Hawilo, M. E. and Berridge, K. C. (2001) Comparative expression of hedonic impact: Affective reactions to taste by human infants and other primates. Neuroscience and Biobehavioral Reviews, 25, pp. 53-74.
99. Stevenson, R. J. and Repacholi, B. M. (2005) Does the source of an interpersonal odour affect disgust? A disease risk model and its alternatives. European Journal of Social Psychology, 35, pp. 375-401.
100. Stoléru, S., Grégoire, M. -C., Gérard, D., Decety, J., Lafarge, E. and Cinotti, L. (1999) Neuroanatomical correlates of visually evoked sexual arousal in human males. Archives of Sexual Behavior, 28, pp. 1-21.
101. Sugai, R., Shiga, S., Azami, S., Watanabe, T., Sadamoto, H. and Fujito, Y. (2006) Taste discrimination in conditioned taste aversion of the pond snail Lymnaea stagnalis. The Journal of Experimental Biology, 209, pp. 826-833.
102. Tataranni, P. A., Gautier, J. F., Chen, K., Uecker, P. A., Bandy, D. and Salbe, A. D. (1999) Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proceedings of the National Academy of Sciences, USA, 96, pp. 4569-4574.
103. Toronchuk, J. A. and Ellis, G. F. R. (2006) Affective neuronal Darwinism: The nature of the primary emotional systems
104. Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V. and Rizzolatti, G. (2003) Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron, 40, pp. 655-664.
105. Wolf, K., Mass, R., Ingenbleek, T., Kiefer, F., Naber, D. and Wiedemann, K. (2005) The facial pattern of disgust, appetence, excited joy and relaxed joy: An improved facial EMG study. Scandinavian Journal of Psychology, 46, pp. 403-409.
106. Yasui, Y., Breder, C. D., Saper, C. B. and Cechetto, D. F. (1991) Autonomic responses and efferent pathways from the insular cortex in the rat. Journal of Comparative Neurology, 303, pp. 355-374.
107. Zhang, Y., Lu, H. and Bargmann, C. I. (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature, 438, pp. 179-184.