Functional Organization of the Human Gustatory Cortex

Journal of Oral Biosciences

Volumn 48, Issue 4, 2006, Pages 244-260

  Kobayashi, Masayuki ^a,b  

^a NIHON UNIVERSITY   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

brain imaging; insula; primate; taste; top down signal

Indexed keywords

EID: 85010109866     PISSN: 13490079     EISSN: None     Source Type: Journal    
DOI: 10.2330/joralbiosci.48.244     Document Type: Article

References (95)

1. Swanson, L. W.: A history of neuroanatomical mapping. In: Brain mapping, The systems. (eds. Toga, A.W. and Mazziotta, J. C.), pp. 77–109, Academic Press, San Diego, 2000.
2. Spurzheim, J. G.: Phrenology, or the doctrin of the mind, third edition. Knight, London, 1825.
3. Kandel, E. W.: Brain and Behavior. In: Principles of neural science, third edition. (eds. Kandel, E. R., Schwartz, J. H. and Jessell, T. M.), pp. 5–17, Elsevier, New York, Amsterdam, London, Tokyo, 1991.
4. Beauchamp, G. K. and Cowart, B. J.: Congenital and experiential factors in the development of human flavor preferences. Appetite 6: 357–372, 1985.
5. Small, D. M. and Prescott, J. W.: Odor/taste integration and the perception of flavor. Exp. Brain Res. 166: 345–357, 2005.
6. Castriota-Scanderbeg, A., Hagberg, G. E., Cerasa, A., Committeri, G., Galati, G., Patria, F., Pitzalis, S., Caltagirone, C. and Frackowiak, R.: The appreciation of wine by sommeliers: a functional magnetic resonance study of sensory integration. Neuroimage 25: 570–578, 2005.
7. Benton, D.: Role of parents in the determination of the food preferences of children and the development of obesity. Int. J. Obes. Relat. Metab. Disord. 28: 858–869, 2004.
8. Yamamoto, T.: Taste responses of cortical neurons. Prog. Neurobiol. 23: 273–315, 1984.
9. Yamamoto, T.: Neural mechanisms of taste aversion learning. Neurosci. Res. 16: 181–185, 1993.
10. Beckstead, R. M. and Norgren, R.: An autoradiographic examination of the central distribution of the trigeminal, facial, glossopharyngeal, and vagal nerves in the monkey. J. Comp. Neurol. 184: 455–472, 1979.
11. Norgren, R.: Central neural mechanisms of taste. In: Handbook of Physiology. (ed. Darien-Smith, I.), Sect. 3, Part 1, pp. 1087–1128, Am. Physiol. Soc., Washington DC, 1984.
12. Pritchard, T. C.: The primate gustatory system. In: Smell and Taste in Health and Disease. (eds. Getchell, T., Doty, R., Bartoshuk, L. and Snow, J.), pp. 109–125, Raven Press, New York, 1991.
13. Beckstead, R. M., Morse, J. R. and Norgren, R.: The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei. J. Comp. Neurol. 190: 259–282, 1980.
14. Pritchard, T. C., Hamilton, P. B., Morse, J. P. and Norgren, P.: Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J. Comp. Neurol. 244: 213–228, 1986.
15. Benjamin, P.: Some thalamic and cortical mechanisms of taste. In: Olfaction and Taste. (ed. Zotter-man, Y), pp. 309–329, Pergamon, New York, 1963.
16. Ogawa, H., Ito, S. and Nomura, T.: Two distinct projection areas from tongue nerves in the frontal operculum of macaque monkeys as revealed with evoked potential mapping. Neurosci. Pes. 2: 447–459, 1985.
17. Scott, T. P. and Plata-Salaman, C. R.: Taste in the monkey cortex. Physiol. Behav. 67: 489–511, 1999.
18. Scott, T. P., Yaxley, S., Sienkiewicz, Z. J. and Polls, E. T.: Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. J. Neurophysiol. 56: 876–890, 1986.
19. Scott, T. P., Plata-Salaman, C. R., Smith, V. L. and Giza, B. K.: Gustatory neural coding in the monkey cortex: stimulus intensity. J. Neurophysiol. 65: 76–86, 1991.
20. Smith-Swintosky, V. L., Plata-Salaman, C. P. and Scott, T. P.: Gustatory neural coding in the monkey cortex: stimulus quality. J. Neurophysiol. 66: 1156–1165, 1991.
21. Yaxley, S., Polls, E. T. and Sienkiewicz, Z. J.: Gustatory responses of single neurons in the insula of the macaque monkey. J. Neurophysiol. 63: 689–700, 1990.
22. Ogawa, H., Ito, S. and Nomura, T.: Oral cavity representation at the frontal operculum of macaque monkeys. Neurosci. Pes. 6: 283–298, 1989.
23. Morecraft, P. J., Geula, C. and Mesulam, M. M.: Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J. Comp. Neurol. 323: 341–358, 1992.
24. Augustine, J. P.: Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Pev. 22: 229–244, 1996.
25. Carmichael, S. T. and Price, J. L.: Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J. Comp. Neurol. 346: 366–402, 1994.
26. Cavada, C., Company, T., Tejedor, J., Cruz-Pizzolo, P. J. and Peinoso-Suarez, F.: The anatomical connections of the macaque monkey orbitofrontal cortex. Cereb. Cortex 10: 220–242, 2000.
27. Thorpe, S. J., Polls, E. T. and Maddison, S.: The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp. Brain Pes. 49: 93–115, 1983.
28. Polls, E. T., Yaxley, S. and Sienkiewicz, Z. J.: Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J. Neurophysiol. 64: 1055–1066, 1990.
29. Polls, E. T.: Information processing in the taste system of primates. J. Exp. Biol. 146: 141–164, 1989.
30. Yaxley, S., Polls, E. T., Sienkiewicz, Z. J. and Scott, T. P.: Satiety does not affect gustatory activity in the nucleus of the solitary tract of the alert monkey. Brain Pes. 347: 85–93, 1985.
31. Polls, E. T., Scott, T. P., Sienkiewicz, Z. J. and Yaxley, S.: The responsiveness of neurones in the frontal opercular gustatory cortex of the macaque monkey is independent of hunger. J. Physiol. 397: 1–12, 1988.
32. Yaxley, S., Polls, E. T. and Sienkiewicz, Z. J.: The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiol. Behav. 42: 223–229, 1988.
33. Polls, E. T. and Baylis, L. L.: Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J. Neurosci. 14: 5437–5452, 1994.
34. Börnstein, W. S.: Cortical representation of taste in man and monkey. H. The localization of the cortical taste area in man and a method of measuring impairment of taste in man. Yale J. Biol. Med. 13: 133–156, 1940.
35. Motta, G.: I centri corticali del gusto. Bull. Sci. Med. 131: 480–493, 1959.
36. Pritchard, T. C., Macaluso, D. A. and Eslinger, P. J.: Taste perception in patients with insular cortex lesions. Behav. Neurosci. 113: 663–671, 1999.
37. Cereda, C., Ghika, J., Maeder, P. and Bogousslavsky, J.: Strokes restricted to the insular cortex. Neurology 59: 1950–1955, 2002.
38. Henkin, P. I., Comiter, H., Fedio, P. and O'Doherty, D.: Defects in taste and smell recognition following temporal lobectomy. Trans. Am. Neurol. Assoc. 102: 146–150, 1977.
39. Small, D. M., Jones-Gotman, M., Zatorre, P. J., Petrides, M. and Evans, A. C.: A role for the right anterior temporal lobe in taste quality recognition. J. Neurosci. 17: 5136–5142, 1997.
40. Shenkin, H. A. and Lewey, F. H.: Taste aura preceding convulsions in a lesion of the parietal operculum. J. Nerv. Ment. Dis. 100: 352–354, 1944.
41. Hausser-Hauw, C. and Bancaud, J.: Gustatory hallucinations in epileptic seizures. Electrophysiological, clinical and anatomical correlates. Brain 110: 339–359, 1987.
42. Penfield, W. and Boldrey, E.: Somatic motor and sensory representation in the cerebral cortex of man as studies by electrical stimulation. Brain 60: 389–443, 1937.
43. Penfield, W. and Faulk, M. E.: The insula. Further observations on its function. Brain 78: 445–470, 1955.
44. Goto, N., Yamamoto, T., Kaneko, M. and Tomita, H.: Primary pontine hemorrhage and gustatory disturbance: clinicoanatomic study. Stroke 14: 507–511, 1983.
45. Jyoichi, T., Honda, H., Noda, Y., Shimojo, S. and Miya-hara, T.: A case of sensory disturbance of left 5th finger associated with gustatory disturbance. Rinsho Shinkeigaku 25: 1066–1069, 1985.
46. Nakajima, Y., Utsumi, H. and Takahashi, H.: Ipsilat-eral disturbance of taste due to pontine haemorrhage. J. Neurol. 229: 133–136, 1983.
47. Shikama, Y., Kato, T., Nagaoka, U., Hosoya, T., Katagiri, T., Yamaguchi, K. and Sasaki, H.: Localization of the gustatory pathway in the human midbrain. Neurosci. Lett. 218: 198–200, 1996.
48. Uesaka, Y., Nose, H., Ida, M. and Takagi, A.: The pathway of gustatory fibers of the human ascends ipsilaterally in the pons. Neurology 50: 827–828, 1998.
49. Fujikane, M., Nakazawa, M., Ogasawara, M., Hirata, K. and Tsudo, N.: Unilateral gustatory disturbance by pontine infarction. Rinsho Shinkeigaku 38: 342–343, 1998.
50. Lee, B. C., Hwang, S. H., Rison, R. and Chang, G. Y.: Central pathway of taste: clinical and MRI study. Eur. Neurol. 39: 200–203, 1998.
51. Onoda, K. and Ikeda, M.: Gustatory disturbance due to cerebrovascular disorder. Laryngoscope 109: 123–128, 1999.
52. Aglioti, S., Tassinari, G., Corballis, M. C. and Berlucchi, G.: Incomplete gustatory lateralization as shown by analysis of taste discrimination after callosotomy. J. Cogn. Neurosci. 12: 238–245, 2000.
53. Aglioti, S. M., Tassinari, G., Fabri, M., Del Pesce, M., Quattrini, A., Manzoni, T. and Berlucchi, G.: Taste laterality in the split brain. Eur. J. Neurosci. 13: 195–200, 2001.
54. Raichle, M. E.: A brief history of human functional brain mapping. In: Brain mapping, The systems. (eds. Toga, A. W. and Mazziotta, J. C.), pp. 33–75, Academic Press, San Diego, 2000.
55. Mosso, A.: Ueber den Kreislauf des Blutes im Menschlichen Gehirn. Verlag von Veit & Company, Leipzig, 1881.
56. Fulton, J. F.: Observation upon the vascularity of the human occipital lobe during visual activity. Brain 51: 310–320, 1928.
57. Ingvar, D. H. and Risberg, J.: Influence of mental activity upon regional cerebral blood flow in man. A preliminary study. Acta Neurol. Scand. Suppl. 14: 183–186, 1965.
58. Sokoloff, L.: Metabolic Probes of Central Nervous System Activity in Experimental Animals and Man. 1st ed., Sinauer Assoc. Sunderland, MA, 1984.
59. Friston, K. J.: Analysing brain images: Principle and overview. In: Human Brain Function. (eds. Frackowiak, R. S. J., Friston, K. J., Frith, C. D., Dolan, R. J. and Mazziotta, J. C.), pp. 25–41, Academic Press, New York, 1997.
60. Ogawa, S., Lee, T. M., Kay, A. R. and Tank, D. W.: Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. U. S. A. 87: 9868–9872, 1990.
61. Ogawa, S., Lee, T. M., Nayak, A. S. and Glynn, P.: Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med. 14: 68–78, 1990.
62. Kinomura, S., Kawashima, R., Yamada, K., Ono, S., Itoh, M., Yoshioka, S., Yamaguchi, T., Matsui, H., Miyazawa, H., Itoh, H., Goto, R., Fujiwara, T., Satoh, K. and Fukuda, H.: Functional anatomy of taste perception in the human brain studied with positron emission tomography. Brain Res. 659: 263–266, 1994.
63. Small, D. M., Jones-Gotman, M., Zatorre, R. J., Petrides, M. and Evans, A. C.: Flavor processing: more than the sum of its parts. Neuroreport 8: 3913–3917, 1997.
64. Frey, S. and Petrides, M.: Re-examination of the human taste region: a positron emission tomography study. Eur. J. Neurosci. 11: 2985–2988, 1999.
65. Small, D. M., Zald, D. H., Jones-Gotman, M., Zatorre, R. J., Pardo, J. V., Frey, S. and Petrides, M.: Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10: 7–14, 1999.
66. Zald, D. H. and Pardo, J. V.: Cortical activation induced by intraoral stimulation with water in humans. Chem. Senses 25: 267–275, 2000.
67. Zald, D. H., Lee, J. T., Fluegel, K. W. and Pardo, J. V.: Aversive gustatory stimulation activates limbic circuits in humans. Brain 121: 1143–1154, 1998.
68. Faurion, A., Cerf, B., Van De Moortele, P. F., Lobel, E., Mac Leod, P. and Le Bihan, D.: Human taste cortical areas studied with functional magnetic resonance imaging: evidence of functional lateralization related to handedness. Neurosci. Lett. 277: 189–192, 1999.
69. Francis, S., Rolls, E. T., Bowtell, R., McGlone, F., O'Doherty, J., Browning, A., Clare, S. and Smith, E.: The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport 10: 453–459, 1999.
70. Barry, M. A., Gatenby, J. C., Zeiger, J. D. and Gore, J. C.: Hemispheric dominance of cortical activity evoked by focal electrogustatory stimuli. Chem. Senses 26: 471–482, 2001.
71. Cerf-Ducastel, B., Van de Moortele, P. F., MacLeod, P., Le Bihan, D. and Faurion, A.: Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. Chem. Senses 26: 371–383, 2001.
72. Kobayashi, M., Takeda, M., Hattori, N., Fukunaga, M., Sasabe, T., Inoue, N., Nagai, Y., Sawada, T., Sada-to, N. and Watanabe, Y.: Functional imaging of gustatory perception and imagery: “top-down” processing of gustatory signals. Neuroimage 23: 1271–1282, 2004.
73. Kringelbach, M. L., de Araujo, I. E. and Rolls, E. T.: Taste-related activity in the human dorsolateral prefrontal cortex. Neuroimage 21: 781–788, 2004.
74. Kikuchi, S., Kubota, F., Nisijima, K., Washiya, S. and Kato, S.: Cerebral activation focusing on strong tasting food: a functional magnetic resonance imaging study. Neuroreport 16: 281–283, 2005.
75. Ogawa, H., Wakita, M., Hasegawa, K., Kobayakawa, T., Sakai, N., Hirai, T., Yamashita, Y. and Saito, S.: Functional MRI detection of activation in the primary gustatory cortices in humans. Chem. Senses 30: 583–592, 2005.
76. Zald, D. H., Hagen, M. C. and Pardo, J. V.: Neural correlates of tasting concentrated quinine and sugar solutions. J. Neurophysiol. 87: 1068–1075, 2002.
77. Kringelbach, M. L. and Rolls, E. T.: The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 72: 341–372, 2004.
78. Hasegawa, I., Fukushima, T., Ihara, T. and Miyashita, Y.: Callosal window between prefrontal cortices: cognitive interaction to retrieve long-term memory. Science 281: 814–818, 1998.
79. Tomita, H., Ohbayashi, M., Nakahara, K., Hasegawa, I. and Miyashita, Y.: Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature 401: 699–703, 1999.
80. Barcelo, F., Suwazono, S. and Knight, R. T.: Prefrontal modulation of visual processing in humans. Nat. Neurosci. 3: 399–403, 2000.
81. Ishai, A., Ungerleider, L. G. and Haxby, J. L.: Distributed neural systems for the generation of visual images. Neuron 28: 979–990, 2000.
82. Kosslyn, S. M., Thompson, W. L. and Alpert, N. M.: Neural systems shared by visual imagery and visual perception: a PET study. Neuroimage 6: 320–334, 1997.
83. Kreiman, G., Koch, C. and Fried, I.: Imagery neurons in the human brain. Nature 408: 357–361, 2000.
84. Gordon, C. M., Dougherty, D. D., Rauch, S. L., Emans, S. J., Grace, E., Lamm, R., Alpert, N. M., Majzoub, J. A. and Fischman, A. J.: Neuroanatomy of human appetitive function: A positron emission tomography investigation. Int. J. Eat Disord. 27: 163–171, 2000.
85. LaBar, K. S., Gitelman, D. R., Parrish, T. B., Kim, Y. H., Nobre, A. C. and Mesulam, M. M.: Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behav. Neurosci. 115: 493–500, 2001.
86. Killgore, W. D., Young, A. D., Femia, L. A., Bogorodz-ki, P., Rogowska, J. and Yurgelun-Todd, D. A.: Cortical and limbic activation during viewing of high-versus low-calorie foods. Neuroimage 19: 1381–1394, 2003.
87. Karhunen, L. J., Lappalainen, R. I., Vanninen, E. J., Kuikka, J. T. and Uusitupa, M. I.: Regional cerebral blood flow during food exposure in obese and normal-weight women. Brain 120: 1675–1684, 1997.
88. Karhunen, L. J., Vanninen, E. J., Kuikka, J. T., Lappalainen, R. I., Tiihonen, J. and Uusitupa, M. I.: Regional cerebral blood flow during exposure to food in obese binge eating women. Psychiatry Res. 99: 29–42, 2000.
89. Simmons, W. K., Martin, A. and Barsalou, L. W.: Pictures of appetizing foods activate gustatory cortices for taste and reward. Cereb. Cortex. 15: 1602–1608, 2005.
90. Buckner, P. L., Paichle, M. E., Miezin, F. M. and Petersen, S. E.: Functional anatomic studies of memory retrieval for auditory words and visual pictures. J. Neurosci. 16: 6219–6235, 1996.
91. Hopfinger, J. B., Buonocore, M. H. and Mangun, G. P.: The neural mechanisms of top-down attentional control. Nat. Neurosci. 3: 284–291, 2000.
92. Polls, E. T.: Taste and olfactory processing in the brain and its relation to the control of eating. Crit. Pev. Neurobiol. 11: 263–287, 1997.
93. Kobayashi, M., Sasabe, T., Takeda, M., Kondo, Y., Yoshikubo, S., Imamura, K., Onoe, H., Sawada, T. and Watanabe, Y.: Functional anatomy of chemical senses in the alert monkey revealed by positron emission tomography. Eur. J. Neurosci. 16: 975–980, 2002.
94. Tsujimoto, T., Ogawa, M., Tsukada, H., Kakiuchi, T. and Sasaki, K.: Activation of the insular and opercular regions of the monkey by drinking as revealed by positron emission tomography. Neurosci. Lett. 261: 135–138, 1999.
95. 15O. II. Implementation and validation. J. Nucl. Med. 24: 790–798, 1983.