Neuronal representations of stimuli in the mouth: The primate insular taste cortex, orbitofrontal cortex and amygdala

Chemical Senses

Volumn 30, Issue 5, 2005, Pages 401-419

  Kadohisa, Mikiko ^a   Rolls, Edmund T ^a   Verhagen, Justus V ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Fat; Flavour; Gritty texture; Insular taste cortex; Macaque; Primary taste cortex; Taste; Texture; Viscosity

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CHEMICAL CUE; FOOD INTAKE; FOOD PREFERENCE; FOOD TEXTURE; GUSTATORY NERVOUS SYSTEM; INSULA; NONHUMAN; OLFACTORY SYSTEM; ORBITAL CORTEX; PALATABILITY; PRIORITY JOURNAL; RHESUS MONKEY; SENSORY STIMULATION; STIMULUS RESPONSE; TASTE; VISCOSITY; VISUAL STIMULATION;

ADULT; AMYGDALA; ANIMALS; CAPSAICIN; CLUSTER ANALYSIS; FATTY ACIDS; FEMALE; FRONTAL LOBE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MACACA MULATTA; MALE; MIDDLE AGED; MOUTH; NEURONS; OLFACTORY PATHWAYS; PSYCHOPHYSICS; PSYCHOPHYSIOLOGY; TASTE; VISUAL CORTEX;

PRIMATES;

EID: 23844470978     PISSN: 0379864X     EISSN: None     Source Type: Journal    
DOI: 10.1093/chemse/bji036     Document Type: Article

References (61)

1. Baylis, L.L., Rolls, E.T. and Baylis, G.C. (1994) Afferent connections of the orbitofrontal cortex taste area of the primate. Neuroscience, 64, 801-812.
2. Beckstead, R.M., Morse, J.R. and Norgren, R. (1980) The nucleus of the solitary tract in the monkey: projections to the thalamus and brainstem nuclei. J. Comp. Neurol., 190, 259-282.
3. Berthoud, H.R. (2003) Neural system controlling food intake and energy balance in the modern world. Curr. Opin. Clin. Nutr. Metab. Care, 6, 615-620.
4. Caterina, M.J., Rosen, T.A., Tominaga, M., Brake, A.J. and Julius, D. (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature, 398, 436-441.
5. Critchley, H.D. and Rolls, E.T. (1996) Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task. J. Neurophysiol., 75, 1659-1672.
6. Danilova, V. and Hellekant, G. (2002) Oral sensation of ethanol in primate model III: responses in the lingual branch of the trigeminal nerve of Macaca mulatta. Alcohol, 26, 3-16.
7. de Araujo, I.E.T. and Rolls, E.T. (2004) The representation in the human brain of food texture and oral fat. J. Neurosci., 24, 3086-3093.
8. de Araujo, I.E.T., Kringelbach, M.L. and Rolls, E.T. (2003a) Tasteolfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur J Neurosci, 18, 2374-2390.
9. de Araujo, I.E.T., Kringelbach, M.L., Rolls, E.T. and Hobden, P. (2003b) The representation of umami taste in the human brain. J. Neurophysiol., 90, 313-319.
10. Deco, G. and Rolls, E.T. (2005) Synaptic and spiking dynamics underlying reward reversal in orbitofrontal cortex. Cereb. Cortex, 15, 15-30.
11. Friedman, D.P., Murray, E.A., O'Neill, J.B. and Mishkin, M. (1986) Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J. Comp. Neurol., 252, 323-347.
12. Gilbertson, T.A. (1998) Gustatory mechanisms for the detection of fat. Curr. Opin. Neurobiol., 8, 447-452.
13. Kadohisa, M., Rolls, E.T. and Verhagen, J.V. (2004) Orbitofrontal cortex neuronal representation of temperature and capsaicin in the mouth. Neuroscience, 127, 207-221.
14. Kadohisa, M., Rolls, E.T. and Verhagen, J.V. (2005) The primate amygdala: neuronal representations of the viscosity, fat texture, grittiness and taste of foods. Neuroscience, 132, 33-48.
15. Kosar, E. and Schwartz, G.J. (1990a) Cortical unit responses to chemical stimulation of the oral cavity in the rat. Brain Res, 513, 212-224.
16. Kosar, E. and Schwartz, G.J. (1990b) Effects of methanol on peripheral nerve and cortical unit responses to thermal stimulation of the oral cavity in the rat. Brain Res, 513, 202-211.
17. Norgren, R. (1976) Taste pathways to hypothalamus and amygdala. J. Comp. Neurol., 166, 17-30.
18. Norgren, R. (1984) Central neural mechanisms of taste. In Darien-Smith, I. (ed.), Handbook of Physiology - The Nervous System III. Sensory Processes 1. American Physiological Society, Washington, DC, pp. 1087-1128.
19. Norgren, R. and Leonard, C.M. (1973) Ascending central gustatory pathways. J. Comp. Neurol., 150, 217-238.
20. 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. J. Neurophysiol., 85, 1315-1321.
21. Ogawa, H., Sato, M. and Yamashita, S. (1968) Chorda tympani fibres of the rat and hamster to gustatory and thermal stimuli. J. Neurophysiol., 199, 223-240.
22. Pritchard, T.C., Hamilton, R.B., Morse, J.R. and Norgren, R. (1986) Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J. Comp. Neurol., 244, 213-228.
23. Pritchard, T.C., Hamilton, R.B. and Norgren, R. (1989) Neural coding of gustatory information in the thalamus of Macaca mulatta. J. Neurophysiol., 61, 1-14.
24. Pritchard, T.C., Macaluso, D.A. and Eslinger, P.J. (1999) Taste perception in patients with insular cortex lesions. Behav Neurosci., 113, 663-671.
25. Rolls, E.T. (1999) The Brain and Emotion. Oxford University Press, Oxford.
26. Rolls, E.T. (2005) Emotion Explained. Oxford University Press, Oxford.
27. Rolls, E.T. and Baylis, L.L. (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J. Neurosci., 14, 5437-5452.
28. Rolls, E.T. and Tovee, M.J. (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J Neurophysiol, 73, 713-726.
29. Rolls, E.T. and Treves, A. (1998) Neural Networks and Brain Function. Oxford University Press, Oxford.
30. Rolls, E.T. and Deco, G. (2002) Computational Neuroscience of Vision. Oxford University Press, Oxford.
31. Rolls, E.T., Scott, T.R., Sienkiewicz, Z.J. and Yaxley, S. (1988) The responsiveness of neurones in the frontal opercular gustatory cortex of the macaque monkey is independent of hunger. J. Physiol., 397, 1-12.
32. Rolls, E.T., Sienkiewicz, Z.J. and Yaxley, S. (1989) Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur J Neurosci, 1, 53-60.
33. Rolls, E.T., Yaxley, S. and Sienkiewicz, Z.J. (1990) Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J. Neurophysiol., 64, 1055-1066.
34. Rolls, E.T., Critchley, H.D., Mason, R. and Wakeman, E.A. (1996) Orbitofrontal cortex neurons: role in olfactory and visual association learning. J. Neurophysiol., 75, 1970-1981.
35. Rolls, E.T., Critchley, H.D., Browning, A.S., Hernadi, A. and Lenard, L. (1999) Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J. Neurosci., 19, 1532-1540.
36. Rolls, E.T., Verhagen, J.V. and Kadohisa, M. (2003) Representations of the texture of food in the primate orbitofrontal cortex: neurons responding to viscosity, grittiness and capsaicin. J. Neurophysiol., 90, 3711-3724.
37. Sato, M., Ogawa, H. and Yamashita, S. (1975) Response properties of macaque monkey chorda tympani fibers. J. Gen. Physiol., 66, 781-821.
38. Schiffman, S.S., Reynolds, M.L. and Young, F.W. (1981) Introduction to Multidimensional Scaling. Academic Press, London.
39. Schneider, R.J., Friedman, D.P. and Mishkin, M. (1993) A modality-specific somatosensory area within the insula of the rhesus monkey. Brain Res., 621, 116-120.
40. Scott, T.R. and Plata-Salaman, C.R. (1999) Taste in the monkey cortex. Physiol Behav, 67, 489-511.
41. Scott, T.R., Yaxley, S., Sienkiewicz, Z.J. and Rolls, E.T. (1986a) Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. J. Neurophysiol., 56, 876-890.
42. Scott, T.R., Yaxley, S., Sienkiewicz, Z.J. and Rolls, E.T. (1986b) Taste responses in the nucleus tractus solitarius of the behaving monkey. J. Neurophysiol., 55, 182-200.
43. Scott, T.R., Plata-Salaman, C.R., Smith, V.L. and Giza, B.K. (1991) Gustatory neural coding in the monkey cortex: stimulus intensity. J Neurophysiol, 65, 76-86.
44. Scott, T.R., Karadi, Z., Oomura, Y., Nishino, H., Plata-Salaman, C.R., Lenard, L., Giza, B.K. and Ao, S. (1993) Gustatory neural coding in the amygdala of the alert monkey. J. Neurophysiol., 69, 1810-1820.
45. Small, D.M., Zald, D.H., Jones-Gotman, M., Zatorre, R.J., Pardo, J.V., Frey, S. and Petrides, M. (1999) Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport, 10, 7-14.
46. Smith, D.V. and Travers, J.B. (1979) A metric for the breadth of tuning of gustatory neurons. Chem. Senses, 4, 215-219.
47. Steinberger, J. and Daniels, S.R. (2003) Obesity, insulin resistance, diabetes, and cardiovascular risk in children. Circulation, 107, 1448-1453.
48. Szolcsanyi, J. (1990) Capsaicin, irritation, and desensitisation: neurophysiological basis and future perspective. Chem. Senses, 2, 141-168.
49. Theunissen, M.J.M. and Kroeze, H.A. (1995) The effect of sweetners on perceived viscosity. Chem. Senses, 20, 441-450.
50. Thorpe, S.J., Rolls, E.T. and Maddison, S. (1983) Neuronal activity in the orbitofrontal cortex of the behaving monkey. Exp Brain Res, 49, 93-115.
51. Turner, B.H., Mishkin, M. and Knapp, M. (1980) Organization of the amygdalopetal modality-specific cortical association areas in the monkey. J. Comp. Neurol., 191, 515-543.
52. Verhagen, J.V., Giza, B.K. and Scott, T.R. (2003a) Responses to taste stimulation in the ventroposteromedial nucleus of the thalamus in rats. J. Neurophysiol., 89, 265-275.
53. Verhagen, J.V., Rolls, E.T. and Kadohisa, M. (2003b) Neurons in the primate orbitofrontal cortex respond to fat texture independently of viscosity. J. Neurophysiol., 90, 1514-1525.
54. Verhagen, J.V., Kadohisa, M. and Rolls, E.T. (2004) The primate insular/opercular taste cortex: neuronal representations of the viscosity, fat texture, grittiness and taste of foods in the mouth. J.Neurophysiol., 92,1685-1699.
55. Weiss, T.J. (1983) Food oils and their uses. Horwood Ltd, Chichester.
56. Wills, W.M., Lencki, R.W. and Marangoni, A.G. (1998) Lipid modification strategies in the production of nutritionally functional fats and oils. Crit. Rev. Food Sci. Nutr., 38, 639-674.
57. Yamamoto, T., Yuyama, N. and Kawamura, Y. (1981) Cortical neurons responding to tactile, thermal and taste stimulations of the rat's tongue. Brain Res., 221, 202-206.
58. Yamamoto, T., Matsuo, R., Kiyomitsu, Y. and Kitamura, R. (1988) Sensory input from the oral region to the cerebral cortex in behaving rats: an analysis of unit responses in cortical somatosensory and taste area during ingestive behaviour. J. Neurophysiol., 60, 1303-1321.
59. Yaxley, S., Rolls, E.T. and Sienkiewicz, Z.J. (1988) The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiol Behav., 42, 223-229.
60. Yaxley, S., Rolls, E.T. and Sienkiewicz, Z.J. (1990) Gustatory responses of single neurons in the insula of the macaque monkey. J. Neurophysiol., 63, 689-700.
61. Zald, D.H., Lee, J.T., Fluegel, K.W. and Pardo, J.V. (1998) Aversive gustatory stimulation activates limbic circuits in humans. Brain, 121, 1143-1154.