Central processing of the chemical senses: An overview

ACS Chemical Neuroscience

Volumn 2, Issue 1, 2011, Pages 5-16

  Lundström, Johan N ^a,b,c   Boesveldt, Sanne ^a,d   Albrecht, Jessica ^a  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

fMRI; neuroimaging; Olfaction; smell; taste; trigeminal

Indexed keywords

BRAIN BLOOD FLOW; BRAIN FUNCTION; BURNING SENSATION; CHEMICAL ANALYSIS; DIFFUSION TENSOR IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOSSOPHARYNGEAL NERVE; GUSTATORY SYSTEM; HUMAN; NEUROANATOMY; NEUROIMAGING; NOCICEPTION; NONHUMAN; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; ORBITAL CORTEX; PAIN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PYRIFORM CORTEX; REVIEW; SENSORY STIMULATION; SKIN TINGLING; SMELLING; SOMATOSENSORY CORTEX; TASTE; TEMPERATURE SENSITIVITY; TOUCH; TRIGEMINAL NERVE;

EID: 78751659096     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn1000843     Document Type: Review

References (102)

1. Kobal, G. (1981) Electrophysiologische Untersuchungen des menschlichen Geruchssinns, Thieme Verlag, Stuttgart, Germany.
2. Plattig, K. H., Dazert, S., and Maeyama, T. (1988) A new gustometer for computer evaluation of taste responses in men and animals Acta Otolaryngol. Suppl. 458, 123-128
3. Rouquier, S., Taviaux, S., Trask, B. J., Brand-Arpon, V., van den Engh, G., Demaille, J., and Giorgi, D. (1998) Distribution of olfactory receptor genes in the human genome Nat. Genet. 18, 243-250
4. Lundstrom, J. N., Boyle, J. A., Zatorre, R. J., and Jones-Gotman, M. (2009) The neuronal substrates of human olfactory based kin recognition Hum. Brain Mapp. 30, 2571-2580
5. Porter, J., Craven, B., Khan, R. M., Chang, S. J., Kang, I., Judkewitz, B., Volpe, J., Settles, G., and Sobel, N. (2007) Mechanisms of scent-tracking in humans Nat. Neurosci. 10, 27-29
6. Laska, M., Genzel, D., and Wieser, A. (2005) The number of functional olfactory receptor genes and the relative size of olfactory brain structures are poor predictors of olfactory discrimination performance with enantiomers Chem. Senses 30, 171-175
7. Laska, M., Seibt, A., and Weber, A. (2000) 'Microsmatic' primates revisited: olfactory sensitivity in the squirrel monkey Chem. Senses 25, 47-53
8. Shepherd, G. M. (2004) The human sense of smell: are we better than we think? PLoS Biol. 2, E146
9. Kay, L. M. and Sherman, S. M. (2007) An argument for an olfactory thalamus Trends Neurosci. 30, 47-53
10. Plailly, J., Howard, J. D., Gitelman, D. R., and Gottfried, J. A. (2008) Attention to odor modulates thalamocortical connectivity in the human brain J. Neurosci. 28, 5257-5267
11. Carmichael, S. T., Clugnet, M. C., and Price, J. L. (1994) Central olfactory connections in the macaque monkey J. Comp. Neurol. 346, 403-434
12. Firestein, S. (2001) How the olfactory system makes sense of scent Nature 413, 211-218
13. Price, J. L. (2003) The Olfactory System, in The Human Nervous System (Paxinos, G., Ed.) pp 1198 - 1212, Academic Press, San Diego, CA.
14. Powell, T. P., Cowan, W. M., and Raisman, G. (1965) The central olfactory connexions J. Anat. 99, 791-813
15. Zatorre, R. J., Jones-Gotman, M., Evans, A. C., and Meyer, E. (1992) Functional localization and lateralization of human olfactory cortex Nature 360, 339-340
16. Savic, I., Gulyas, B., Larsson, M., and Roland, P. (2000) Olfactory functions are mediated by parallel and hierarchical processing Neuron 26, 735-745
17. Zald, D. H. and Pardo, J. V. (2000) Functional neuroimaging of the olfactory system in humans Int. J. Psychophysiol. 36, 165-181
18. Cleland, T. A. and Linster, C. (2005) Computation in the olfactory system Chem. Senses 30, 801-813
19. Haberly, L. B. (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry Chem. Senses 26, 551-576
20. Zelano, C., Bensafi, M., Porter, J., Mainland, J., Johnson, B., Bremner, E., Telles, C., Khan, R., and Sobel, N. (2005) Attentional modulation in human primary olfactory cortex Nat. Neurosci. 8, 114-120
21. Dade, L. A., Zatorre, R. J., and Jones-Gotman, M. (2002) Olfactory learning: convergent findings from lesion and brain imaging studies in humans Brain 125, 86-101
22. Gottfried, J. A., Smith, A. P., Rugg, M. D., and Dolan, R. J. (2004) Remembrance of odors past: human olfactory cortex in cross-modal recognition memory Neuron 42, 687-695
23. Gottfried, J. A., O'Doherty, J., and Dolan, R. J. (2002) Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging J. Neurosci. 22, 10829-10837
24. Zelano, C., Montag, J., Johnson, B., Khan, R., and Sobel, N. (2007) Dissociated representations of irritation and valence in human primary olfactory cortex J. Neurophysiol. 97, 1969-1976
25. Gottfried, J. A. (2010) Central mechanisms of odour object perception Nat. Rev. Neurosci. 11, 628-641
26. Maresh, A., Rodriguez Gil, D., Whitman, M. C., and Greer, C. A. (2008) Principles of glomerular organization in the human olfactory bulb: implications for odor processing PLoS One 3, e2640
27. Chaudhury, D., Manella, L., Arellanos, A., Escanilla, O., Cleland, T. A., and Linster, C. (2010) Olfactory bulb habituation to odor stimuli Behav. Neurosci. 124, 490-499
28. Barnes, D. C., Hofacer, R. D., Zaman, A. R., Rennaker, R. L., and Wilson, D. A. (2008) Olfactory perceptual stability and discrimination Nat. Neurosci. 11, 1378-1380
29. Gottfried, J. A., Winston, J. S., and Dolan, R. J. (2006) Dissociable codes of odor quality and odorant structure in human piriform cortex Neuron 49, 467-479
30. Royet, J. P., Hudry, J., Zald, D. H., Godinot, D., Gregoire, M. C., Lavenne, F., Costes, N., and Holley, A. (2001) Functional neuroanatomy of different olfactory judgments Neuroimage 13, 506-519
31. Zald, D. H. and Pardo, J. V. (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation Proc. Natl. Acad. Sci. U.S.A. 94, 4119-4124
32. Gottfried, J. A. and Dolan, R. J. (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception Neuron 39, 375-386
33. Rolls, E. T. and Baylis, L. L. (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex J. Neurosci. 14, 5437-5452
34. Carmichael, S. T. and Price, J. L. (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys J. Comp. Neurol. 363, 642-664
35. Gottfried, J. A. and Zald, D. H. (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates Brain Res. Brain Res. Rev. 50, 287-304
36. Lundstrom, J. N., Boyle, J. A., Zatorre, R. J., and Jones-Gotman, M. (2008) Functional neuronal processing of body odors differ from that of similar common odors Cereb. Cortex 18, 1466-1474
37. Lundstrom, J. N., Olsson, M. J., Schaal, B., and Hummel, T. (2006) A putative social chemosignal elicits faster cortical responses than perceptually similar odorants Neuroimage 30, 1340-1346
38. Wesson, D. W. and Wilson, D. A. (2010) Sniffing out the contributions of the olfactory tubercle to the sense of smell: hedonics; sensory integration; and more? Neurosci. Biobehav. Rev., published online Aug 26, 2010.
39. Anderson, A. K., Christoff, K., Stappen, I., Panitz, D., Ghahremani, D. G., Glover, G., Gabrieli, J. D., and Sobel, N. (2003) Dissociated neural representations of intensity and valence in human olfaction Nat. Neurosci. 6, 196-202
40. Winston, J. S., Gottfried, J. A., Kilner, J. M., and Dolan, R. J. (2005) Integrated neural representations of odor intensity and affective valence in human amygdala J. Neurosci. 25, 8903-8907
41. Grabenhorst, F., Rolls, E. T., Margot, C., da Silva, M. A. A. P., and Velazco, M. I. (2007) How pleasant and unpleasant stimuli combine in different brain regions: odor mixtures J. Neurosci. 27, 13532-13540
42. de Araujo, I. E., Rolls, E. T., Velazco, M. I., Margot, C., and Cayeux, I. (2005) Cognitive modulation of olfactory processing Neuron 46, 671-679
43. Dolan, R. J. and Vuilleumier, P. (2003) Amygdala automaticity in emotional processing Ann. N.Y. Acad. Sci. 985, 348-355
44. Sacco, T. and Sacchetti, B. (2010) Role of secondary sensory cortices in emotional memory storage and retrieval in rats Science 329, 649-656
45. Rolls, E. T., Kringelbach, M. L., and de Araujo, I. E. (2003) Different representations of pleasant and unpleasant odours in the human brain Eur. J. Neurosci. 18, 695-703
46. Savic, I., Berglund, H., Gulyas, B., and Roland, P. (2001) Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans Neuron 31, 661-668
47. Sela, L. and Sobel, N. (2010) Human olfaction: a constant state of change-blindness Exp. Brain Res. 205, 13-29
48. Witt, M., Reutter, K., and Miller, I. J. J. (2003) Morphology of the Peripheral Taste System, in Handbook of Olfaction and Gustation (Doty, R. L., Ed.) Marcel Dekker, New York.
49. Beckstead, R. M., Morse, J. R., and Norgren, R. (1980) The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei J. Comp. Neurol. 190, 259-282
50. Cavada, C., Company, T., Tejedor, J., Cruz-Rizzolo, R. J., and Reinoso-Suarez, F. (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review Cereb. Cortex 10, 220-242
51. 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
52. Ogawa, H., Ito, S., and Nomura, T. (1985) Two distinct projection areas from tongue nerves in the frontal operculum of macaque monkeys as revealed with evoked potential mapping Neurosci. Res. 2, 447-459
53. 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
54. Baylis, L. L., Rolls, E. T., and Baylis, G. C. (1995) Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate Neuroscience 64, 801-812
55. Aggleton, J. P., Burton, M. J., and Passingham, R. E. (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta) Brain Res. 190, 347-368
56. Kinomura, S., Kawashima, R., Yamada, K., Ono, S., Itoh, M., Yoshioka, S., Yamaguchi, T., Matsui, H., Miyazawa, H., and Itoh, H. 1994, Functional anatomy of taste perception in the human brain studied with positron emission tomography Brain Res. 659, 263-266
57. Veldhuizen, M. G., Albrecht, J., Zelano, C., Boesveldt, S., Breslin, P., and Lundstrom, J. N. Identification of human gustatory cortex by activation likelihood estimation, Hum Brain Mapp., in press.
58. Haase, L., Cerf-Ducastel, B., and Murphy, C. (2009) Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety Neuroimage 44, 1008-1021
59. Schoenfeld, M. A., Neuer, G., Tempelmann, C., Schussler, K., Noesselt, T., Hopf, J. M., and Heinze, H. J. (2004) Functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex Neuroscience 127, 347-353
60. de Araujo, I. E., 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 Eur. J. Neurosci. 18, 2059-2068
61. Rudenga, K., Green, B., Nachtigal, D., and Small, D. (2010) Evidence for an integrated oral sensory module in the human anterior ventral insula Chem Senses. 35, 693-703
62. Grabenhorst, F., Rolls, E. T., and Bilderbeck, A. (2008) How cognition modulates affective responses to taste and flavor: top-down influences on the orbitofrontal and pregenual cingulate cortices Cereb. Cortex 18, 1549-1559
63. 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, 701-711
64. Pritchard, T. C., Edwards, E. M., Smith, C. A., Hilgert, K. G., Gavlick, A. M., Maryniak, T. D., Schwartz, G. J., and Scott, T. R. (2005) Gustatory neural responses in the medial orbitofrontal cortex of the old world monkey J. Neurosci. 25, 6047-6056
65. Kringelbach, M. L. (2005) The human orbitofrontal cortex: linking reward to hedonic experience Nat. Rev. Neurosci. 6, 691-702
66. Rolls, E. T. (2008) The Anterior and Midcingulate Cortices and Reward, in Cingulate Neurobiology and Disease (Vogt, B. A., Ed.) Oxford University Press, New York.
67. Zald, D. H., Lee, J. T., Fluegel, K. W., and Pardo, J. V. (1998) Aversive gustatory stimulation activates limbic circuits in humans Brain 121 (Pt 6) 1143-1154
68. O'Doherty, J., Rolls, E. T., Francis, S., Bowtell, R., and McGlone, F. (2001) Representation of pleasant and aversive taste in the human brain J. Neurophysiol. 85, 1315-1321
69. Bender, G., Veldhuizen, M. G., Meltzer, J. A., Gitelman, D. R., and Small, D. M. (2009) Neural correlates of evaluative compared with passive tasting Eur. J. Neurosci. 30, 327-338
70. Veldhuizen, M. G., Bender, G., Constable, R. T., and Small, D. M. (2007) Trying to detect taste in a tasteless solution: modulation of early gustatory cortex by attention to taste Chem. Senses 32, 569-581
71. Landis, B. N., Welge-Luessen, A., Bramerson, A., Bende, M., Mueller, C. A., Nordin, S., and Hummel, T. (2009) "Taste Strips": a rapid, lateralized, gustatory bedside identification test based on impregnated filter papers J. Neurol. 256, 242-248
72. Boesveldt, S., Tessler-Lindau, S., McClintock, M. K., Hummel, T., and Lundstrom, J. N. (2010) Gustatory and olfactory dysfunction in older adults: a national probability study, Rhinology, in press.
73. Jacobson, A., Green, E., and Murphy, C. (2010) Age-related functional changes in gustatory and reward processing regions: An fMRI study Neuroimage 53, 602-610
74. Kringelbach, M. L., O'Doherty, J., Rolls, E. T., and Andrews, C. (2003) Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness Cereb. Cortex 13, 1064-1071
75. Uher, R., Treasure, J., Heining, M., Brammer, M. J., and Campbell, I. C. (2006) Cerebral processing of food-related stimuli: effects of fasting and gender Behav. Brain Res. 169, 111-119
76. DelParigi, A., Chen, K., Salbe, A. D., Reiman, E. M., and Tataranni, P. A. (2005) Sensory experience of food and obesity: a positron emission tomography study of the brain regions affected by tasting a liquid meal after a prolonged fast Neuroimage 24, 436-443
77. Stice, E., Spoor, S., Ng, J., and Zald, D. H. (2009) Relation of obesity to consummatory and anticipatory food reward Physiol. Behav. 97, 551-560
78. Doty, R. L., Brugger, W. E., Jurs, P. C., Orndorff, M. A., Snyder, P. J., and Lowry, L. D. (1978) Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans Physiol. Behav. 20, 175-185
79. Hummel, T. and Livermore, A. (2002) Intranasal chemosensory function of the trigeminal nerve and aspects of its relation to olfaction Int. Arch. Occup. Environ. Health 75, 305-313
80. Silver, W. L. (1991) Psychological Factors in Nasal Trigeminal Chemoreceptions, in Chemical Senses (Green, B. G., Mason, J. R., and Kare, M. R., Eds.) pp 21 - 37, Marcel Dekker, New York.
81. Anton, F. and Peppel, P. (1991) Central projections of trigeminal primary afferents innervating the nasal mucosa: a horseradish peroxidase study in the rat Neuroscience 41, 617-628
82. de Leeuw, R., Albuquerque, R., Okeson, J., and Carlson, C. (2005) The contribution of neuroimaging techniques to the understanding of supraspinal pain circuits: implications for orofacial pain Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 100, 308-314
83. Treede, R. D., Kenshalo, D. R., Gracely, R. H., and Jones, A. K. (1999) The cortical representation of pain Pain 79, 105-111
84. Boyle, J. A., Heinke, M., Gerber, J., Frasnelli, J., and Hummel, T. (2007) Cerebral activation to intranasal chemosensory trigeminal stimulation Chem. Senses 32, 343-353
85. Albrecht, J., Kopietz, R., Frasnelli, J., Wiesmann, M., Hummel, T., and Lundstrom, J. N. (2010) The neuronal correlates of intranasal trigeminal function-an ALE meta-analysis of human functional brain imaging data Brain Res. Rev. 62, 183-196
86. May, A. (2007) Neuroimaging: visualising the brain in pain Neurol. Sci. 28 (Suppl. 2) S101-S107
87. Seifert, F. and Maihofner, C. (2009) Central mechanisms of experimental and chronic neuropathic pain: findings from functional imaging studies Cell. Mol. Life Sci. 66, 375-390
88. Tracey, I. (2008) Imaging pain Br. J. Anaesth. 101, 32-39
89. Iannilli, E., Del Gratta, C., Gerber, J. C., Romani, G. L., and Hummel, T. (2008) Trigeminal activation using chemical, electrical, and mechanical stimuli Pain 139, 376-388
90. Craig, A. D. (2009) How do you feel - now? The anterior insula and human awareness Nat. Rev. Neurosci. 10, 59-70
91. Ploner, M., Lee, M. C., Wiech, K., Bingel, U., and Tracey, I. (2010) Flexible cerebral connectivity patterns subserve contextual modulations of pain, Cereb. Cortex [online early access], DOI: 10.1093/cercor/bhq146.
92. Kurth, F., Zilles, K., Fox, P. T., Laird, A. R., and Eickhoff, S. B. (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis Brain Struct. Funct. 214, 519-534
93. Bensafi, M., Iannilli, E., Gerber, J., and Hummel, T. (2008) Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems Neuroscience 154, 832-838
94. Sobel, N., Prabhakaran, V., Desmond, J. E., Glover, G. H., Goode, R. L., Sullivan, E. V., and Gabrieli, J. D. (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex Nature 392, 282-286
95. Boyle, J. A., Frasnelli, J., Gerber, J., Heinke, M., and Hummel, T. (2007) Cross-modal integration of intranasal stimuli: A functional magnetic resonance imaging study Neuroscience 149, 223-231
96. Small, D. M., Jones-Gotman, M., Zatorre, R. J., Petrides, M., and Evans, A. C. (1997) Flavor processing: more than the sum of its parts Neuroreport 8, 3913-3917
97. Small, D. (2008) Flavor and the formation of category-specific processing in olfaction Chemosensory Perception 1, 136-146
98. Calvert, G. A., Campbell, R., and Brammer, M. J. (2000) Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex Curr. Biol. 10, 649-657
99. Lundstrom, J. N., Albrecht, J., and Djordjevic, J. (2010) The localization of human olfactory cortex: an ALE meta-analysis of functional neuroimaging studies, submitted for publication.
100. Cruikshank, S. J. and Weinberger, N. M. (1996) Evidence for the Hebbian hypothesis in experience-dependent physiological plasticity of neocortex: a critical review Brain Res. Brain Res. Rev. 22, 191-228
101. Verhagen, J. V. and Engelen, L. (2007) The neurocognitive bases of human multimodal food perception: Sensory integration Neurosci. Biobehav. Rev. 53, 271-286
102. Stevenson, R. J. and Tomiczek, C. (2007) Olfactory-induced synesthesias: a review and model Psychol. Bull. 133, 294-309