Experience-dependent neural integration of taste and smell in the human brain

Journal of Neurophysiology

Volumn 92, Issue 3, 2004, Pages 1892-1903

  Small, Dana M ^a,c,d   Voss, Joel ^a,b   Mak, Y Erica ^a   Simmons, Katharine B ^a   Parrish, Todd ^a   Gitelman, Darren ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c JOHN B PIERCE LABORATORY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN; CINGULATE GYRUS; EXPERIENCE; FEMALE; FLAVOR; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; ODOR; ORBITAL CORTEX; PARIETAL LOBE; PERCEPTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; TASTE;

ADULT; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; LIFE CHANGE EVENTS; MALE; SMELL; TASTE;

EID: 4143060388     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00050.2004     Document Type: Article

References (83)

1. Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, Gabrieli JDE, and Sobel N. Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6: 196-202, 2003.
2. Barry MA, Gatenby JC, Zeiger JD, and Gore JC. Hemispheric dominance of cortical activity evoked by focal electrogustatory stimuli. Chem Senses 26: 471-482, 2001.
3. Bartoshuk LM and Beauchamp GK. Chemical senses. Annu Rev Psychology 45: 419-449, 1994.
4. Bushara KO, Grafman J, and Hallet M. Neural correlates of auditory-visual stimulus onset asynchrony detection. J Neurosci 21: 300-304, 2001.
5. Bushara KO, Hanakawa T, Immisch I, Toma K, Kanasaku K, and Hallet M. Neural correlates of cross-modal binding. Nat Neurosci 6: 190-195, 2003.
6. Calvert GA. Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb Cortex 11: 1110-1123, 2001.
7. Calvert GA, Brammer MJ, Bullmore ET, Campbell R, Iversen SD, and David AS. Response amplification in sensory-specific cortices during cross-modal binding. Neuroreport 10: 2619-2623, 1999.
8. Calvert GA, Hansen PC, Iversen SD, and Brammer MJ. Detection of audio-visual integration sites in humans by application of electrophysiological criteria to the BOLD effect. Neuroimage 14: 427-438, 2001.
9. Cerf B, Lebihan D, Van de Moortele PF, Mac Leod P, and Faurion A. Functional lateralization of human gustatory cortex related to handedness disclosed by fMRI study. Ann NY Acad Sci 855: 575-578, 1998.
10. Cerf-Ducastel B and Murphy C. fMRI activation in response to odorants orally delivered in aqueous solutions. Chem Senses 26: 625-637, 2001.
11. Cerf-Ducastel B, Van de Moortele PF, 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.
12. Dalton P, Doolittle N, Nagata H, and Breslin PA. The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 3: 431-432, 2000.
13. de Araujo E, Rolls Et, Kringelbach ML, McGlone F, and Phillips N. Taste-olfactory conergence, and the representation of the pleasantness of flavour in the human brain. Eur J Neurosci 18: 2059-2068, 2003.
14. Del Parigi A, Chen K, Salbe AD, Gautier JF, Ravussin E, Reiman EM, and Tataranni PA. Tasting a liquid meal after a prolonged fast is associated with preferential activation of the left hemisphere. Neuroreport 13: 1141-1145, 2002.
15. Elliott R, Dolan RJ, and Frith CD. Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb Cortex 10: 308-317, 2000.
16. Elliott R, Friston KJ, and Dolan RJ. Dissociable neural responses in human reward systems. J Neurosci 20: 6159-6165, 2000.
17. Elliott R, Newman JL, Longe OA, and Deakin JF. Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: a parametric functional magnetic resonance imaging study. J Neurosci 23: 303-307, 2003.
18. Faurion A, Cerf B, Le Bihan D, and Pillias AM. fMRI study of taste cortical areas in humans. Ann NY Acad Sci 855: 535-545, 1998.
19. Francis S, Rolls ET, 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: 435-459, 1999.
20. Frank RA, Ducheny K, and Mize SS. Strawberry odor, but not red color, enhances the sweetness of sucrose solutions. Chem Senses 14: 371-377, 1989.
21. Friston KJ, Jezzard P, and Turner R. Analysis of functional MRI time-series. Human Brain Mapp 1: 153-171, 1994.
22. Frey S and Petrides M. Re-examination of the human taste region: a positron emission tomography study. Eur J Neurosci 11: 2985-2988, 1999.
23. Gerber J, Small DM, Heilmann S, and Hummel T. Comparison of orthonasal and retronasal perception of non-food odors: a functional MR imaging study. Chem Senses 28: 554, 2003.
24. Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Kim YH, Meyer JR, and Mesulam M. A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain 122: 1093-1106, 1999.
25. Gottfried JA, Deichmann R, Winston JS, and Dolan RJ. Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J Neurosci 22: 10819-10828, 2002a.
26. Gottfried JA and Dolan RJ. The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39: 375-396, 2003.
27. Gottfried JA, O'Doherty J, and Dolan RJ. Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J Neurosci 22: 10829-10837, 2002b.
28. Green BG, Dalton P, Cowart B, Shaffer G, Rankin K, and Higgins J. Evaluating the "Labeled Magnitude Scale" for measuring sensations of taste and smell. Chem Senses 21: 323-334, 1996.
29. Heilmann S and Hummel T. Olfactory Event-Related Potentials to Ortho- and Retronasal Stimulation. Sarasota, FL: Association for Chemoreception Sciences (AChemS), 2001.
30. Henson RN, Price CJ, Rugg MD, Turner R, and Friston KJ. Detecting latency differences in event-related BOLD responses: application to words versus nonwords and initial versus repeated face presentations. Neuroimage 15: 83-97, 2002.
31. Kinomura S, Kawashima M, Yamada K, Ono S, Itoh M, Yoshioka S, Yamaguchi T, Matsui H, Miyazawa H, and Itoh H. Functional anatomy of taste perception in the human brain studied with positron emission tomography. Brain Res 659: 263-266, 1994.
32. Laing DG, Link C, Jings AL, and Hutchinson I. The limited capacity of humans to identify the components of taste mixtures and taste-odor mixtures. Perception 31: 617-635, 2002.
33. Laurienti PJ, Burdette JH, Wallace MT, Yen YF, Field AS, and Stein BE. Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci 14: 420-429, 2002.
34. Macaluso E, Frith C, and Driver J. Modulation of human visual cortex by crossmodal spatial attention. Science 289: 1206-1208, 2000.
35. Meredith MA, Nemitz JW, and Stein BE. Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors. J Neurosci 7: 3215-3229, 1987.
36. Meredith MA and Stein BE. Visual, auditory and somatosensory convergence on cells in the superior colliculus results in multisensory integration. J Neurophysiol 56: 640-662, 1986.
37. Meredith MA and Stein BE. Spatial determinants of multisensory integration in cat superior colliculus neurons. J Neurophysiol 75: 1843-1857, 1996.
38. O'Doherty J, Critchley HD, Deichmann R, and Dolan RJ. Dissociating valence outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci 23: 7931-7939, 2003.
39. O'Doherty J, Kringelbach ML, Rolls ET, Hornak J, and Andrews C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4: 95-102, 2001a.
40. O'Doherty J, Rolls ET, Francis S, Bowtell R, and McGlone F. Representation of pleasant and aversive taste in the human brain. J Neurophysiol 85: 1315-1321, 2001b.
41. O'Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G, Renner B, and Ahne G. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex [republished in Neuroreport 2000 Mar 20;11(4):893-897]. Neuroreport 11: 399-403, 2000.
42. O'Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G, Renner B, and Ahne G. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex [republished in Neuroreport 2000 Mar 20;11(4):893-897]. Neuroreport 11: 399-403, 2000.
43. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97-113, 1971.
44. Parrish TB, Gitelman DR, LaBar KS, and Mesulam MM. Impact of signal-to-noise on functional MRI. Magn Reson Med 44: 925-932, 2000.
45. Pierce J and Halpern BP. Orthonasal and retronasal odorant identification based upon vapor phase input from common substances. Chem Senses 21: 529-543, 1996.
46. Plata-Salaman CR, Smith-Swintosky VL, and Scott TR. Gustatory neural coding in the monkey cortex: mixtures. J Neurophysiol 75: 2369-2379, 1996.
47. Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, and Kwong KK. Activation and habituation in olfaction-an fMRI study. Neuroimage 13: 547-560, 2001.
48. Prescott J. Flavour as a psychological construct: implications for perceiving and measuring the sensory qualities of foods. Food Qual Prefer 10: 349-356, 1999.
49. Price JL, Carmichael ST, Carnes K, Clugnet MC, and Kuroda M. Olfactory input to the prefrontal cortex. In: Olfaction: A Model System for Computational Neuroscience, edited by J Davis and H Eichenbaum Cambridge, MA: MIT Press, 1991, p. 101-120.
50. Prutkin J, Fisher EM, Etter L, Fast K, Gardner E, Lucchina LA, Snyder DJ, Tie K, Weiffenbach J, and Bartoshuk LM. Genetic variation and inferences about perceived taste intensity in mice and men. Physiol Behav 69: 161-173, 2000.
51. Rolls ET. The orbitofrontal cortex and reward. Cereb Cortex 10: 284-294, 2000.
52. Rolls ET and Baylis LL. Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14: 5437-5452, 1994.
53. Rolls ET, Critchley HD, and Treves A. Representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol 75: 1982-1996, 1996.
54. Rolls ET, Kringelbach ML, and de Araujo E. Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci 18: 695-703, 2003.
55. Royet JP, Plailly J, Delon-Martin C, Kareken DA, and Segebarth C. fMRI of emotional responses to odors: influence of hedonic valence and judgment, handedness, and gender. Neuroimage 20: 713-728, 2003.
56. Rozin P. "Taste-smell confusions" and the duality of the olfactory sense. Percept Psychophys 31: 397-401, 1982.
57. Savic I and Berglund H. Right-nostril dominance in discrimination of unfamiliar, but not familiar, odours. Chem Senses 25: 517-523, 2000.
58. Savic I and Gulyas B. PET shows that odors are processed both ipsilaterally and contralaterally to the stimulated nostril. Neuroreport 11: 2861-2866, 2000.
59. Savic I, Gulyas B, Larsson M, and Roland P. Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26: 735-745, 2000.
60. Schifferstein HN and Verlegh PW. The role of congruency and pleasantness in odor-induced taste enhancement. Acta Psychologica 94: 87-105, 1996.
61. Scott TR and Plata-Salaman CR. Taste in the monkey cortex. Physiol Behav 67: 489-511, 1999.
62. Slotnick BM, Westbrook F, and Darling FMC. What the rat's nose tells the rat's mouth: long delay aversion conditioning with aqueous odors and potentiation of taste by odors. Anim Learn Behav 25: 357-369, 1997.
63. Small DM, Gregory MD, Mak YE, Gitelman DR, Mesulam MM, and Parrish TB. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39: 701-711, 2003.
64. Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, and Evans AC. Flavor processing: more than the sum of its parts. Neuroreport 8: 3913-3917, 1997a.
65. Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, and Evans AC. A role for the right anterior temporal lobe in taste quality recognition. J Neurosci 17: 5136-5142, 1997b.
66. Small DM, Zald DH, Jones-Gotman M, Zatorre RJ, Pardo JV, Frey S, and Petrides M. Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10: 7-14, 1999.
67. Small DM, Zatorre RJ, Dagher A, Evans AC, and Jones-Gotman M. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 124: 1720-1733, 2001.
68. Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, and Gabrieli JD. Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392: 282-286, 1998.
69. Stein BE. Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp Brain Res 123: 124-135, 1998.
70. Stevenson RJ, Boakes RA, and Prescott J. Changes in odor sweetness resulting from implicit learning of a simultaneous odor-sweetness association: an example of learned synesthesia. Learn Motiv 29: May 1998: US, http://www, 1998.
71. Stevenson RJ and Prescott J. The aquisition of taste properties by odors. Learn Motiv 26: 433-455, 1995.
72. Stevenson RJ, Prescott J, and Boakes RA. Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes. Chem Senses 24: 627-635, 1999.
73. Talairach J and Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme, 1988.
74. Voirol E and Dagnet N. Comparative study of nasal and retronasal olfactory perception. Food Sci Technol 19: 316-319, 1986.
75. Williams GV, Rolls ET, Leonard CM, and Stern C. Neuronal responses in the ventral striatum of the behaving macaque. Behav Brain Res 55: 243-252, 1993.
76. Wilson FA and Rolls ET. Neuronal responses related to the novelty and familiarity of visual stimuli in the substantia innominata, diagonal band of Broca and periventricular region of the primate basal forebrain. Exp Brain Res 80: 104-120, 1990.
77. Worsley KJ and Friston KJ. Analysis of fMRI time-series revisited-again [letter; comment]. Neuroimage 2: 173-181, 1995.
78. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, and Evans AC. A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapp 4: 58-73, 1996.
79. Zald DH, Hagen MC, and Pardo JV. Neural correlates of tasting concentrated quinine and sugar solutions. J Neurophysiol. 87: 1068-1075, 2002.
80. Zald DH, Lee JT, Fluegel KW, and Pardo JV. Aversive gustatory stimulation activates limbic circuits in humans. Brain 121: 1143-1154, 1998.
81. Zald DH and Pardo JV. Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA 94: 4119-4124, 1997.
82. Zald DH and Pardo JV. Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol 36: 165-181, 2000.
83. Zatorre RJ, Jones-Gotman M, Evans AC, and Meyer E. Functional localization and lateralization of human olfactory cortex. Nature 360: 339-340, 1992.