Chemosensory Perception

, Volume 1, Issue 2, pp 136–146 | Cite as

Flavor and the Formation of Category-Specific Processing in Olfaction

  • Dana M. Small


The perception of flavor occurs when objects, such as food and drink, are placed in the mouth. Although the sensation that ensues depends upon inputs from multiple sensory modalities, due to a combination of oral referral and common sensory qualities (e.g., odors and tastes can both be sweet), it is experienced as a unitary flavor perception. In this paper, it is proposed that neural processing within the somatomotor mouth area of the Rolandic operculum mediates oral referral and causes the neural binding of multimodal inputs to create a flavor percept. It is further proposed that unimodal taste and unimodal smell neurons alter the selectivity of bimodal taste/smell cells only if the binding mechanism in the somatomotor mouth area is active. The encoded flavor object is thus represented by a bounded pattern of response that includes the sculpted bimodal cells as well as the unimodal responses distributed across the insula, operculum, anterior cingulate cortex, and orbitofrontal cortex. Once an odor is encoded in this way, the odor acquires the ability to reactivate this encoded percept, whether experienced orthonasally or retronasally. Finally, it is proposed that one manifestation of this process is the existence of category-specific processing in olfaction.


Flavor Perception Neural Binding Multi-Sensory Integration Insula Olfaction Gustation Domain-Specific Processing 



I would like to thank Barry Green for many inspiring conversations about flavor perception. The ideas in this manuscript emerged from insights that occurred during these conversations. I also want to thank Barry for his comments on earlier versions of this manuscript. Thanks to Ivan de Aruajo and Justus Verhagen for informative conversations about the neurophysiology of flavor, and thanks to Marga Veldhuizen, Genevieve Bender, and Kristi Rudenga for proofreading the manuscript. This work was supported by NIDCDR03 DC006169 and NIDCDR01 DC6706-01.


  1. Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, Gabrieli JDE, Sobel N (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6:196–202Google Scholar
  2. Ashkenazi A, Marks LE (2004) Effect of endogenous attention on detection of weak gustatory and olfactory flavors. Percept Psychophys 66:596–608Google Scholar
  3. Auvray M, Spence C (2007) The multisensory perception of flavor. Conscious Cogn (in press) DOI 10.1016/j.concog.2007.06.005
  4. Baeyens F, Eelen P, Van den Bergh O, Crombez G (1989) Acquired affective–evaluative vale: conservative but not interchangeable. Behav Res Therapy 27:279–287Google Scholar
  5. Breslin PA (2000) Human gustation. In: Finger TE, Singer WL (eds) The neurobiology of taste and smell. Wiley–Liss, San Diego, pp 423–461Google Scholar
  6. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187Google Scholar
  7. Bult JH, de Wijk RA, Hummel T (2007) Investigations on multimodal sensory integration: texture, taste, and ortho- and retronasal olfactory stimuli in concert. Neurosci Lett 411:6–10Google Scholar
  8. Calvert GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cerebral Cortex 11:1110–1123Google Scholar
  9. Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of Macaque monkeys. J Comp Physiol Psychol 371:179–207Google Scholar
  10. Cerf-Ducastel B, Murphy C (2001) fMRI activation in response to odorants orally delivered in aqueous solutions. Chem Senses 26:625–637Google Scholar
  11. Cruikshank SJ, Weinberger NM (1996) Evidence for the Hebbian hypothesis in experience-dependent physiological plasticity of the neocortex: a critical review. Brains Res Rev 22:191–228Google Scholar
  12. Dade LA, Jones-Gotman M, Zatorre RJ, Evans AC (1998) Human brain function during odor encoding and recognition. A PET activation study. Ann NY Acad Sci 855:572–574Google Scholar
  13. Dalton P, Doolittle N, Nagata H, Breslin PA (2000) The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 3:431–432Google Scholar
  14. Dalton P, Doolittle N, Breslin PA (2002) Gender-specific induction of enhanced sensitivity to odors. Nat Neurosci 5:199–200Google Scholar
  15. de Araujo E, Rolls ET (2004) Representation in the human brain of food texture and oral fat. J Neurosci 24:3086–3093Google Scholar
  16. de Araujo E, Rolls Et, Kringelbach ML, McGlone F, Phillips N (2003) Taste-olfactory conergence, and the representation of the pleasantness of flavour in the human brain. Eur J Neurosci 18:2059–2068Google Scholar
  17. Delwiche JF, Heffelfinger AL (2005) Cross-modal additivity of taste and smell. J Sens Stud 20:512–525Google Scholar
  18. Delwiche JF, Lera MF, Breslin PAS (2000) Selective removal of a target stimulus localized by taste in humans. Chem Senses 25:181–187Google Scholar
  19. Djordjevic J, Zatorre RJ, Jones-Gotman M (2004a) Effects of perceived and imagined odors on taste detection. Chem Senses 29:199–208Google Scholar
  20. Djordjevic J, Zatorre RJ, Jones-Gotman M (2004b) Odor-induced changes in taste perception. Exp Brain Res 159:405–408Google Scholar
  21. Djordjevic J, Zatorre RJ, Petrides M, Jones-Gotman M (2004c) The mind’s nose: effects of odor and visual imagery on odor detection. Psychol Sci 15:143–148Google Scholar
  22. Dravnieks A (1985) Atlas of odor character profiles (ASTM Data series DS61). American Society for Testing and Materials, West Conshohocken, PAGoogle Scholar
  23. Francis S, Rolls ET, Bowtell R, McGlone F, O’Doherty J, Browning A, Clare S, Smith E (1999) The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport 10:435–459Google Scholar
  24. Frank RA, Byram J (1988) Taste-smell interactions are tastant and odorant dependent. Chem Senses 13:445–455Google Scholar
  25. Frank RA, Ducheny K, Mize SS (1989) Strawberry odor, but not red color, enhances the sweetness of sucrose solutions. Chem Senses 14:371–377Google Scholar
  26. Frank RA, van der Klaauw NJ, Schifferstein HN (1993) Both perceptual and conceptual factors influence taste-odor and taste-taste interactions. Percept Psychophys 54:343–354Google Scholar
  27. Frank GK, Kaye WH, Carter CS, Brooks S, May C, Fissell K, Stenger VA (2003) The evaluation of brain activity in response to taste stimuli—a pilot study and method for central taste activation as assessed by event-related fMRI. J Neurosci Methods 131:99–105Google Scholar
  28. Friston K, Price CJ (2001) Dynamic representations and generative models of brain function. Brain Res Bull 54:275–285Google Scholar
  29. Friston K, Harrison L, Penny WD (2003) Dynamic causal modelling. Neuroimage 19:1273–1302Google Scholar
  30. Gottfried JA, O'Doherty J, Dolan RJ (2002a) Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J Neurosci 22:10829–10837Google Scholar
  31. Gottfried JA, Deichmann R, Winston JS, Dolan RJ (2002b) Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J Neurosci 22:10819–10828Google Scholar
  32. Gottfried JA, O'Doherty J, Dolan RJ (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301:1104–1107Google Scholar
  33. Gottfried JA, Small DM, Zald DH (2006a) The chemical senses. In: Zald DH, Rauch SL (eds) The orbitofrontal cortex. Oxford University Press, Oxford, pp 125–171Google Scholar
  34. Gottfried JA, Winston JS, Dolan RJ (2006b) Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49:467–479Google Scholar
  35. Green BG (2002) Studying taste as a cutaneous sense. Food Qual Prefer 14:99–109Google Scholar
  36. Harper R, Land DG, Griffiths NM, Bate-Smith EC (1968) Odor qualities: a glossary of usage. Br J Psychol 59:231–252Google Scholar
  37. Harris JA, Shand FL, Carroll LQ, Westbrook RF (2004) Persistence of preference for a flavor presented in simultaneous compound with sucrose. J Exp Psychol Anim Behav Processes 30:177–189Google Scholar
  38. Heilmann S, Hummel T (2001) Olfactory event-related potentials to ortho- and retronasal stimulation. Achems, Sarasota, FLGoogle Scholar
  39. Heilmann S, Hummel T (2004) A new method for comparing orthonasal and retronasal olfaction. Behav Neurosci 118:412–419Google Scholar
  40. Hollingworth HL, Poffenberger AT (1917) The sense of taste. Moffat, Yard and Company, New YorkGoogle Scholar
  41. Hummel T, Heilmann S, Landis BN, Reden J, Frasnelli J, Small DM, Gerber J (2006) Perceptual differences between chemical stimuli presented through the ortho- or retronasal route. Flavour Fragr J 21:42–47Google Scholar
  42. Kanwisher N, Wojciulik E (2000) Visual attention: insights from brain imaging. Nat Rev Neurosci 1:91–100Google Scholar
  43. Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311Google Scholar
  44. LaBar KS, Gitelman DR, Parrish TB, Kim YH, Nobre AC, Mesulam MM (2001) Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behav Neurosci 115:493–500Google Scholar
  45. Li W, Luxenberg E, Parrish T, Gottfried JA (2006) Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron 52:1097–1108Google Scholar
  46. Lim J, Green BG (2008) Tactile interaction with taste localization: influence of gustatory quality and intensity. Chem Senses 33:137–143Google Scholar
  47. Livermore A, Laing DG (1996) Influence of training and experience on the perception of multicomponent odor mixtures. J Exp Psychol Hum Percept Perform 46:809–814Google Scholar
  48. Marciani L, Pfeiffer JC, Hort J, Head K, Bush D, Taylor AJ, Spiller RC, Francis S, Gowland PA (2006) Improved methods for fMRI studies of combined taste and aroma stimuli. J Neurosci Methods 158:186–194Google Scholar
  49. Martin A, Chao LL (2001) Semantic memory and the brain: structure and process. Curr Opin Neurobiol 11:194–201Google Scholar
  50. McBurney DH (1986) Taste, smell and flavor terminology: taking the confusion out of confusion. In: Meiselman HL, Rivkin RS (eds) Clinical measurement of taste and smell. Macmillan, New York, pp 117–124Google Scholar
  51. McCabe C, Rolls ET (2007) Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain. Eur J Neurosci 25:1855–1864Google Scholar
  52. Murphy CA, Cain WS (1980) Taste and olfaction: independence vs interaction. Physiol Behav 24:601–605Google Scholar
  53. Murphy C, Cain WS, Bartoshuk LM (1977) Mutual action of taste and olfaction. Sens Process 1:204–211Google Scholar
  54. O’Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G, Renner B, Ahne G (2000) Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11:399–403 [republished in Neuroreport 2000 Mar 20;11(4):893–7]CrossRefGoogle Scholar
  55. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ (2002) Neural responses during anticipation of a primary taste reward. Neuron 33:815–826Google Scholar
  56. Pearce JM (2002) Evaluation and development of a connectionist theory of configural learning. Anim Learn Behav 30:73–95Google Scholar
  57. Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, Kwong KK (2001) Activation and habituation in olfaction—an fMRI study. Neuroimage 13:547–560Google Scholar
  58. Prescott J (1999) Flavour as a psychological construct: implications for perceiving and measuring the sensory qualities of foods. Food Qual Prefer 10:349–356Google Scholar
  59. Prescott J, Johnstone V, Francis J (2004) Odor-taste interactions: effects of attentional strategies during exposure. Chem Senses 29:331–340Google Scholar
  60. Rescorla RA (1981) Simultaneous associations. In: Harzen P, Zeilner MD (eds) Predictability, correlation, and contiguity. Wiley, Chichester, pp 47–80Google Scholar
  61. Rescorla RA, Freeberg L (1978) The extinction of within-compound flavor associations. Learn Motiv 9:411–427Google Scholar
  62. Rolls ET (2006) Brain mechanisms underlying flavour and appetite. Philos Trans R Soc Lond B Biol Sci 361:1123–1136Google Scholar
  63. Rolls ET, Baylis LL (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437–5452Google Scholar
  64. Rolls ET, Critchley HD, Treves A (1996) Representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol 75:1982–1996Google Scholar
  65. Royet JP, Plailly J, Delon-Martin C, Kareken DA, Segebarth C (2003) fMRI of emotional responses to odors: influence of hedonic valence and judgment, handedness, and gender. Neuroimage 20:713–728Google Scholar
  66. Rozin P (1982) “Taste-smell confusions” and the duality of the olfactory sense. Percept Psychophys 31:397–401Google Scholar
  67. Sakai N, Kobayakawa T, Gotow N, Saito S, Imada S (2001) Enhancement of sweetness ratings of aspartame by a vanilla odor presented either by orthonasal or retronasal routes. Percept Mot Skills 92:1002–1008Google Scholar
  68. Savic I, Gulyas B, Larsson M, Roland P (2000) Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26:735–745Google Scholar
  69. Savic I, Gulyas B, Berglund H (2002) Odorant differentiated pattern of cerebral activation: comparison of acetone and vanillin. Hum Brain Mapp 17:17–27Google Scholar
  70. Schifferstein HNJ, Verlegh PWJ (1996) The role of congruency and pleasantness in odor-induced taste enhancement. Acta Psychol 94:87–105Google Scholar
  71. Schoenbaum G, Eichenbaum H (1995a) Information coding in the rodent prefrontal cortex. II. Ensemble activity in orbitofrontal cortex. J Neurophysiol 74:751–762Google Scholar
  72. Schoenbaum G, Eichenbaum H (1995b) Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J Neurophysiol 74:733–750Google Scholar
  73. Scott TR, Plata-Salaman CR (1999) Taste in the monkey cortex. Physiol Behav 67:489–511Google Scholar
  74. Shikata H, McMahon DB, Breslin PA (2000) Psychophysics of taste lateralization on anterior tongue. Percept Psychophys 62:684–694Google Scholar
  75. Simmons WK, Martin A, Barsalou LW (2005) Pictures of appetizing foods activate gustatory cortices for taste and reward. Cerebral Cortex 15:1602–1608Google Scholar
  76. Small DM (2004) Crossmodal integration—insights from the chemical senses. Trends Neurosci 27:120–122Google Scholar
  77. Small DM, Prescott J (2005) Odor/taste integration and the perception of flavor. Exp Brain Res 166:345–357Google Scholar
  78. Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, Evans AC (1997) Flavor processing: more than the sum of its parts. Neuroreport 8:3913–3917Google Scholar
  79. Small DM, Zald DH, Jones-Gotman M, Zatorre RJ, Pardo JV, Frey S, Petrides M (1999) Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10:7–14Google Scholar
  80. Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M (2001) Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 124:1720–1733Google Scholar
  81. Small DM, Gregory MD, Mak YE, Gitelman DR, Mesulam MM, Parrish TB (2003) Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39:701–711Google Scholar
  82. Small DM, Voss J, Mak YE, Simmons KB, Parrish TB, Gitelman DR (2004) Experience-dependent neural integration of taste and smell in the human brain. J Neurophysiol 92:1892–1903Google Scholar
  83. Small DM, Gerber J, Mak YE, Hummel T (2005) Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47:593–605Google Scholar
  84. Small DM, Veldhuizen MG, Felsted J, Mak YE, McGlone F (2008) Separable substrates for anticipatory and consummatory food chemosensation. Neuron (in press)Google Scholar
  85. Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD (1998a) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392:282–286Google Scholar
  86. Sobel N, Prabhakaran V, Hartley CA, Desmond JE, Zhao Z, Glover GH, Gabrieli JD, Sullivan EV (1998b) Odorant-induced and sniff-induced activation in the cerebellum of the human. J Neurosci 18:8990–9001Google Scholar
  87. Stein BE (1998) Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp Brain Res 123:124–135Google Scholar
  88. Stevenson RJ (2001a) Associative learning and odor quality perception: how sniffing an odor mixture can alter the smell of its parts. Learn Motiv 32:154–177Google Scholar
  89. Stevenson RJ (2001b) Is sweetness taste enhancement cognitively impenetrable? Effects of exposure, training and knowledge. Appetite 36:241–242Google Scholar
  90. Stevenson RJ, Boakes RA (2003) A mnemonic theory of odor perception. Psychol Rev 110:340–364Google Scholar
  91. Stevenson RJ, Boakes RA (2004) Sweet and sour smells: learned synesthesia between the senses of taste and smell. In: Calvert GA, Spence C, Stein BE (eds) The handbook of multisensory processes. MIT, Boston, pp 69–83Google Scholar
  92. Stevenson RJ, Case TI (2003) Preexposure to the stimulus elements, but not training to detect them, retards human odour-taste learning. Behav Processes 61:13–25Google Scholar
  93. Stevenson RJ, Prescott J (1995) The acquisition of taste properties by odors. Learn Motiv 26:433–455Google Scholar
  94. Stevenson RJ, Tomiczek C (2007) Olfactory-induced synesthesias: a review and model. Psychol Bull 133:294–309Google Scholar
  95. Stevenson RJ, Boakes RA, Prescott J (1998) Changes in odor sweetness resulting from implicit learning of a simultaneous odor-sweetness association: an example of learned synesthesia. Learn Motiv 29:113–132Google Scholar
  96. Stevenson RJ, Prescott J, Boakes RA (1999) Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes. Chem Senses 24:627–635Google Scholar
  97. Stevenson RJ, Boakes RA, Wilson JP (2000a) Counter-conditioning following human odor-taste and color-taste learning. Learn Motiv 31:114–127Google Scholar
  98. Stevenson RJ, Boakes RA, Wilson JP (2000b) Resistance to extinction of conditioned odor perceptions: evaluative conditioning is not unique. J Exper Psychol, Learn, Mem, Cogn 26:423–440Google Scholar
  99. Sun BC, Halpern BP (2005) Identification of air phase retronasal and orthonasal odorant pairs. Chem Senses 30:693–706Google Scholar
  100. Tastevin J (1937) En partant de l’experience d’Aristote. Encephale 1:57–84, 140–158Google Scholar
  101. Todrank J, Bartoshuk LM (1991) A taste illusion: taste sensation localized by touch. Physiol Behav 50:1027–1031Google Scholar
  102. van de Klauuw NJ, Frank RA (1996) Scaling component intensities of complex stimuli: the influence of response alternatives. Environ Int 22:21–31Google Scholar
  103. Verhagen JV, Engelen L (2006) The neurocognitive bases of human multimodal food perception: sensory integration. Neurosci Biobehav Rev 30:613–650Google Scholar
  104. Verhagen JV, Kadohisa M, Rolls ET (2004) Primate insular/opercular taste cortex: neuronal representations of the viscosity, fat texture, grittiness, temperature, and taste of foods. J Neurophysiol 92:1685–1699Google Scholar
  105. Vogt BA, Pandya D (1987) Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 262:271–289Google Scholar
  106. von Sydow E, Moskowitz H, Jacobs H, Meiselman H (1974) Odor-taste interaction in fruit juices. Lebensm-Wiss Technol 7:9–16Google Scholar
  107. Welge-Lussen A, Drago J, Wolfensberger M, Hummel T (2005) Gustatory stimulation influences the processing of intranasal stimuli. Brain Res 1038:69–75Google Scholar
  108. Wilson DA (2004) Plasticity in the olfactory system: lessons for the neurobiology of memory. Neuroscientist 10:513–524Google Scholar
  109. Wilson DA, Stevenson RJ (2004) The fundamental role of memory in olfactory perception. Trends Neurosci 25:243–247Google Scholar
  110. Wilson DA, Kadohisa M, Fletcher ML (2006) Cortical contributions to olfaction: plasticity and perception. Semin Cell Dev Biol 17:462–470Google Scholar
  111. Winston JS, Gottfried JA, Kilner JM, Dolan RJ (2005) Integrated neural representations of odor intensity and affective valence in human amygdala. J Neurosci 25:8903–8907Google Scholar
  112. Yeomans MR (2006) Olfactory influences on appetite and satiety in humans. Physiol Behav 87:800–804Google Scholar
  113. Yeomans MR, Mobini S, Elliman TD, Walker HC, Stevenson RJ (2006) Hedonic and sensory characteristics of odors conditioned by pairing with tastants in humans. J Exp Psychol, Anim Behav Processes 32:215–228Google Scholar
  114. Zald DH, Pardo JV (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci U S A 94:4119–4124Google Scholar
  115. Zald DH, Lee JT, Fluegel KW, Pardo JV (1998) Aversive gustatory stimulation activates limbic circuits in humans. Brain 121:1143–1154Google Scholar
  116. Zatorre RJ, Jones-Gotman M, Evans AC, Meyer E (1992) Functional localization and lateralization of human olfactory cortex. Nature 360:339–340Google Scholar
  117. Zatorre RJ, Jones-Gotman M, Rouby C (2000) Neural mechanisms involved in odor pleasantness and intensity judgments. Neuroreport 11:2711–2716Google Scholar

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© Springer-Verlag 2008

Authors and Affiliations

  1. 1.The John B Pierce LaboratoryNew HavenUSA
  2. 2.Department of PsychiatryYale University School of MedicineNew HavenUSA
  3. 3.Department of PsychologyYale UniversityNew HavenUSA

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