Abstract
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.
Similar content being viewed by others
References
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 6:196–202
Ashkenazi A, Marks LE (2004) Effect of endogenous attention on detection of weak gustatory and olfactory flavors. Percept Psychophys 66:596–608
Auvray M, Spence C (2007) The multisensory perception of flavor. Conscious Cogn (in press) DOI 10.1016/j.concog.2007.06.005
Baeyens F, Eelen P, Van den Bergh O, Crombez G (1989) Acquired affective–evaluative vale: conservative but not interchangeable. Behav Res Therapy 27:279–287
Breslin PA (2000) Human gustation. In: Finger TE, Singer WL (eds) The neurobiology of taste and smell. Wiley–Liss, San Diego, pp 423–461
Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187
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 411:6–10
Calvert GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cerebral Cortex 11:1110–1123
Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of Macaque monkeys. J Comp Physiol Psychol 371:179–207
Cerf-Ducastel B, Murphy C (2001) fMRI activation in response to odorants orally delivered in aqueous solutions. Chem Senses 26:625–637
Cruikshank SJ, Weinberger NM (1996) Evidence for the Hebbian hypothesis in experience-dependent physiological plasticity of the neocortex: a critical review. Brains Res Rev 22:191–228
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 855:572–574
Dalton P, Doolittle N, Nagata H, Breslin PA (2000) The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 3:431–432
Dalton P, Doolittle N, Breslin PA (2002) Gender-specific induction of enhanced sensitivity to odors. Nat Neurosci 5:199–200
de Araujo E, Rolls ET (2004) Representation in the human brain of food texture and oral fat. J Neurosci 24:3086–3093
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 18:2059–2068
Delwiche JF, Heffelfinger AL (2005) Cross-modal additivity of taste and smell. J Sens Stud 20:512–525
Delwiche JF, Lera MF, Breslin PAS (2000) Selective removal of a target stimulus localized by taste in humans. Chem Senses 25:181–187
Djordjevic J, Zatorre RJ, Jones-Gotman M (2004a) Effects of perceived and imagined odors on taste detection. Chem Senses 29:199–208
Djordjevic J, Zatorre RJ, Jones-Gotman M (2004b) Odor-induced changes in taste perception. Exp Brain Res 159:405–408
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 15:143–148
Dravnieks A (1985) Atlas of odor character profiles (ASTM Data series DS61). American Society for Testing and Materials, West Conshohocken, PA
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 10:435–459
Frank RA, Byram J (1988) Taste-smell interactions are tastant and odorant dependent. Chem Senses 13:445–455
Frank RA, Ducheny K, Mize SS (1989) Strawberry odor, but not red color, enhances the sweetness of sucrose solutions. Chem Senses 14:371–377
Frank RA, van der Klaauw NJ, Schifferstein HN (1993) Both perceptual and conceptual factors influence taste-odor and taste-taste interactions. Percept Psychophys 54:343–354
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 131:99–105
Friston K, Price CJ (2001) Dynamic representations and generative models of brain function. Brain Res Bull 54:275–285
Friston K, Harrison L, Penny WD (2003) Dynamic causal modelling. Neuroimage 19:1273–1302
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 22:10829–10837
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 22:10819–10828
Gottfried JA, O'Doherty J, Dolan RJ (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301:1104–1107
Gottfried JA, Small DM, Zald DH (2006a) The chemical senses. In: Zald DH, Rauch SL (eds) The orbitofrontal cortex. Oxford University Press, Oxford, pp 125–171
Gottfried JA, Winston JS, Dolan RJ (2006b) Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49:467–479
Green BG (2002) Studying taste as a cutaneous sense. Food Qual Prefer 14:99–109
Harper R, Land DG, Griffiths NM, Bate-Smith EC (1968) Odor qualities: a glossary of usage. Br J Psychol 59:231–252
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 30:177–189
Heilmann S, Hummel T (2001) Olfactory event-related potentials to ortho- and retronasal stimulation. Achems, Sarasota, FL
Heilmann S, Hummel T (2004) A new method for comparing orthonasal and retronasal olfaction. Behav Neurosci 118:412–419
Hollingworth HL, Poffenberger AT (1917) The sense of taste. Moffat, Yard and Company, New York
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 21:42–47
Kanwisher N, Wojciulik E (2000) Visual attention: insights from brain imaging. Nat Rev Neurosci 1:91–100
Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311
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 115:493–500
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 52:1097–1108
Lim J, Green BG (2008) Tactile interaction with taste localization: influence of gustatory quality and intensity. Chem Senses 33:137–143
Livermore A, Laing DG (1996) Influence of training and experience on the perception of multicomponent odor mixtures. J Exp Psychol Hum Percept Perform 46:809–814
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 158:186–194
Martin A, Chao LL (2001) Semantic memory and the brain: structure and process. Curr Opin Neurobiol 11:194–201
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 117–124
McCabe C, Rolls ET (2007) Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain. Eur J Neurosci 25:1855–1864
Murphy CA, Cain WS (1980) Taste and olfaction: independence vs interaction. Physiol Behav 24:601–605
Murphy C, Cain WS, Bartoshuk LM (1977) Mutual action of taste and olfaction. Sens Process 1:204–211
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]
O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ (2002) Neural responses during anticipation of a primary taste reward. Neuron 33:815–826
Pearce JM (2002) Evaluation and development of a connectionist theory of configural learning. Anim Learn Behav 30:73–95
Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, Kwong KK (2001) Activation and habituation in olfaction—an fMRI study. Neuroimage 13:547–560
Prescott J (1999) Flavour as a psychological construct: implications for perceiving and measuring the sensory qualities of foods. Food Qual Prefer 10:349–356
Prescott J, Johnstone V, Francis J (2004) Odor-taste interactions: effects of attentional strategies during exposure. Chem Senses 29:331–340
Rescorla RA (1981) Simultaneous associations. In: Harzen P, Zeilner MD (eds) Predictability, correlation, and contiguity. Wiley, Chichester, pp 47–80
Rescorla RA, Freeberg L (1978) The extinction of within-compound flavor associations. Learn Motiv 9:411–427
Rolls ET (2006) Brain mechanisms underlying flavour and appetite. Philos Trans R Soc Lond B Biol Sci 361:1123–1136
Rolls ET, Baylis LL (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437–5452
Rolls ET, Critchley HD, Treves A (1996) Representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol 75:1982–1996
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 20:713–728
Rozin P (1982) “Taste-smell confusions” and the duality of the olfactory sense. Percept Psychophys 31:397–401
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 92:1002–1008
Savic I, Gulyas B, Larsson M, Roland P (2000) Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26:735–745
Savic I, Gulyas B, Berglund H (2002) Odorant differentiated pattern of cerebral activation: comparison of acetone and vanillin. Hum Brain Mapp 17:17–27
Schifferstein HNJ, Verlegh PWJ (1996) The role of congruency and pleasantness in odor-induced taste enhancement. Acta Psychol 94:87–105
Schoenbaum G, Eichenbaum H (1995a) Information coding in the rodent prefrontal cortex. II. Ensemble activity in orbitofrontal cortex. J Neurophysiol 74:751–762
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 74:733–750
Scott TR, Plata-Salaman CR (1999) Taste in the monkey cortex. Physiol Behav 67:489–511
Shikata H, McMahon DB, Breslin PA (2000) Psychophysics of taste lateralization on anterior tongue. Percept Psychophys 62:684–694
Simmons WK, Martin A, Barsalou LW (2005) Pictures of appetizing foods activate gustatory cortices for taste and reward. Cerebral Cortex 15:1602–1608
Small DM (2004) Crossmodal integration—insights from the chemical senses. Trends Neurosci 27:120–122
Small DM, Prescott J (2005) Odor/taste integration and the perception of flavor. Exp Brain Res 166:345–357
Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, Evans AC (1997) Flavor processing: more than the sum of its parts. Neuroreport 8:3913–3917
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 10:7–14
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 124:1720–1733
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 39:701–711
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 92:1892–1903
Small DM, Gerber J, Mak YE, Hummel T (2005) Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47:593–605
Small DM, Veldhuizen MG, Felsted J, Mak YE, McGlone F (2008) Separable substrates for anticipatory and consummatory food chemosensation. Neuron (in press)
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 392:282–286
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 18:8990–9001
Stein BE (1998) Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp Brain Res 123:124–135
Stevenson RJ (2001a) Associative learning and odor quality perception: how sniffing an odor mixture can alter the smell of its parts. Learn Motiv 32:154–177
Stevenson RJ (2001b) Is sweetness taste enhancement cognitively impenetrable? Effects of exposure, training and knowledge. Appetite 36:241–242
Stevenson RJ, Boakes RA (2003) A mnemonic theory of odor perception. Psychol Rev 110:340–364
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 69–83
Stevenson RJ, Case TI (2003) Preexposure to the stimulus elements, but not training to detect them, retards human odour-taste learning. Behav Processes 61:13–25
Stevenson RJ, Prescott J (1995) The acquisition of taste properties by odors. Learn Motiv 26:433–455
Stevenson RJ, Tomiczek C (2007) Olfactory-induced synesthesias: a review and model. Psychol Bull 133:294–309
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 29:113–132
Stevenson RJ, Prescott J, Boakes RA (1999) Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes. Chem Senses 24:627–635
Stevenson RJ, Boakes RA, Wilson JP (2000a) Counter-conditioning following human odor-taste and color-taste learning. Learn Motiv 31:114–127
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 26:423–440
Sun BC, Halpern BP (2005) Identification of air phase retronasal and orthonasal odorant pairs. Chem Senses 30:693–706
Tastevin J (1937) En partant de l’experience d’Aristote. Encephale 1:57–84, 140–158
Todrank J, Bartoshuk LM (1991) A taste illusion: taste sensation localized by touch. Physiol Behav 50:1027–1031
van de Klauuw NJ, Frank RA (1996) Scaling component intensities of complex stimuli: the influence of response alternatives. Environ Int 22:21–31
Verhagen JV, Engelen L (2006) The neurocognitive bases of human multimodal food perception: sensory integration. Neurosci Biobehav Rev 30:613–650
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 92:1685–1699
Vogt BA, Pandya D (1987) Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 262:271–289
von Sydow E, Moskowitz H, Jacobs H, Meiselman H (1974) Odor-taste interaction in fruit juices. Lebensm-Wiss Technol 7:9–16
Welge-Lussen A, Drago J, Wolfensberger M, Hummel T (2005) Gustatory stimulation influences the processing of intranasal stimuli. Brain Res 1038:69–75
Wilson DA (2004) Plasticity in the olfactory system: lessons for the neurobiology of memory. Neuroscientist 10:513–524
Wilson DA, Stevenson RJ (2004) The fundamental role of memory in olfactory perception. Trends Neurosci 25:243–247
Wilson DA, Kadohisa M, Fletcher ML (2006) Cortical contributions to olfaction: plasticity and perception. Semin Cell Dev Biol 17:462–470
Winston JS, Gottfried JA, Kilner JM, Dolan RJ (2005) Integrated neural representations of odor intensity and affective valence in human amygdala. J Neurosci 25:8903–8907
Yeomans MR (2006) Olfactory influences on appetite and satiety in humans. Physiol Behav 87:800–804
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 32:215–228
Zald DH, Pardo JV (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci U S A 94:4119–4124
Zald DH, Lee JT, Fluegel KW, Pardo JV (1998) Aversive gustatory stimulation activates limbic circuits in humans. Brain 121:1143–1154
Zatorre RJ, Jones-Gotman M, Evans AC, Meyer E (1992) Functional localization and lateralization of human olfactory cortex. Nature 360:339–340
Zatorre RJ, Jones-Gotman M, Rouby C (2000) Neural mechanisms involved in odor pleasantness and intensity judgments. Neuroreport 11:2711–2716
Acknowledgment
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Small, D.M. Flavor and the Formation of Category-Specific Processing in Olfaction. Chem. Percept. 1, 136–146 (2008). https://doi.org/10.1007/s12078-008-9015-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12078-008-9015-3