Abstract
Flavour perception is one of the most complex of human behaviours. It involves almost all of the senses, particularly the sense of smell, which is involved through odour images generated in the olfactory pathway. In the human brain, the perceptual systems are closely linked to systems for learning, memory, emotion and language, so distributed neural mechanisms contribute to food preference and food cravings. Greater recognition of the role of the brain's flavour system and its connection with eating behaviour is needed for a deeper understanding of why people eat what they do, and to generate better recommendations about diet and nutrition.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 (1991).
Zhang, X. & Firestein, S. The olfactory receptor gene superfamily of the mouse. Nature Neurosci. 5, 124–133 (2002).
Crasto, C., Marenco, L., Miller, P. & Shepherd, G. Olfactory receptor database: a metadata-driven automated population from sources of gene and protein sequences. Nucleic Acids Res. 30, 354–360 (2002).
Quignon, P. et al. The dog and rat olfactory receptor repertoires. Genome Biol. 6, R83 (2005).
Laska, M., Seibt, A. & Weber, A. 'Microsmatic' primates revisited: olfactory sensitivity in the squirrel monkey. Chem. Senses 25, 47–53 (2000).
Shepherd, G. M. The human sense of smell: are we better than we think? PLoS Biol. 2, e146 (2004).
Stewart, W. B., Kauer, J. S. & Shepherd, G. M. Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. J. Comp. Neurol. 185, 715–734 (1979).
Adrian, E. D. Sensory messages and sensation; the response of the olfactory organ to different smells. Acta Physiol. Scand. 29, 5–14 (1953)
Johnson, B. A., Farahbod, H., Saber, S. & Leon, M. Effects of functional group position on spatial representations of aliphatic odorants in the rat olfactory bulb. J. Comp. Neurol. 483, 192–204 (2005).
Xu, F. Q. et al. Odor maps of aldehydes and esters revealed by fMRI in the glomerular layer of the mouse olfactory bulb. Proc. Natl Acad. Sci. USA 100, 11029–11034 (2003).
Laska, M., Joshi, D. & Shepherd, G. M. Olfactory sensitivity for aliphatic aldehydes in CD-1 mice. Behav. Brain Res. 167, 349–354 (2006).
Xu, F., Greer, C. A. & Shepherd, G. M. Odor maps in the olfactory bulb. J. Comp. Neurol. 422, 489–495 (2000).
Spors, H., Wachowiak, M., Cohen, L. B. & Friedrich, R. W. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J. Neurosci. 26, 1247–1259 (2006).
Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nature Rev. Neurosci. 3, 884–895 (2002).
Willhite, D. C. et al. Viral tracing identified distributed columnar organization in the olfactory bulb. Proc. Natl Acad. Sci. USA 103, 12592–12597 (2006).
Hildebrand, J. G. & Shepherd, G. M. Molecular mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595–631 (1997).
Shepherd, G. M. Outline of a theory of olfactory processing and its relevance to humans. Chem. Senses 30 (Suppl. 1), i3–i5 (2005).
Acree, T. E., Deibler, K. D. & Kittel, K. M. in Handbook of Flavor Characterization: Sensory Analysis, Chemistry, and Physiology (eds Deibler, K. D. & Delwiche, J.) 83–91 (Marcel Dekker, New York, 2004).
Rozin, P. 'Taste–smell confusions' and the duality of the olfactory sense. Percept. Psychophys. 31, 397–401 (1982).
Sun, B. C. & Halpern, B. P. Identification of air phase retronasal and orthonasal odorant pairs. Chem. Senses 30, 693–706 (2005).
Duffy, V. B., Backstrand, J. & Ferris, A. M. Olfactory dysfunction and related nutritional risk in free-living, elderly women. J. Am. Diet. Assoc. 95, 879–884 (1995).
Shepherd-Barr, K. & Shepherd, G. M. Madeleines and neuromodernism: reassessing mechanisms of autobiographical memory in Proust. Auto/Biography Studies 13, 40–60 (1998).
Taylor, A. J., Linforth, R. S. T., Harvey, B. A. & Blake, A. Atmospheric pressure chemical ionisation for monitoring of volatile flavour release in vivo. Food Chem. 71, 327–338 (2000).
Bartoshuk, L. M. et al. From psychophysics to the clinic: missteps and advances. Food Qual. Preference 15, 617–632 (2004).
Murphy, C., Cain, W. S. & Bartoshuk, L. M. Mutual action of taste and olfaction. Sens. Process. 1, 204–211 (1977).
Mozell, M., Smith, B., Smith, P., Sullivan, L. & Swender, P. Nasal chemoreception in flavor identification. Arch. Otolaryngol. 90, 367–373 (1969).
Farb, P. & Armelagos, G. Consuming Passions: The Anthropology of Eating (Houghton Mifflin, Boston, 1980).
Scalera, G., Grigson, P. S. & Norgren, R. Gustatory functions, sodium appetite, and conditioned taste aversion survive excitotoxic lesions of the thalamic taste area. Behav. Neurosci. 111, 633–645 (1997).
Steiner, J. E. Discussion paper: innate, discriminative human facial expressions to taste and smell stimulation. Ann. NY Acad. Sci. 237, 229–233 (1974).
Small, D. M., Gerber, J. C., Mak, Y. E. & Hummel, T. Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47, 593–605 (2005).
Ongur, D., Ferry, A. T. & Price, J. L. Architectonic subdivision of the human orbital and medial prefrontal cortex. J. Comp. Neurol. 460, 425–449 (2003).
Rolls, E. T. Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol. Behav. 85, 45–56 (2005).
Small, D. M. et al. Experience-dependent neural integration of taste and smell in the human brain. J. Neurophysiol. 92, 1892–1903 (2004).
Gottfried, J. A. & Zald, D. H. On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res. Brain Res. Rev. 50, 287–304 (2005).
Koza B. J., Cilimi, A., Dolese, M. & Zellner, D. A. Color enhances orthonasal olfactory intensity and reduces retronasal intensity. Chem. Senses 30, 643–649 (2005).
Morrot, G., Brochet, F. & Dubourdieu, D. The color of odors. Brain Lang. 79, 309–320 (2001).
Haberly, L. B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26, 551–576 (2001).
Wilson, D. A. & Stevenson, R. J. Olfactory perceptual learning: the critical role of memory in odor discrimination. Neurosci. Biobehav. 27, 307–328 (2003).
Ross, R. S., McGaughy, J. & Eichenbaum, H. Acetylcholine in the orbitofrontal cortex is necessary for the acquisition of a socially transmitted food preference. Learn. Mem. 12, 302–306 (2005).
Linster, C., Maloney, M., Patil, M. & Hasselmo, M. E. Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex. Neurobiol. Learn. Mem. 80, 302–314 (2003).
Gietzen, D. W. & Rogers, Q. R. Nutritional homeostasis and indispensable amino acid sensing: a new solution to an old puzzle. Trends Neurosci. 29, 91–99 (2006).
Rolls, E. T., Kringelbach, M. L. & de Araujo, I. E. Different representations of pleasant and unpleasant odours in the human brain. Eur. J. Neurosci. 18, 695–703 (2003).
Pelchat, M. L., Johnson, A., Chan, R., Valdez, J. & Ragland, J. D. Images of desire: food-craving activation during fMRI. Neuroimage 23, 1486–1493 (2004).
Volkow, N. D. & Wise, R. A. How can drug addiction help us understand obesity? Nature Neurosci. 8, 555–560 (2005).
Pelchat, M. L. Of human bondage: food craving, obsession, compulsion and addiction. Physiol. Behav. 76, 347–352 (2002).
Carpino, S. et al. Composition and aroma compounds of Ragusano cheese: native pasture and total mixed rations. J. Dairy Sci. 87, 816–830 (2004).
Deibler, K. D. & Delwiche, J. (eds) Handbook of Flavor Characterization: Sensory Analysis, Chemistry, and Physiology (Marcel Dekker, New York, 2003).
Licitra, G. (ed.) Cheese Art 2004. Ragusa: Consorzio Ricerca Filiera Lattiero Casearia. (Ragusa, Italy, 5 Jun 2004).
Duffy, V. B., Cain, W. S. & Ferris, A. M. Measurement of sensitivity to olfactory flavor: application in a study of aging and dentures. Chem. Senses 24, 671–677 (1999).
Corriher, S.O. CookWise (William Morrow, New York, 1997).
McGee, H. On Food and Cooking: The Science and Lore of the Kitchen (Scribner, New York, 2004).
This, H. Molecular gastronomy. Nature Mater. 4, 5–7 (2005).
Mori, K., Nagao, H. & Yoshihara, Y. The olfactory bulb: coding and processing of odor molecule information. Science 286, 711–715 (1999).
Smith, D. V. & Frank, M. E. in Mechanisms of Taste Transduction (eds Simon, S. A. & Roper, S. D.) 295–338 (CRC Press, Baton Rouge, 1993).
Rolls, E. T. The representation of information about faces in the temporal and frontal lobes. Neuropsychologia [Epub ahead of print] 22 Jun 2006 (doi:10.1016/j.neuropsychologia.2006.04.019).
Lorig, T. S. On the similarity of odor and language perception. Neurosci. Biobehav. Rev. 23, 391–398 (1999).
Herz, R. S. The effect of verbal context on olfactory perception. J. Exp. Psychol. Gen. 132, 595–606 (2003).
Wrangham, R. & Conklin-Brittain, N. Cooking as a biological trait. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 136, 35–46 (2003).
Acknowledgements
Research in my laboratory is supported by the National Institutes of Health National Institute for Deafness and Other Communicative Disorders, and by the Human Brain Project. I thank M. L. Pelchat, E. T. Rolls, D. Small, L. Bartoshuk, T. Acree, F. Q. Xu and V. Duffy for valuable advice.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The author declares no competing financial interests.
Additional information
Author Information Reprints and permissions information is available at npg.nature.com/reprintsandpermissions.
Rights and permissions
About this article
Cite this article
Shepherd, G. Smell images and the flavour system in the human brain. Nature 444, 316–321 (2006). https://doi.org/10.1038/nature05405
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature05405
This article is cited by
-
Multivariate statistical regression analysis and relative quantification based on dimensional-reduction method to compare the taste-active components of different chicken breeds
Food Production, Processing and Nutrition (2024)
-
The Association Between Neurocognitive Disorders and Gustatory Dysfunction: A Systematic Review and Meta-Analysis
Neuropsychology Review (2024)
-
Smell and taste of milk during tube feeding of preterm infants: neurodevelopmental follow-up of the randomized TASTE trial, study protocol
Trials (2023)
-
An immortal porcine preadipocyte cell strain for efficient production of cell-cultured fat
Communications Biology (2023)
-
Virtual taste: digital simulation of taste sensations via electric, thermal, and hybrid stimulations
Multimedia Tools and Applications (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.