Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Smell images and the flavour system in the human brain

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

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Odour images in the olfactory glomerular layer.
Figure 2: The dual olfactory system.
Figure 3: The human brain flavour systems that evaluate and regulate food intake.

Similar content being viewed by others

References

  1. Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 (1991).

    Article  CAS  PubMed  Google Scholar 

  2. Zhang, X. & Firestein, S. The olfactory receptor gene superfamily of the mouse. Nature Neurosci. 5, 124–133 (2002).

    Article  CAS  PubMed  Google Scholar 

  3. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Quignon, P. et al. The dog and rat olfactory receptor repertoires. Genome Biol. 6, R83 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Laska, M., Seibt, A. & Weber, A. 'Microsmatic' primates revisited: olfactory sensitivity in the squirrel monkey. Chem. Senses 25, 47–53 (2000).

    Article  CAS  PubMed  Google Scholar 

  6. Shepherd, G. M. The human sense of smell: are we better than we think? PLoS Biol. 2, e146 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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).

    Article  CAS  PubMed  Google Scholar 

  8. Adrian, E. D. Sensory messages and sensation; the response of the olfactory organ to different smells. Acta Physiol. Scand. 29, 5–14 (1953)

    Article  CAS  PubMed  Google Scholar 

  9. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  11. Laska, M., Joshi, D. & Shepherd, G. M. Olfactory sensitivity for aliphatic aldehydes in CD-1 mice. Behav. Brain Res. 167, 349–354 (2006).

    Article  CAS  PubMed  Google Scholar 

  12. Xu, F., Greer, C. A. & Shepherd, G. M. Odor maps in the olfactory bulb. J. Comp. Neurol. 422, 489–495 (2000).

    Article  CAS  PubMed  Google Scholar 

  13. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nature Rev. Neurosci. 3, 884–895 (2002).

    Article  CAS  Google Scholar 

  15. Willhite, D. C. et al. Viral tracing identified distributed columnar organization in the olfactory bulb. Proc. Natl Acad. Sci. USA 103, 12592–12597 (2006).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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).

    Article  CAS  PubMed  Google Scholar 

  17. Shepherd, G. M. Outline of a theory of olfactory processing and its relevance to humans. Chem. Senses 30 (Suppl. 1), i3–i5 (2005).

    Article  PubMed  Google Scholar 

  18. 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).

    Google Scholar 

  19. Rozin, P. 'Taste–smell confusions' and the duality of the olfactory sense. Percept. Psychophys. 31, 397–401 (1982).

    Article  CAS  PubMed  Google Scholar 

  20. Sun, B. C. & Halpern, B. P. Identification of air phase retronasal and orthonasal odorant pairs. Chem. Senses 30, 693–706 (2005).

    Article  PubMed  Google Scholar 

  21. 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).

    Article  CAS  PubMed  Google Scholar 

  22. Shepherd-Barr, K. & Shepherd, G. M. Madeleines and neuromodernism: reassessing mechanisms of autobiographical memory in Proust. Auto/Biography Studies 13, 40–60 (1998).

    Google Scholar 

  23. 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).

    Article  CAS  Google Scholar 

  24. Bartoshuk, L. M. et al. From psychophysics to the clinic: missteps and advances. Food Qual. Preference 15, 617–632 (2004).

    Article  Google Scholar 

  25. Murphy, C., Cain, W. S. & Bartoshuk, L. M. Mutual action of taste and olfaction. Sens. Process. 1, 204–211 (1977).

    CAS  Google Scholar 

  26. Mozell, M., Smith, B., Smith, P., Sullivan, L. & Swender, P. Nasal chemoreception in flavor identification. Arch. Otolaryngol. 90, 367–373 (1969).

    Article  CAS  PubMed  Google Scholar 

  27. Farb, P. & Armelagos, G. Consuming Passions: The Anthropology of Eating (Houghton Mifflin, Boston, 1980).

    Google Scholar 

  28. 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).

    Article  CAS  PubMed  Google Scholar 

  29. Steiner, J. E. Discussion paper: innate, discriminative human facial expressions to taste and smell stimulation. Ann. NY Acad. Sci. 237, 229–233 (1974).

    Article  ADS  CAS  PubMed  Google Scholar 

  30. 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).

    Article  CAS  PubMed  Google Scholar 

  31. 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).

    Article  PubMed  Google Scholar 

  32. Rolls, E. T. Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol. Behav. 85, 45–56 (2005).

    Article  CAS  PubMed  Google Scholar 

  33. Small, D. M. et al. Experience-dependent neural integration of taste and smell in the human brain. J. Neurophysiol. 92, 1892–1903 (2004).

    Article  PubMed  Google Scholar 

  34. 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).

    Article  PubMed  Google Scholar 

  35. 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).

    Article  PubMed  Google Scholar 

  36. Morrot, G., Brochet, F. & Dubourdieu, D. The color of odors. Brain Lang. 79, 309–320 (2001).

    Article  CAS  PubMed  Google Scholar 

  37. 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).

    Article  CAS  PubMed  Google Scholar 

  38. Wilson, D. A. & Stevenson, R. J. Olfactory perceptual learning: the critical role of memory in odor discrimination. Neurosci. Biobehav. 27, 307–328 (2003).

    Article  Google Scholar 

  39. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  40. 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).

    Article  CAS  PubMed  Google Scholar 

  41. 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).

    Article  CAS  PubMed  Google Scholar 

  42. 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).

    Article  PubMed  Google Scholar 

  43. 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).

    Article  PubMed  Google Scholar 

  44. Volkow, N. D. & Wise, R. A. How can drug addiction help us understand obesity? Nature Neurosci. 8, 555–560 (2005).

    Article  CAS  PubMed  Google Scholar 

  45. Pelchat, M. L. Of human bondage: food craving, obsession, compulsion and addiction. Physiol. Behav. 76, 347–352 (2002).

    Article  CAS  PubMed  Google Scholar 

  46. Carpino, S. et al. Composition and aroma compounds of Ragusano cheese: native pasture and total mixed rations. J. Dairy Sci. 87, 816–830 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Deibler, K. D. & Delwiche, J. (eds) Handbook of Flavor Characterization: Sensory Analysis, Chemistry, and Physiology (Marcel Dekker, New York, 2003).

    Book  Google Scholar 

  48. Licitra, G. (ed.) Cheese Art 2004. Ragusa: Consorzio Ricerca Filiera Lattiero Casearia. (Ragusa, Italy, 5 Jun 2004).

    Google Scholar 

  49. 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).

    Article  CAS  PubMed  Google Scholar 

  50. Corriher, S.O. CookWise (William Morrow, New York, 1997).

    Google Scholar 

  51. McGee, H. On Food and Cooking: The Science and Lore of the Kitchen (Scribner, New York, 2004).

    Google Scholar 

  52. This, H. Molecular gastronomy. Nature Mater. 4, 5–7 (2005).

    Article  ADS  CAS  Google Scholar 

  53. Mori, K., Nagao, H. & Yoshihara, Y. The olfactory bulb: coding and processing of odor molecule information. Science 286, 711–715 (1999).

    Article  CAS  PubMed  Google Scholar 

  54. 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).

    Google Scholar 

  55. 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).

    Google Scholar 

  56. Lorig, T. S. On the similarity of odor and language perception. Neurosci. Biobehav. Rev. 23, 391–398 (1999).

    Article  CAS  PubMed  Google Scholar 

  57. Herz, R. S. The effect of verbal context on olfactory perception. J. Exp. Psychol. Gen. 132, 595–606 (2003).

    Article  PubMed  Google Scholar 

  58. Wrangham, R. & Conklin-Brittain, N. Cooking as a biological trait. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 136, 35–46 (2003).

    Article  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Gordon M. Shepherd.

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

Reprints 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

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05405

This article is cited by

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing