Skip to main content
SpringerLink
Log in

The Role of the Piriform Cortex in Human Olfactory Perception: Insights from Functional Neuroimaging Studies

  • Published:
Chemosensory Perception

Abstract

Functional neuroimaging studies of the olfactory system during the last two decades have studied the role of the piriform cortex (PC) in human olfaction. Whereas some reported absence of PC activation, most suggested that the PC is more than a relay and plays an active role from sensory to more cognitive aspects of human olfactory perception. The aim of the present review is to clarify our current understanding of the role of the PC in human odor perception, by underscoring the sensory and cognitive factors which are important in piriform activity modulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albrecht J, Kopietz R, Linn J, Sakar V, Anzinger A, Schreder T, Pollatos O, Bruckmann H, Kobal G, Wiesmann M (2009) Activation of olfactory and trigeminal cortical areas following stimulation of the nasal mucosa with low concentrations of S(-)-nicotine vapor–an fMRI study on chemosensory perception. Hum Brain Mapp 30:699–710

    Article  Google Scholar 

  • Algom D, Cain WS (1991) Remembered odors and mental mixtures: tapping reservoirs of olfactory knowledge. J Exp Psychol Hum Percept Perform 17:1104–1119

    Article  CAS  Google Scholar 

  • Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, Gabrieli JD, Sobel N (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6:196–202

    Article  CAS  Google Scholar 

  • Bensafi M, Sobel N, Khan RM (2007) Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. J Neurophysiol 98:3254–3262

    Article  Google Scholar 

  • Bensafi M, Iannilli E, Gerber J, Hummel T (2008) Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems. Neuroscience 154:832–838

    Article  CAS  Google Scholar 

  • Billot PE, Comte A, Galliot E, Andrieu P, Bonnans V, Tatu L, Gharbi T, Moulin T, Millot JL (2011) Time course of odorant- and trigeminal-induced activation in the human brain: an event-related functional magnetic resonance imaging study. Neuroscience 189:370–376

    Article  CAS  Google Scholar 

  • Boyle JA, Heinke M, Gerber J, Frasnelli J, Hummel T (2007) Cerebral activation to intranasal chemosensory trigeminal stimulation. Chem Senses 32:343–353

    Article  Google Scholar 

  • Boyle JA, Djordjevic J, Olsson MJ, Lundstrom JN, Jones-Gotman M (2009) The human brain distinguishes between single odorants and binary mixtures. Cereb Cortex 19:66–71

    Article  Google Scholar 

  • Carrasco M, Ridout JB (1993) Olfactory perception and olfactory imagery: a multidimensional analysis. J Exp Psychol Hum Percept Perform 19:287–301

    Article  CAS  Google Scholar 

  • Cerf-Ducastel B, Murphy C (2003) FMRI brain activation in response to odors is reduced in primary olfactory areas of elderly subjects. Brain Res 986:39–53

    Article  CAS  Google Scholar 

  • Cerf-Ducastel B, Murphy C (2006) Neural substrates of cross-modal olfactory recognition memory: an fMRI study. NeuroImage 31:386–396

    Article  Google Scholar 

  • Ciumas C, Lindstrom P, Aoun B, Savic I (2008) Imaging of odor perception delineates functional disintegration of the limbic circuits in mesial temporal lobe epilepsy. NeuroImage 39:578–592

    Article  Google Scholar 

  • Cleland T, Linster C (2003) Central olfactory structures. In: Doty R (ed) Handbook of olfaction and gustation, 2nd edn. Marcel Dekker, Inc, New York, pp 165–180

    Google Scholar 

  • Dade LA, Jones-Gotman M, Zatorre RJ, Evans AC (1998) Human brain function during odor encoding and recognition. A PET activation study. Ann N Y Acad Sci 855:572–574

    Article  CAS  Google Scholar 

  • Dade LA, Zatorre RJ, Evans AC, Jones-Gotman M (2001) Working memory in another dimension: functional imaging of human olfactory working memory. NeuroImage 14:650–660

    Article  CAS  Google Scholar 

  • Dade LA, Zatorre RJ, Jones-Gotman M (2002) Olfactory learning: convergent findings from lesion and brain imaging studies in humans. Brain 125:86–101

    Article  Google Scholar 

  • Djordjevic J, Zatorre RJ, Petrides M, Boyle JA, Jones-Gotman M (2005) Functional neuroimaging of odor imagery. NeuroImage 24:791–801

    Article  CAS  Google Scholar 

  • Elmes DG (1998) Is there an inner nose? Chem Senses 23:443–445

    Article  CAS  Google Scholar 

  • Frasnelli J, Lundstrom JN, Boyle JA, Katsarkas A, Jones-Gotman M (2011) The vomeronasal organ is not involved in the perception of endogenous odors. Hum Brain Mapp 32:450–460

    Article  Google Scholar 

  • Fulbright RK, Skudlarski P, Lacadie CM, Warrenburg S, Bowers AA, Gore JC, Wexler BE (1998) Functional MR imaging of regional brain responses to pleasant and unpleasant odors. AJNR Am J Neuroradiol 19:1721–1726

    CAS  Google Scholar 

  • Gonzalez J, Barros-Loscertales A, Pulvermuller F, Meseguer V, Sanjuan A, Belloch V, Avila C (2006) Reading cinnamon activates olfactory brain regions. NeuroImage 32:906–912

    Article  Google Scholar 

  • Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11:628–641

    Article  CAS  Google Scholar 

  • Gottfried JA, Dolan RJ (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39:375–386

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Gottfried JA, Smith AP, Rugg MD, Dolan RJ (2004) Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron 42:687–695

    Article  CAS  Google Scholar 

  • Gottfried JA, Winston JS, Dolan RJ (2006) Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49:467–479

    Article  CAS  Google Scholar 

  • Grabenhorst F, Rolls ET (2009) Different representations of relative and absolute subjective value in the human brain. NeuroImage 48:258–268

    Article  Google Scholar 

  • Grabenhorst F, Rolls ET, Margot C, da Silva MA, Velazco MI (2007) How pleasant and unpleasant stimuli combine in different brain regions: odor mixtures. J Neurosci 27:13532–13540

    Article  CAS  Google Scholar 

  • Heilmann S, Hummel T (2004) A new method for comparing orthonasal and retronasal olfaction. Behav Neurosci 118:412–419

    Article  Google Scholar 

  • Herz RS, Eliassen J, Beland S, Souza T (2004) Neuroimaging evidence for the emotional potency of odor-evoked memory. Neuropsychologia 42:371–378

    Article  Google Scholar 

  • Howard JD, Plailly J, Grueschow M, Haynes JD, Gottfried JA (2009) Odor quality coding and categorization in human posterior piriform cortex. Nat Neurosci 12:932–938

    Article  CAS  Google Scholar 

  • Isaacson JS (2011) Odor representations in mammalian cortical circuits. Curr Opin Neurobiol 20:328–331

    Article  Google Scholar 

  • Ishii A, Roudnitzky N, Beno N, Bensafi M, Hummel T, Rouby C, Thomas-Danguin T (2008) Synergy and masking in odor mixtures: an electrophysiological study of orthonasal vs. retronasal perception. Chem Senses 33:553–561

    Article  CAS  Google Scholar 

  • Jeannerod M, Frak V (1999) Mental imaging of motor activity in humans. Curr Opin Neurobiol 9:735–739

    Article  CAS  Google Scholar 

  • Kadohisa M, Wilson DA (2006) Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci U S A 103:15206–15211

    Article  CAS  Google Scholar 

  • Kareken DA, Mosnik DM, Doty RL, Dzemidzic M, Hutchins GD (2003) Functional anatomy of human odor sensation, discrimination, and identification in health and aging. Neuropsychology 17:482–495

    Article  Google Scholar 

  • Kareken DA, Sabri M, Radnovich AJ, Claus E, Foresman B, Hector D, Hutchins GD (2004) Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex. NeuroImage 22:456–465

    Article  Google Scholar 

  • Kosslyn SM, Thompson WL (2003) When is early visual cortex activated during visual mental imagery? Psychol Bull 129:723–746

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Li W, Howard JD, Gottfried JA (2011) Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 133:2714–2726

    Article  Google Scholar 

  • Litaudon P, Datiche F, Cattarelli M (1997) Optical recording of the rat piriform cortex activity. Prog Neurobiol 52:485–510

    Article  CAS  Google Scholar 

  • Lombion S, Comte A, Tatu L, Brand G, Moulin T, Millot JL (2009) Patterns of cerebral activation during olfactory and trigeminal stimulations. Hum Brain Mapp 30:821–828

    Article  Google Scholar 

  • Lundstrom JN, Boyle JA, Zatorre RJ, Jones-Gotman M (2008) Functional neuronal processing of body odors differs from that of similar common odors. Cereb Cortex 18:1466–1474

    Article  Google Scholar 

  • Lundstrom JN, Boyle JA, Zatorre RJ, Jones-Gotman M (2009) The neuronal substrates of human olfactory based kin recognition. Hum Brain Mapp 30:2571–2580

    Article  Google Scholar 

  • Osterbauer RA, Matthews PM, Jenkinson M, Beckmann CF, Hansen PC, Calvert GA (2005) Color of scents: chromatic stimuli modulate odor responses in the human brain. J Neurophysiol 93:3434–3441

    Article  Google Scholar 

  • Plailly J, Bensafi M, Pachot-Clouard M, Delon-Martin C, Kareken DA, Rouby C, Segebarth C, Royet JP (2005) Involvement of right piriform cortex in olfactory familiarity judgments. NeuroImage 24:1032–1041

    Article  Google Scholar 

  • Plailly J, d'Amato T, Saoud M, Royet JP (2006) Left temporo-limbic and orbital dysfunction in schizophrenia during odor familiarity and hedonicity judgments. NeuroImage 29:302–313

    Article  Google Scholar 

  • Plailly J, Radnovich AJ, Sabri M, Royet JP, Kareken DA (2007) Involvement of the left anterior insula and frontopolar gyrus in odor discrimination. Hum Brain Mapp 28:363–372

    Article  Google Scholar 

  • Plailly J, Howard JD, Gitelman DR, Gottfried JA (2008) Attention to odor modulates thalamocortical connectivity in the human brain. J Neurosci 28:5257–5267

    Article  CAS  Google Scholar 

  • Plailly J, Delon-Martin C, Royet JP (2011) Experience induces functional reorganization in brain regions involved in odor imagery in perfumers. Hum Brain Mapp. doi:10.1002/hbm.21207

  • 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

    Article  CAS  Google Scholar 

  • Porter J, Anand T, Johnson B, Khan RM, Sobel N (2005) Brain mechanisms for extracting spatial information from smell. Neuron 47:581–592

    Article  CAS  Google Scholar 

  • Qureshy A, Kawashima R, Imran MB, Sugiura M, Goto R, Okada K, Inoue K, Itoh M, Schormann T, Zilles K, Fukuda H (2000) Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol 84:1656–1666

    CAS  Google Scholar 

  • Reske M, Kellermann T, Shah NJ, Schneider F, Habel U (2010) Impact of valence and age on olfactory induced brain activation in healthy women. Behav Neurosci 124:414–422

    Article  Google Scholar 

  • Rinck F, Rouby C, Bensafi M (2009) Which format for odor images? Chem Senses 34:11–13

    Article  Google Scholar 

  • Rolls ET, Kringelbach ML, de Araujo IE (2003) Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci 18:695–703

    Article  Google Scholar 

  • Rolls ET, Grabenhorst F, Margot C, da Silva MA, Velazco MI (2008) Selective attention to affective value alters how the brain processes olfactory stimuli. J Cogn Neurosci 20:1815–1826

    Article  Google Scholar 

  • Rouby C, Bourgeat F, Rinck F, Poncelet J, Bensafi M (2009) Perceptual and sensorimotor differences between "good" and "poor" olfactory mental imagers. Ann N Y Acad Sci 1170:333–337

    Article  Google Scholar 

  • Royet JP, Koenig O, Gregoire MC, Cinotti L, Lavenne F, Le Bars D, Costes N, Vigouroux M, Farget V, Sicard G, Holley A, Mauguiere F, Comar D, Froment JC (1999) Functional anatomy of perceptual and semantic processing for odors. J Cogn Neurosci 11:94–109

    Article  CAS  Google Scholar 

  • Royet JP, Zald D, Versace R, Costes N, Lavenne F, Koenig O, Gervais R (2000) Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: a positron emission tomography study. J Neurosci 20:7752–7759

    CAS  Google Scholar 

  • Royet JP, Hudry J, Zald DH, Godinot D, Gregoire MC, Lavenne F, Costes N, Holley A (2001) Functional neuroanatomy of different olfactory judgments. NeuroImage 13:506–519

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Royet JP, Morin-Audebrand L, Cerf-Ducastel B, Haase L, Issanchou S, Murphy C, Fonlupt P, Sulmont-Rosse C, Plailly J (2011) True and false recognition memories of odors induce distinct neural signatures. Front Hum Neurosci 5:65

    Article  Google Scholar 

  • Rozin P (1982) "Taste-smell confusions" and the duality of the olfactory sense. Percept Psychophys 31:397–401

    Article  CAS  Google Scholar 

  • Sabri M, Radnovich AJ, Li TQ, Kareken DA (2005) Neural correlates of olfactory change detection. NeuroImage 25:969–974

    Article  Google Scholar 

  • Savic I, Berglund H (2004) Passive perception of odors and semantic circuits. Hum Brain Mapp 21:271–278

    Article  Google Scholar 

  • Savic I, Gulyas B, Larsson M, Roland P (2000) Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26:735–745

    Article  CAS  Google Scholar 

  • Savic I, Berglund H, Gulyas B, Roland P (2001) Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31:661–668

    Article  CAS  Google Scholar 

  • Savic I, Gulyas B, Berglund H (2002) Odorant differentiated pattern of cerebral activation: comparison of acetone and vanillin. Hum Brain Mapp 17:17–27

    Article  Google Scholar 

  • Savic I, Berglund H, Lindstrom P (2005) Brain response to putative pheromones in homosexual men. Proc Natl Acad Sci U S A 102:7356–7361

    Article  CAS  Google Scholar 

  • Savic I, Heden-Blomqvist E, Berglund H (2009) Pheromone signal transduction in humans: what can be learned from olfactory loss. Hum Brain Mapp 30:3057–3065

    Article  Google Scholar 

  • Small DM, Gerber JC, Mak YE, Hummel T (2005) Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47:593–605

    Article  CAS  Google Scholar 

  • Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392:282–286

    Article  CAS  Google Scholar 

  • Sobel N, Prabhakaran V, Zhao Z, Desmond JE, Glover GH, Sullivan EV, Gabrieli JD (2000) Time course of odorant-induced activation in the human primary olfactory cortex. J Neurophysiol 83:537–551

    CAS  Google Scholar 

  • Sobel N, Johnson B, Mainland J, Yousem D (2003) Functional neuroimaging of human olfaction. In: Doty R (ed) Handbook of olfaction and gustation, 2nd edn. Marcel Dekker, Inc, New York, pp 251–273

    Google Scholar 

  • Veldhuizen MG, Small DM (2011) Modality-specific neural effects of selective attention to taste and odor. Chem Senses 36:747–760

    Article  Google Scholar 

  • Wilson DA (2003) Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. J Neurophysiol 90:65–72

    Article  Google Scholar 

  • Wilson JM, Jezzard P (2002) Optimization of static field homogeneity in human brain using diamagnetic passive shims. Magn Reson Med 48:906–914

    Article  Google Scholar 

  • Wilson DA, Rennaker RL (2011) Cortical activity evoked by odors. In: Menini A (ed) The neurobiology of olfaction, p Chapter 14. FL: Boca Raton

  • Yousem DM, Maldjian JA, Hummel T, Alsop DC, Geckle RJ, Kraut MA, Doty RL (1999) The effect of age on odor-stimulated functional MR imaging. AJNR Am J Neuroradiol 20:600–608

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zatorre RJ, Halpern AR (2005) Mental concerts: musical imagery and auditory cortex. Neuron 47:9–12

    Article  CAS  Google Scholar 

  • Zatorre RJ, Jones-Gotman M (1991) Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain 114(Pt 1A):71–84

    Google Scholar 

  • Zatorre RJ, Jones-Gotman M, Evans AC, Meyer E (1992) Functional localization and lateralization of human olfactory cortex. Nature 360:339–340

    Article  CAS  Google Scholar 

  • Zatorre RJ, Jones-Gotman M, Rouby C (2000) Neural mechanisms involved in odor pleasantness and intensity judgments. Neuroreport 11:2711–2716

    Article  CAS  Google Scholar 

  • Zelano C, Bensafi M, Porter J, Mainland J, Johnson B, Bremner E, Telles C, Khan R, Sobel N (2005) Attentional modulation in human primary olfactory cortex. Nat Neurosci 8:114–120

    Article  CAS  Google Scholar 

  • Zelano C, Montag J, Johnson B, Khan R, Sobel N (2007) Dissociated representations of irritation and valence in human primary olfactory cortex. J Neurophysiol 97:1969–1976

    Article  CAS  Google Scholar 

  • Zelano C, Montag J, Khan R, Sobel N (2009) A specialized odor memory buffer in primary olfactory cortex. PLoS One 4:e4965

    Article  Google Scholar 

  • Zhou W, Chen D (2008) Encoding human sexual chemosensory cues in the orbitofrontal and fusiform cortices. J Neurosci 28:14416–14421

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. CNRS, UMR5292, INSERM, U1028, Lyon Neuroscience Research Center, Neuroplasticity and Neuropathology of Olfactory Perception Team, University of Lyon, 50 av Tony Garnier, 69007, Lyon, France

    Moustafa Bensafi

Authors
  1. Moustafa Bensafi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Moustafa Bensafi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bensafi, M. The Role of the Piriform Cortex in Human Olfactory Perception: Insights from Functional Neuroimaging Studies. Chem. Percept. 5, 4–10 (2012). https://doi.org/10.1007/s12078-011-9110-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12078-011-9110-8

Keywords

Search

Navigation