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

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.

[1]  Donald A Wilson,et al.  Separate encoding of identity and similarity of complex familiar odors in piriform cortex , 2006, Proceedings of the National Academy of Sciences.

[2]  Barbara Cerf-Ducastel,et al.  Neural substrates of cross-modal olfactory recognition memory: An fMRI study , 2006, NeuroImage.

[3]  Jane Plailly,et al.  Left temporo-limbic and orbital dysfunction in schizophrenia during odor familiarity and hedonicity judgments , 2006, NeuroImage.

[4]  Gilles Sicard,et al.  Functional Anatomy of Perceptual and Semantic Processing for Odors , 1999, Journal of Cognitive Neuroscience.

[5]  R. Dolan,et al.  The Nose Smells What the Eye Sees Crossmodal Visual Facilitation of Human Olfactory Perception , 2003, Neuron.

[6]  Alan C. Evans,et al.  Working Memory in Another Dimension: Functional Imaging of Human Olfactory Working Memory , 2001, NeuroImage.

[7]  Ivanka Savic,et al.  Brain response to putative pheromones in homosexual men. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Moustafa Bensafi,et al.  Which format for odor images? , 2008, Chemical senses.

[9]  Dana M Small,et al.  Modality-specific neural effects of selective attention to taste and odor. , 2011, Chemical senses.

[10]  T. Hummel,et al.  A new method for comparing orthonasal and retronasal olfaction. , 2004, Behavioral neuroscience.

[11]  Chantal Delon-Martin,et al.  fMRI of emotional responses to odors: influence of hedonic valence and judgment, handedness, and gender , 2003, NeuroImage.

[12]  M. Cattarelli,et al.  Optical recording of the rat piriform cortex activity , 1997, Progress in Neurobiology.

[13]  I. Savic,et al.  Pheromone signal transduction in humans: What can be learned from olfactory loss , 2009, Human brain mapping.

[14]  Fabian Grabenhorst,et al.  How Pleasant and Unpleasant Stimuli Combine in Different Brain Regions: Odor Mixtures , 2007, The Journal of Neuroscience.

[15]  D. Gitelman,et al.  Attention to Odor Modulates Thalamocortical Connectivity in the Human Brain , 2008, The Journal of Neuroscience.

[16]  Alan C. Evans,et al.  Human Brain Function during Odor Encoding and Recognition: A PET Activation Study a , 1998, Annals of the New York Academy of Sciences.

[17]  Donald A. Wilson,et al.  Cortical Activity Evoked by Odors , 2010 .

[18]  D. Yousem,et al.  The effect of age on odor-stimulated functional MR imaging. , 1999, AJNR. American journal of neuroradiology.

[19]  M. Wiesmann,et al.  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 , 2009, Human brain mapping.

[20]  Noam Sobel,et al.  Functional Neuroimaging of Human Olfaction , 2003 .

[21]  B. Gulyás,et al.  Odorant differentiated pattern of cerebral activation: Comparison of acetone and vanillin , 2002, Human brain mapping.

[22]  M. Bensafi,et al.  Perceptual and Sensorimotor Differences between “Good” and “Poor” Olfactory Mental Imagers , 2009, Annals of the New York Academy of Sciences.

[23]  C. Linster,et al.  Central Olfactory Structures , 2003 .

[24]  David A. Kareken,et al.  Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex , 2004, NeuroImage.

[25]  R J Zatorre,et al.  Human olfactory discrimination after unilateral frontal or temporal lobectomy. , 1991, Brain : a journal of neurology.

[26]  Jane Plailly,et al.  True and False Recognition Memories of Odors Induce Distinct Neural Signatures , 2011, Front. Hum. Neurosci..

[27]  D. Kareken,et al.  Functional anatomy of human odor sensation, discrimination, and identification in health and aging. , 2003, Neuropsychology.

[28]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[29]  James Eliassen,et al.  Neuroimaging evidence for the emotional potency of odor-evoked memory , 2004, Neuropsychologia.

[30]  M. Bensafi,et al.  Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems , 2008, Neuroscience.

[31]  U. Habel,et al.  Impact of valence and age on olfactory induced brain activation in healthy women. , 2010, Behavioral neuroscience.

[32]  Thierry Moulin,et al.  Patterns of cerebral activation during olfactory and trigeminal stimulations , 2009, Human brain mapping.

[33]  Michael D Rugg,et al.  Remembrance of Odors Past Human Olfactory Cortex in Cross-Modal Recognition Memory , 2004, Neuron.

[34]  Brad Johnson,et al.  Dissociated representations of irritation and valence in human primary olfactory cortex. , 2007, Journal of neurophysiology.

[35]  Mark Jenkinson,et al.  Color of scents: chromatic stimuli modulate odor responses in the human brain. , 2005, Journal of neurophysiology.

[36]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[37]  D. Elmes.  Is there an inner nose? , 1998, Chemical senses.

[38]  M. Jones-Gotman,et al.  The vomeronasal organ is not involved in the perception of endogenous odors , 2011, Human brain mapping.

[39]  B. Gulyás,et al.  Olfactory Functions Are Mediated by Parallel and Hierarchical Processing , 2000, Neuron.

[40]  Ralf Deichmann,et al.  Functional Heterogeneity in Human Olfactory Cortex: An Event-Related Functional Magnetic Resonance Imaging Study , 2002, The Journal of Neuroscience.

[41]  Mark Jenkinson,et al.  Optimization of static field homogeneity in human brain using diamagnetic passive shims , 2002, Magnetic resonance in medicine.

[42]  M. Carrasco,et al.  Olfactory perception and olfactory imagery: a multidimensional analysis. , 1993, Journal of experimental psychology. Human perception and performance.

[43]  G H Glover,et al.  Time course of odorant-induced activation in the human primary olfactory cortex. , 2000, Journal of neurophysiology.

[44]  Edmund T. Rolls,et al.  Selective Attention to Affective Value Alters How the Brain Processes Olfactory Stimuli , 2008, Journal of Cognitive Neuroscience.

[45]  M. Bensafi,et al.  Synergy and masking in odor mixtures: an electrophysiological study of orthonasal vs. retronasal perception. , 2008, Chemical senses.

[46]  I. Savic,et al.  Passive perception of odors and semantic circuits , 2004, Human brain mapping.

[47]  M. Jones-Gotman,et al.  The human brain distinguishes between single odorants and binary mixtures. , 2009, Cerebral cortex.

[48]  E. Rolls,et al.  Different representations of pleasant and unpleasant odours in the human brain , 2003, The European journal of neuroscience.

[49]  P. Rozin,et al.  “Taste-smell confusions” and the duality of the olfactory sense , 1982, Perception & Psychophysics.

[50]  Alexander J. Radnovich,et al.  Involvement of the left anterior insula and frontopolar gyrus in odor discrimination , 2007, Human brain mapping.

[51]  T. Schormann,et al.  Functional mapping of human brain in olfactory processing: a PET study. , 2000, Journal of neurophysiology.

[52]  C. Delon-Martin,et al.  Experience induces functional reorganization in brain regions involved in odor imagery in perfumers , 2012, Human brain mapping.

[53]  J. Isaacson,et al.  Odor representations in mammalian cortical circuits , 2010, Current Opinion in Neurobiology.

[54]  Robert J. Zatorre,et al.  Mental Concerts: Musical Imagery and Auditory Cortex , 2005, Neuron.

[55]  M. Jeannerod,et al.  Mental imaging of motor activity in humans , 1999, Current Opinion in Neurobiology.

[56]  R. Zatorre,et al.  Neural mechanisms involved in odor pleasantness and intensity judgments , 2000, Neuroreport.

[57]  T. Gharbi,et al.  Time course of odorant- and trigeminal-induced activation in the human brain: an event-related functional magnetic resonance imaging study , 2011, Neuroscience.

[58]  D. Small,et al.  Differential Neural Responses Evoked by Orthonasal versus Retronasal Odorant Perception in Humans , 2005, Neuron.

[59]  Raymond J. Dolan,et al.  Dissociable Codes of Odor Quality and Odorant Structure in Human Piriform Cortex , 2006, Neuron.

[60]  Donald A Wilson,et al.  Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. , 2003, Journal of neurophysiology.

[61]  W S Cain,et al.  Remembered odors and mental mixtures: tapping reservoirs of olfactory knowledge. , 1991, Journal of experimental psychology. Human perception and performance.

[62]  Thomas Hummel,et al.  Cerebral activation to intranasal chemosensory trigeminal stimulation. , 2007, Chemical senses.

[63]  J. D. E. Gabrieli,et al.  Sniffing and smelling: separate subsystems in the human olfactory cortex , 1998, Nature.

[64]  Friedemann Pulvermüller,et al.  Reading cinnamon activates olfactory brain regions , 2006, NeuroImage.

[65]  R. Zatorre,et al.  The neuronal substrates of human olfactory based kin recognition , 2009, Human brain mapping.

[66]  J. Gottfried.  Central mechanisms of odour object perception , 2010, Nature Reviews Neuroscience.

[67]  David A. Kareken,et al.  Neural correlates of olfactory change detection , 2005, NeuroImage.

[68]  B. Gulyás,et al.  Smelling of Odorous Sex Hormone-like Compounds Causes Sex-Differentiated Hypothalamic Activations in Humans , 2001, Neuron.

[69]  Alan C. Evans,et al.  Functional localization and lateralization of human olfactory cortex , 1992, Nature.

[70]  Chantal Delon-Martin,et al.  Involvement of right piriform cortex in olfactory familiarity judgments , 2005, NeuroImage.

[71]  John-Dylan Haynes,et al.  Odor quality coding and categorization in human posterior piriform cortex , 2009, Nature Neuroscience.

[72]  Robert J Zatorre,et al.  Olfactory learning: convergent findings from lesion and brain imaging studies in humans. , 2002, Brain : a journal of neurology.

[73]  J. Gottfried,et al.  Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. , 2010, Brain : a journal of neurology.

[74]  J. Pardo,et al.  Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[75]  C. Zelano,et al.  A Specialized Odor Memory Buffer in Primary Olfactory Cortex , 2009, PloS one.

[76]  N. Costes,et al.  Emotional Responses to Pleasant and Unpleasant Olfactory, Visual, and Auditory Stimuli: a Positron Emission Tomography Study , 2000, The Journal of Neuroscience.

[77]  T. Parrish,et al.  Learning to Smell the Roses: Experience-Dependent Neural Plasticity in Human Piriform and Orbitofrontal Cortices , 2006, Neuron.

[78]  Noam Sobel,et al.  Attentional modulation in human primary olfactory cortex , 2005, Nature Neuroscience.

[79]  Bruce R. Rosen,et al.  Activation and Habituation in Olfaction—An fMRI Study , 2001, NeuroImage.

[80]  R. Zatorre,et al.  Functional neuronal processing of body odors differs from that of similar common odors. , 2008, Cerebral cortex.

[81]  S. Kosslyn,et al.  When is early visual cortex activated during visual mental imagery? , 2003, Psychological bulletin.

[82]  Noam Sobel,et al.  Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. , 2007, Journal of neurophysiology.

[83]  Edmund T. Rolls,et al.  Different representations of relative and absolute subjective value in the human brain , 2009, NeuroImage.

[84]  B. Cerf-Ducastel,et al.  FMRI brain activation in response to odors is reduced in primary olfactory areas of elderly subjects , 2003, Brain Research.

[85]  Jessica Porter,et al.  Brain Mechanisms for Extracting Spatial Information from Smell , 2005, Neuron.

[86]  P. Skudlarski,et al.  Functional MR imaging of regional brain responses to pleasant and unpleasant odors. , 1998, AJNR. American journal of neuroradiology.

[87]  Wen Zhou,et al.  Encoding Human Sexual Chemosensory Cues in the Orbitofrontal and Fusiform Cortices , 2008, The Journal of Neuroscience.

[88]  Carolina Ciumas,et al.  Imaging of odor perception delineates functional disintegration of the limbic circuits in mesial temporal lobe epilepsy , 2008, NeuroImage.

[89]  A. Holley,et al.  Functional Neuroanatomy of Different Olfactory Judgments , 2001, NeuroImage.

[90]  M. Petrides,et al.  Functional neuroimaging of odor imagery , 2005, NeuroImage.