Spatio–temporal dynamics of olfactory processing in the human brain: an event-related source imaging study

Although brain structures involved in central nervous olfactory processing in humans have been well identified with functional neuroimaging, little is known about the temporal sequence of their activation. We recorded olfactory event-related potentials (ERP) to H(2)S stimuli presented to the left and right nostril in 12 healthy subjects. Topographic and source analysis identified four distinct processing steps between 200 and 1000 ms. Activation started ipsilateral to the stimulated nostril in the mesial and lateral temporal cortex (amygdala, parahippocampal gyrus, superior temporal gyrus, insula). Subsequently, the corresponding structures on the contralateral side became involved, followed by frontal structures at the end of the activation period. Thus, based on EEG-related data, current results suggest that olfactory information in humans is processed first ipsilaterally to the stimulated nostril and then activates the major relays in olfactory information processing in both hemispheres. Most importantly, the currently described techniques allow the investigation of the spatial processing of olfactory information at a high temporal resolution.

[1]  T. Hummel,et al.  Assessment of olfactory function. , 2006, Advances in oto-rhino-laryngology.

[2]  T. Hummel,et al.  Neuroleptic-induced parkinsonism is associated with olfactory dysfunction , 2008, Journal of Neurology.

[3]  R. Zatorre,et al.  Odor Recognition Memory in Humans: Role of Right Temporal and Orbitofrontal Regions , 1993, Brain and Cognition.

[4]  S. Morand,et al.  Electric source imaging of human brain functions , 2001, Brain Research Reviews.

[5]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[6]  Sanne Boesveldt,et al.  Signal-to-noise ratio of chemosensory event-related potentials , 2007, Clinical Neurophysiology.

[7]  Herbert G. Vaughan,et al.  THE NEURAL ORIGINS OF HUMAN EVENT‐RELATED POTENTIALS * , 1980 .

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

[9]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[10]  R. Doty,et al.  Influence of Epilepsy and Temporal Lobe Resection on Olfactory Function , 1995, Epilepsia.

[11]  J. Gottfried,et al.  Smell: central nervous processing. , 2006, Advances in oto-rhino-laryngology.

[12]  Christoph M. Michel,et al.  Spatiotemporal Dynamics of Human Cognition. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[13]  E. Rolls,et al.  The orbitofrontal cortex and beyond: From affect to decision-making , 2008, Progress in Neurobiology.

[14]  H. Stefan,et al.  Chemosensory Function in Patients With Vagal Nerve Stimulators , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[15]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  Gerd Kobal,et al.  Olfactory Event-Related Potentials , 2001 .

[17]  R. Herz.  Scents of Time , 2000 .

[18]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

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

[20]  D. Bilecen,et al.  Olfactory-induced brain activity in Parkinson's disease relates to the expression of event-related potentials: a functional magnetic resonance imaging study , 2009, Neuroscience.

[21]  Riitta Salmelin,et al.  Electromagnetic brain imaging , 2009, Human brain mapping.

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

[23]  T. Hummel,et al.  Is there directional smelling? , 1989, Experientia.

[24]  Christoph M. Michel,et al.  Principles of Topographic Analyses for Electrical Neuroimaging , 2009 .

[25]  B. Slotnick,et al.  The olfactory thalamocortical system and odor reversal learning examined using an asymmetrical lesion paradigm in rats. , 1997, Behavioral neuroscience.

[26]  D. Lehmann,et al.  Event-related potentials of the brain and cognitive processes: Approaches and applications , 1986, Neuropsychologia.

[27]  Christoph M. Michel,et al.  Early neuronal responses in right limbic structures mediate harmony incongruity processing in musical experts , 2008, NeuroImage.

[28]  Todd C. Handy.  Brain Signal Analysis: Advances In Neuroelectric and Neuromagnetic Methods , 2011 .

[29]  Dietrich Lehmann,et al.  Spatial analysis of evoked potentials in man—a review , 1984, Progress in Neurobiology.

[30]  P. Rossini,et al.  High-resolution electro-encephalogram: source estimates of Laplacian-transformed somatosensory-evoked potentials using a realistic subject head model constructed from magnetic resonance images , 2000, Medical and Biological Engineering and Computing.

[31]  H. Stefan,et al.  Chemosensory Event‐Related Potentials in Patients with Temporal Lobe Epilepsy , 1995, Epilepsia.

[32]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

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

[34]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. II. Demonstration of Sublobar Accuracy in Patients with Simultaneous Surface and Depth Recordings , 2004, Brain Topography.

[35]  E. Rolls,et al.  Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  E. Rolls,et al.  Cognitive Modulation of Olfactory Processing , 2005, Neuron.

[37]  Richard Axel.  The molecular logic of smell. , 1995 .

[38]  E. Rolls.  Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion. , 2008, Acta physiologica Hungarica.

[39]  R J Zatorre,et al.  Contribution of medial versus lateral temporal-lobe structures to human odour identification. , 1997, Brain : a journal of neurology.

[40]  Thomas Koenig,et al.  Electrical Neuroimaging in the time domain , 2009 .

[41]  M. Curtis,et al.  Polysynaptic olfactory pathway to the ipsi- and contralateral entorhinal cortex mediated via the hippocampus , 2005, Neuroscience.

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

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

[44]  B Sojka,et al.  The nature of the late positive complex within the olfactory event-related potential (OERP). , 1996, Psychophysiology.

[45]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

[46]  André Duchamp,et al.  QUALITATIVE AND QUANTITATIVE DISCRIMINATION IN THE FROG OLFACTORY RECEPTORS: ANALYSIS FROM ELECTROPHYSIOLOGICAL DATA , 1974, Annals of the New York Academy of Sciences.

[47]  T. Hummel,et al.  Kallmann's syndrome and chemosensory evoked potentials , 2004, European Archives of Oto-Rhino-Laryngology.

[48]  C. Michel,et al.  Electromagnetic Inverse Solutions in Anatomically Constrained Spherical Head Models , 2004, Brain Topography.

[49]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[50]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[51]  Jörn Lötsch,et al.  Olfactory function in mild cognitive impairment and Alzheimer's disease: an investigation using psychophysical and electrophysiological techniques. , 2003, The American journal of psychiatry.

[52]  M. T. Shipley,et al.  Anatomical evidence for convergence of olfactory, gustatory, and visceral afferent pathways in mouse cerebral cortex , 1984, Brain Research Bulletin.

[53]  Riitta Salmelin,et al.  Odorants activate the human superior temporal sulcus , 1996, Neuroscience Letters.

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

[55]  R. Kakigi,et al.  Neuromagnetic Changes of Brain Rhythm Evoked by Intravenous Olfactory Stimulation in Humans , 2006, Brain Topography.

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

[57]  Gordon M. Shepherd,et al.  Olfactory cortex , 1998 .

[58]  I Savic,et al.  PET shows that odors are processed both ipsilaterally and contralaterally to the stimulated nostril , 2000, Neuroreport.

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

[60]  G Kobal,et al.  Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa. , 1988, Electroencephalography and clinical neurophysiology.

[61]  T. Hummel,et al.  Functional Imaging of Olfactory Activation in the Human Brain , 2001 .

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

[63]  R. Wennberg,et al.  Source localization of mesial temporal interictal epileptiform discharges: Correlation with intracranial foramen ovale electrode recordings , 2005, Clinical Neurophysiology.

[64]  Stéphanie Morand,et al.  Neural transition from short‐ to long‐term memory and the medial temporal lobe: A human evoked‐potential study , 2009, Hippocampus.

[65]  Yoshimi Anzai,et al.  In vivo imaging of functional disruption, recovery and alteration in rat olfactory circuitry after lesion , 2006, NeuroImage.

[66]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

[67]  John J. Foxe,et al.  Boundary Completion Is Automatic and Dissociable from Shape Discrimination , 2006, The Journal of Neuroscience.

[68]  M. N. Chong,et al.  Concurrent computing for picture archiving and communication system , 2006, Medical and Biological Engineering and Computing.