Patterns of cerebral activation during olfactory and trigeminal stimulations

It is well known that most odorants stimulate both the olfactory system and the trigeminal system. However, the overlap between the brain processes involved in each of these sensorial perceptions is still poorly documented. This study aims to compare fMRI brain activations while smelling two odorants of a similar perceived intensity and pleasantness: phenyl ethyl alcohol (a pure olfactory stimulus) and iso‐amyl‐acetate (a bimodal olfactory‐trigeminal stimulus) in a homogeneous sample of 15 healthy, right‐handed female subjects. The analysis deals with the contrasts of brain activation patterns between these two odorant conditions. The results showed a significant recruitment of the right insular cortex, and bilaterally in the cingulate in response to the trigeminal component. These findings are discussed in relation to the characteristics of these odorants compared with those tested in previous studies. Hum Brain Mapp, 2009. © 2008 Wiley‐Liss, Inc.

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

[2]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[3]  J. A. Boyle,et al.  Cross-modal integration of intranasal stimuli: A functional magnetic resonance imaging study , 2007, Neuroscience.

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

[5]  J. Vincent,et al.  Information processing in the mammalian olfactory system. , 2005, Physiological reviews.

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

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

[8]  A. Dravnieks,et al.  Hedonics of odors and odor descriptors , 1984 .

[9]  G. Brand,et al.  Complexity of olfactory lateralization processes revealed by functional imaging: a review , 2001, Neuroscience & Biobehavioral Reviews.

[10]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[11]  B. Gulyás,et al.  Brain activation during odor perception in males and females , 2001, Neuroreport.

[12]  T. Hummel,et al.  'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. , 1997, Chemical senses.

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

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

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

[16]  J. Schmahmann The role of the cerebellum in affect and psychosis , 2000, Journal of Neurolinguistics.

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

[18]  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.

[19]  M J Brammer,et al.  Functional MR imaging during odor stimulation: preliminary data. , 1997, Radiology.

[20]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[21]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

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

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

[25]  Frank Schneider,et al.  Same or different? Neural correlates of happy and sad mood in healthy males , 2005, NeuroImage.

[26]  G. Brand Olfactory/trigeminal interactions in nasal chemoreception , 2006, Neuroscience & Biobehavioral Reviews.

[27]  R. Goebel BRAINVOYAGER: a program for analyzing and visualizing functional and structural magnetic resonance data sets , 1996, NeuroImage.

[28]  Ivanka Savic,et al.  Processing of odorous signals in humans , 2001, Brain Research Bulletin.

[29]  W. Cain,et al.  Trigeminal and olfactory sensitivity: comparison of modalities and methods of measurement , 1998, International archives of occupational and environmental health.

[30]  Brain imaging studies of the functional organization of human olfaction. , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[31]  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.

[32]  P. Jurs,et al.  Intranasal trigeminal stimulation from odorous volatiles: Psychometric responses from anosmic and normal humans , 1978, Physiology & Behavior.

[33]  Olfactometry in fMRI studies: odor presentation using nasal continuous positive airway pressure. , 2004, Acta neurobiologiae experimentalis.

[34]  K. Hörmann,et al.  Chemosensory event-related potentials in relation to side of stimulation, age, sex, and stimulus concentration , 2006, Clinical Neurophysiology.

[35]  J. Royet,et al.  Lateralization of olfactory processes. , 2004, Chemical senses.

[36]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[37]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[38]  T. Hummel,et al.  Intranasal trigeminal function in subjects with and without an intact sense of smell , 2007, Brain Research.

[39]  C. S. Lin,et al.  Functional MRI of human olfaction. , 1997, Journal of computer assisted tomography.

[40]  R G Robinson,et al.  Neglect after right insular cortex infarction. , 1999, Stroke.

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