Individual differences in prefrontal cortex activity during perception of bitter taste using fNIRS methodology.

Although bitter taste has a crucial role in nutrition by preventing the ingestion of toxic foods, there are few studies on bitter taste neuroimaging. To identify cortical areas involved in bitter taste perception and to determine if individual differences in taste sensitivity to 6-n-propylthiouracil (PROP) are represented in the brain by different cortical activation patterns, we examined 48 healthy volunteers using functional near-infrared spectroscopy. Participants rated the perceived intensity of filter paper disks impregnated with PROP and NaCl during the imaging procedure and were then classified as PROP tasters and nontasters. We monitored cortical activity in both the anterior and posterior regions of the dorsolateral prefrontal cortex (DLPFC) and in the ventrolateral prefrontal cortex (VLPFC). No activity was detected in the anterior DLPFC in any of the participants. However, during the administration of PROP, significant cortical activation was detected in the more posterior regions of the left DLPFC and in the left and right VLPFC but only in PROP tasters. PROP nontasters showed no cortical activity in these areas. These data suggest that the prefrontal cortex is involved in the conscious perception of the bitter taste of PROP and that the pattern of activity is consistent with individual differences in the ability to taste this compound. Thus, the PROP phenotype is associated with fundamental differences in cortical taste processing.

[1]  Mark Leppert,et al.  Positional Cloning of the Human Quantitative Trait Locus Underlying Taste Sensitivity to Phenylthiocarbamide , 2003, Science.

[2]  A. Blakeslee,et al.  OUR DIFFERENT TASTE WORLDS P. T. C. as a Demonstration of Genetic Differences in Taste , 1932 .

[3]  P. Gasparini,et al.  Variation in the Bitter‐taste Receptor Gene TAS2R38, and Adiposity in a Genetically Isolated Population in Southern Italy , 2008, Obesity.

[4]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[5]  Archana K. Singh,et al.  Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI , 2005, NeuroImage.

[6]  M. Behrens,et al.  Signaling in chemosensory systems , 2006, Cellular and Molecular Life Sciences CMLS.

[7]  T Kobayakawa,et al.  Functional MRI detection of activation in the primary gustatory cortices in humans. , 2005, Chemical senses.

[8]  P. Shi,et al.  Extraordinary diversity of chemosensory receptor gene repertoires among vertebrates. , 2009, Results and problems in cell differentiation.

[9]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[10]  Judith R Kidd,et al.  Supertasting and PROP bitterness depends on more than the TAS2R38 gene. , 2008, Chemical senses.

[11]  J. Hebden,et al.  Diagnostic imaging with light. , 1997, The British journal of radiology.

[12]  L. Leguire,et al.  Using FMRI and FNIRS for localization and monitoring of visual cortex activities , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[13]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[14]  H. Kalmus,et al.  IMPROVEMENTS IN THE CLASSIFICATION OF THE TASTER GENOTYPES , 1958, Annals of human genetics.

[15]  Tsunehiro Takeda,et al.  The primary gustatory area in human cerebral cortex studied by magnetoencephalography , 1996, Neuroscience Letters.

[16]  D. Reed,et al.  The genetics of phenylthiocarbamide perception. , 2001, Annals of human biology.

[17]  Atsushi Maki,et al.  Non-invasive assessment of language dominance with near-infrared spectroscopic mapping , 1998, Neuroscience Letters.

[18]  D. Boas,et al.  Non-invasive neuroimaging using near-infrared light , 2002, Biological Psychiatry.

[19]  Tetsuro Ogaki,et al.  The effect of maximal finger tapping on cerebral activation. , 2004, Journal of physiological anthropology and applied human science.

[20]  K. Tie,et al.  Genetic variation and inferences about perceived taste intensity in mice and men , 2000, Physiology & Behavior.

[21]  Masako Okamoto,et al.  Prefrontal activity during taste encoding: An fNIRS study , 2006, NeuroImage.

[22]  Beverly J. Tepper,et al.  Development of brief methods to classify individuals by PROP taster status , 2001, Physiology & Behavior.

[23]  Nicholas J Timpson,et al.  Refining associations between TAS2R38 diplotypes and the 6-n-propylthiouracil (PROP) taste test: findings from the Avon Longitudinal Study of Parents and Children , 2007, BMC Genetics.

[24]  P. Breslin,et al.  Variability in a taste-receptor gene determines whether we taste toxins in food , 2006, Current Biology.

[25]  S. Kinomura,et al.  Functional anatomy of taste perception in the human brain studied with positron emission tomography , 1994, Brain Research.

[26]  A. L. Fox The Relationship between Chemical Constitution and Taste. , 1932, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Michael J Bamshad,et al.  Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. , 2004, American journal of human genetics.

[28]  Sungho Tak,et al.  Wavelet minimum description length detrending for near-infrared spectroscopy. , 2009, Journal of biomedical optics.

[29]  T. R. Scott,et al.  Electrophysiological Responses to Bitter Stimuli in Primate Cortex a , 1998, Annals of the New York Academy of Sciences.

[30]  Alan C. Evans,et al.  Flavor processing: more than the sum of its parts , 1997, Neuroreport.

[31]  Archana K. Singh,et al.  Exploring the false discovery rate in multichannel NIRS , 2006, NeuroImage.

[32]  A. Drewnowski,et al.  Bitter taste, phytonutrients, and the consumer: a review. , 2000, The American journal of clinical nutrition.

[33]  Hellmuth Obrig,et al.  Linear Aspects of Changes in Deoxygenated Hemoglobin Concentration and Cytochrome Oxidase Oxidation during Brain Activation , 2001, NeuroImage.

[34]  F. Jöbsis Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. , 1977, Science.

[35]  D. Yves von Cramon,et al.  Prefrontal activation due to Stroop interference increases during development—an event-related fNIRS study , 2004, NeuroImage.

[36]  Morten L Kringelbach,et al.  Taste-related activity in the human dorsolateral prefrontal cortex , 2004, NeuroImage.

[37]  Sungho Tak,et al.  NIRS-SPM: Statistical parametric mapping for near-infrared spectroscopy , 2009, NeuroImage.

[38]  J. Slack,et al.  The Molecular Basis of Individual Differences in Phenylthiocarbamide and Propylthiouracil Bitterness Perception , 2005, Current Biology.

[39]  Tatsu Kobayakawa,et al.  Gustatory evoked cortical activity in humans studied by simultaneous EEG and MEG recording. , 2002, Chemical senses.

[40]  P. W. Mccormick,et al.  Intracerebral penetration of infrared light. Technical note. , 1992, Journal of neurosurgery.

[41]  M. Behrens,et al.  The molecular receptive ranges of human TAS2R bitter taste receptors. , 2010, Chemical senses.

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

[43]  E. Watanabe,et al.  Spatial and temporal analysis of human motor activity using noninvasive NIR topography. , 1995, Medical physics.

[44]  E. Rolls,et al.  Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. , 2003, Cerebral cortex.

[45]  E. Rolls,et al.  Taste‐olfactory convergence, and the representation of the pleasantness of flavour, in the human brain , 2003, The European journal of neuroscience.

[46]  D. Drayna,et al.  Bitter taste study in a sardinian genetic isolate supports the association of phenylthiocarbamide sensitivity to the TAS2R38 bitter receptor gene. , 2004, Chemical senses.

[47]  G. Kobal Gustatory evoked potentials in man. , 1985, Electroencephalography and clinical neurophysiology.

[48]  J. Fahey,et al.  The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. , 2001, Phytochemistry.

[49]  M. Herrmann,et al.  Prefrontal activation through task requirements of emotional induction measured with NIRS , 2003, Biological Psychology.

[50]  Joel L. Voss,et al.  Experience-dependent neural integration of taste and smell in the human brain. , 2004, Journal of neurophysiology.

[51]  S. Firestein,et al.  Genomics of olfactory receptors. , 2009, Results and problems in cell differentiation.

[52]  P. Gasparini,et al.  Genetic Variation in Taste Sensitivity to 6‐n‐Propylthiouracil and Its Relationship to Taste Perception and Food Selection , 2009, Annals of the New York Academy of Sciences.

[53]  Masako Okamoto,et al.  Virtual spatial registration of stand-alone fNIRS data to MNI space , 2007, NeuroImage.

[54]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[55]  Judith Meek,et al.  Basic principles of optical imaging and application to the study of infant development , 2002 .

[56]  B. Tepper,et al.  A paper screening test to assess genetic taste sensitivity to 6-n-propylthiouracil , 2003, Physiology & Behavior.

[57]  Masako Okamoto,et al.  Prefrontal activity during flavor difference test: Application of functional near-infrared spectroscopy to sensory evaluation studies , 2006, Appetite.

[58]  L. Clowney,et al.  Activation in ventro-lateral prefrontal cortex during the act of tasting: An fNIRS study , 2009, Neuroscience Letters.

[59]  Francis McGlone,et al.  Lingual tactile acuity, taste perception, and the density and diameter of fungiform papillae in female subjects , 2003, Physiology & Behavior.

[60]  K. Kidd,et al.  Bitter receptor gene (TAS2R38), 6-n-propylthiouracil (PROP) bitterness and alcohol intake. , 2004, Alcoholism, clinical and experimental research.

[61]  B Cowart,et al.  Evaluating the 'Labeled Magnitude Scale' for measuring sensations of taste and smell. , 1996, Chemical senses.

[62]  John Merriam Kingsbury,et al.  Poisonous plants of the United States and Canada , 1964 .