Functional MRI detection of activation in the primary gustatory cortices in humans.

Magnetoencephalography (MEG) has recently revealed that the transitions between the parietal operculum (Pop) and the insula (area G) and the ventral end of the central sulcus (cs) were activated with the shortest latency by instrumental gustatory stimulation, which suggests that the location of the primary gustatory area is in these two regions. However, studies using other noninvasive brain-imaging methods such as positron-emission tomography or functional magnetic resonance imaging (fMRI) with manual application of tastants into the mouth have been unable to confirm this. The present study examined cortical activation by repetitive stimulation of the tongue tip with 1 M NaCl with a computer-controlled stimulator and used fMRI to detect it. In individual brains, activations were detected with multiple comparisons (false discovery rate) across the whole brain corrected (threshold at P < 0.05) at both area G and frontal operculum (Fop) in 8 of 11 subjects and at the rolandic operculum (Rop) in 7 subjects. Activations were also found at the ventral end of the cs (n = 3). Group analysis with random-effect models (multiple comparison using familywise error in regions of interest, P < 0.02) revealed activation at area G in both hemispheres and in the Fop, Rop, and ventral end of the cs on the left side. The present study revealed no activation on the gyrus of the external cerebral surface except for the Rop. Taking MEG findings into consideration, the present findings strongly indicate that the primary gustatory area is present at both the transition between the Pop and insula and the Rop including the gray matter within a ventral part of the cs.

[1]  Alan C. Evans,et al.  A Role for the Right Anterior Temporal Lobe in Taste Quality Recognition , 1997, The Journal of Neuroscience.

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

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

[4]  F. Sanides The architecture of the cortical taste nerve areas in squirrel monkey (Saimiri sciureus) and their relationships to insular, sensorimotor and prefrontal regions. , 1968, Brain research.

[5]  J. Pardo,et al.  Cortical activation induced by intraoral stimulation with water in humans. , 2000, Chemical senses.

[6]  H. Ogawa,et al.  Neural activities in the fronto-opercular cortex of macaque monkeys during tasting and mastication. , 1994, The Japanese journal of physiology.

[7]  H. Ogawa,et al.  Gustatory coding in the precentral extension of area 3 in Japanese macaque monkeys; comparison with area G , 2005, Experimental Brain Research.

[8]  E. Rolls,et al.  Representation of pleasant and aversive taste in the human brain. , 2001, Journal of neurophysiology.

[9]  J C Gore,et al.  Hemispheric dominance of cortical activity evoked by focal electrogustatory stimuli. , 2001, Chemical senses.

[10]  H. Burton,et al.  Projection of taste nerve afferents to anterior opercular-insular cortex in squirrel monkey (Saimiri sciureus). , 1968, Brain research.

[11]  S. C. Strother,et al.  The Quantitative Evaluation of Functional Neuroimaging Experiments: Mutual Information Learning Curves , 2002, NeuroImage.

[12]  H. Ogawa,et al.  Cytochrome oxidase staining facilitates unequivocal visualization of the primary gustatory area in the fronto-operculo-insular cortex of macaque monkeys , 1991, Neuroscience Letters.

[13]  D Le Bihan,et al.  Latencies in fMRI time‐series: effect of slice acquisition order and perception , 1997, NMR in biomedicine.

[14]  H. Ogawa,et al.  Two distinct projection areas from tongue nerves in the frontal operculum of macaque monkeys as revealed with evoked potential mapping , 1985, Neuroscience Research.

[15]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[16]  R B Hamilton,et al.  Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis , 1986, The Journal of comparative neurology.

[17]  H. Jasper,et al.  Epilepsy and the functional anatomy of the human brain , 1985 .

[18]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[19]  C Tempelmann,et al.  Functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex , 2004, Neuroscience.

[20]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[21]  D Le Bihan,et al.  Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. , 2001, Chemical senses.

[22]  D. Le Bihan,et al.  fMRI Study of Taste Cortical Areas in Humans , 1998, Annals of the New York Academy of Sciences.

[23]  Y. Kawamura,et al.  A role of oral afferents in aversion to taste solutions , 1968 .

[24]  William R. Amberson Epilepsy and the Functional Anatomy of the Human Brain. Wilder Penfield and Herbert Jasper.Little, Brown, Boston, 1954. 896 pp. Illus. + plates.$16.00 , 1954 .

[25]  Jens Frahm,et al.  Functional mapping of color processing by magnetic resonance imaging of responses to selective P- and M-pathway stimulation , 1996, Experimental Brain Research.

[26]  T Kusama,et al.  Connections of the fronto-parietal operculum and the postcentral gyrus with the posterior ventral thalamic nucleus, especially its medial nucleus, in monkeys. , 1985, Journal fur Hirnforschung.

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

[28]  原 節男 Interrelationship among stimulus intensity, stimulated area and reaction time in the human gustatory sensation , 1957 .

[29]  M. Ikeda,et al.  Clinical Use of Electrogustometry: Strengths and Limitations , 2002, Acta oto-laryngologica. Supplementum.

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

[31]  T. R. Scott,et al.  Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. , 1986, Journal of neurophysiology.

[32]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[33]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Preul The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[35]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[36]  J. Desmond,et al.  A method for functional magnetic resonance imaging of olfaction , 1997, Journal of Neuroscience Methods.

[37]  M Petrides,et al.  Re‐examination of the human taste region: a positron emission tomography study , 1999, The European journal of neuroscience.

[38]  W. Penfield,et al.  The insula; further observations on its function. , 1955, Brain : a journal of neurology.

[39]  H. Duvernoy The Human Brain , 1999, Springer Vienna.

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

[41]  T Kobayakawa,et al.  Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. , 1999, Chemical senses.

[42]  R J Zatorre,et al.  Human cortical gustatory areas: a review of functional neuroimaging data. , 1999, Neuroreport.

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

[45]  M. O'Mahony,et al.  Increased Taste Discrimination Ability by Flowing Stimuli over the Tongue , 1994 .

[47]  P. F. Moortele,et al.  Human taste cortical areas studied with functional magnetic resonance imaging: evidence of functional lateralization related to handedness , 1999, Neuroscience Letters.