Abstract
The primary taste cortex is located in the insula. However, exactly where in the insula the human primary taste cortex is located remains a controversial issue. Human neuroimaging studies have shown prominent variation concerning the location of taste-responsive activation within the insula. A standard protocol for gustatory testing in neuroimaging studies has not been developed, which might underlie such variations. In order to localize the primary taste cortex in an fMRI experiment, we used a taste delivery system to suppress non-taste stimuli and psychological effects. Then, we compared brain response to taste solution during a passive tasting task condition and a taste quality identification task condition to verify whether this cognitive task affected the location of taste-responsive activation within the insula. To examine which part of insula is the primary taste area, we performed dynamic causal modeling (DCM) to verify the neural network of the taste coding-related region and random-effects Bayesian model selection (BMS) at the family level to reveal the optimal input region. Passive tasting resulted in activation of the right middle insula (MI), and the most favorable model selected by DCM analysis showed that taste effect directly influenced the MI. Additionally, BMS results at the family level suggested that the taste inputs entered into the MI. Taken together, our results suggest that the human primary taste cortex is located in the MI.
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References
Arnsten AF (2009) Toward a new understanding of attention-deficit hyperactivity disorder pathophysiology: an important role for prefrontal cortex dysfunction. CNS Drugs 23(Suppl 1):33–41. doi:10.2165/00023210-200923000-00005
Beauchamp MS, Haxby JV, Jennings JE, DeYoe EA (1999) An fMRI version of the Farnsworth–Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. Cereb Cortex 9:257–263
Bender G, Veldhuizen MG, Meltzer JA, Gitelman DR, Small DM (2009) Neural correlates of evaluative compared with passive tasting. Eur J Neurosci 30:327–338. doi:10.1111/j.1460-9568.2009.06819.x
Bisley JW (2011) The neural basis of visual attention. J Physiol 589:49–57. doi:10.1113/jphysiol.2010.192666
Buchel C, Friston KJ (1997) Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. Cereb Cortex 7:768–778
Cauda F, D’Agata F, Sacco K, Duca S, Geminiani G, Vercelli A (2011) Functional connectivity of the insula in the resting brain. Neuroimage 55:8–23. doi:10.1016/j.neuroimage.2010.11.049
Cerf-Ducastel B, Van de Moortele PF, MacLeod P, Le Bihan D, Faurion A (2001) Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. Chem Senses 26:371–383
Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324. doi:10.1016/j.neuron.2008.04.017
Craig AD (2008) Interception and emotion: a neuroanatomical perspective. In: Lewis M, Haviland-Jones JM, Barrett LF (eds) Handbook of emotions, 3rd edn. The Guilford Press, New York, pp 272–290
De Araujo IE, Rolls ET (2004) Representation in the human brain of food texture and oral fat. J Neurosci 24:3086–3093. doi:10.1523/JNEUROSCI.0130-04.2004
de Araujo IE, Kringelbach ML, Rolls ET, Hobden P (2003a) Representation of umami taste in the human brain. J Neurophysiol 90:313–319. doi:10.1152/jn.00669.2002
de Araujo IE, Kringelbach ML, Rolls ET, McGlone F (2003b) Human cortical responses to water in the mouth, and the effects of thirst. J Neurophysiol 90:1865–1876. doi:10.1152/jn.00297.2003
de Araujo IE, Geha P, Small DM (2012) Orosensory and homeostatic functions of the insular taste cortex. Chemosens Percept 5:64–79. doi:10.1007/s12078-012-9117-9
Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21:1498–1506. doi:10.1093/cercor/bhq186
Fajardo C, Escobar MI, Buritica E, Arteaga G, Umbarila J, Casanova MF, Pimienta H (2008) Von Economo neurons are present in the dorsolateral (dysgranular) prefrontal cortex of humans. Neurosci Lett 435:215–218. doi:10.1016/j.neulet.2008.02.048
Faurion A, Cerf B, Le Bihan D, Pillias AM (1998) fMRI study of taste cortical areas in humans. Ann NY Acad Sci 855:535–545
Faurion A, Cerf B, Van De Moortele PF, Lobel E, Mac Leod P, Le Bihan D (1999) Human taste cortical areas studied with functional magnetic resonance imaging: evidence of functional lateralization related to handedness. Neurosci Lett 277:189–192
Frank GK, Oberndorfer TA, Simmons AN, Paulus MP, Fudge JL, Yang TT, Kaye WH (2008) Sucrose activates human taste pathways differently from artificial sweetener. Neuroimage 39:1559–1569. doi:10.1016/j.neuroimage.2007.10.061
Friedman DP, Murray EA, O’Neill JB, Mishkin M (1986) Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J Comp Neurol 252:323–347. doi:10.1002/cne.902520304
Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273–1302. doi:10.1016/S1053-8119(03)00202-7
Grabenhorst F, Rolls ET (2008) Selective attention to affective value alters how the brain processes taste stimuli. Eur J Neurosci 27:723–729. doi:10.1111/j.1460-9568.2008.06033.x
Grabenhorst F, Rolls ET, Bilderbeck A (2008) How cognition modulates affective responses to taste and flavor: top-down influences on the orbitofrontal and pregenual cingulate cortices. Cereb Cortex 18:1549–1559. doi:10.1093/cercor/bhm185
Guest S, Grabenhorst F, Essick G, Chen Y, Young M, McGlone F, de Araujo I, Rolls ET (2007) Human cortical representation of oral temperature. Physiol Behav 92:975–984. doi:10.1016/j.physbeh.2007.07.004
Haase L, Cerf-Ducastel B, Buracas G, Murphy C (2007) On-line psychophysical data acquisition and event-related fMRI protocol optimized for the investigation of brain activation in response to gustatory stimuli. J Neurosci Methods 159:98–107. doi:10.1016/j.jneumeth.2006.07.009
Iannilli E, Singh PB, Schuster B, Gerber J, Hummel T (2012) Taste laterality studied by means of umami and salt stimuli: An fMRI study. Neuroimage 60:426–435. doi:10.1016/j.neuroimage.2011.12.088
Kami YN, Goto TK, Tokumori K, Yoshiura T, Kobayashi K, Nakamura Y, Honda H, Ninomiya Y, Yoshiura K (2008) The development of a novel automated taste stimulus delivery system for fMRI studies on the human cortical segregation of taste. J Neurosci Methods 172:48–53. doi:10.1016/j.jneumeth.2008.04.009
Kobayakawa T, Ogawa H, Kaneda H, Ayabe-Kanamura S, Endo H, Saito S (1999) Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. Chem Senses 24:201–209
Kobayakawa T, Saito S, Gotow N (2012) Temporal characteristics of neural activity associated with perception of gustatory stimulus intensity in humans. Chem Percept 5:80–86. doi:10.1007/s12078-012-9123-y
Kobayashi M (2006) Functional organization of the human gustatory cortex. J Oral Biosci 48:244–260. doi:10.2330/joralbiosci.48.244
Kobayashi M, Takeda M, Hattori N, Fukunaga M, Sasabe T, Inoue N, Nagai Y, Sawada T, Sadato N, Watanabe Y (2004) Functional imaging of gustatory perception and imagery: “top-down” processing of gustatory signals. Neuroimage 23:1271–1282. doi:10.1016/j.neuroimage.2004.08.002
Kringelbach ML, de Araujo IE, Rolls ET (2004) Taste-related activity in the human dorsolateral prefrontal cortex. Neuroimage 21:781–788. doi:10.1016/j.neuroimage.2003.09.063
Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239
Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach Atlas. Neuroimage 21:450–455
Martin RE, Goodyear BG, Gati JS, Menon RS (2001) Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol 85:938–950
McCabe C, Rolls ET (2007) Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain. Eur J Neurosci 25:1855–1864. doi:10.1111/j.1460-9568.2007.05445.x
Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J Comp Neurol 212:1–22. doi:10.1002/cne.902120102
Miki A, Liu GT, Modestino EJ, Liu CS, Bonhomme GR, Dobre CM, Haselgrove JC (2001) Functional magnetic resonance imaging of the visual system. Curr Opin Ophthalmol 12:423–431
Nakamura Y, Goto TK, Tokumori K, Yoshiura T, Kobayashi K, Nakamura Y, Honda H, Ninomiya Y, Yoshiura K (2011) Localization of brain activation by umami taste in humans. Brain Res 1406:18–29. doi:10.1016/j.brainres.2011.06.029
Nitschke JB, Dixon GE, Sarinopoulos I, Short SJ, Cohen JD, Smith EE, Kosslyn SM, Rose RM, Davidson RJ (2006) Altering expectancy dampens neural response to aversive taste in primary taste cortex. Nat Neurosci 9:435–442. doi:10.1038/nn1645
O’Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F (2001) Representation of pleasant and aversive taste in the human brain. J Neurophysiol 85:1315–1321
Ogawa H, Wakita M, Hasegawa K, Kobayakawa T, Sakai N, Hirai T, Yamashita Y, Saito S (2005) Functional MRI detection of activation in the primary gustatory cortices in humans. Chem Senses 30:583–592. doi:10.1093/chemse/bji052
Onoda K, Kobayakawa T, Ikeda M, Saito S, Kida A (2005) Laterality of human primary gustatory cortex studied by MEG. Chem Senses 30:657–666. doi:10.1093/chemse/bji059
Onoda K, Ikeda M, Sekine H, Ogawa H (2012) Clinical study of central taste disorders and discussion of the central gustatory pathway. J Neurol 259:261–266. doi:10.1007/s00415-011-6165-z
Penny WD, Stephan KE, Daunizeau J, Rosa MJ, Friston KJ, Schofield TM, Leff AP (2010) Comparing families of dynamic causal models. PLoS Comput Biol 6:e1000709. doi:10.1371/journal.pcbi.1000709
Petrides M, Alivisatos B, Pandya ND, Evans AC (1996) Gustatory cortex: comparative architectonic analysis in the human and the macaque brain and functional data. NeuroImage 3:S344. ISSN 1053-8119. doi:10.1016/S1053-8119(96)80346-6
Pritchard TC (2011) Gustatory system. In: Mai JK, Paxinos G (eds) The human nervous system, 3rd edn. Academic Press, London, pp 1187–1218
Pritchard TC, Macaluso DA, Eslinger PJ (1999) Taste perception in patients with insular cortex lesions. Behav Neurosci 113:663–671
Rolls ET (2007) Sensory processing in the brain related to the control of food intake. Proc Nutr Soc 66:96–112. doi:10.1017/S0029665107005332
Rudenga K, Green B, Nachtigal D, Small DM (2010) Evidence for an integrated oral sensory module in the human anterior ventral insula. Chem Senses 35:693–703. doi:10.1093/chemse/bjq068
Schall JD (2004) On the role of frontal eye field in guiding attention and saccades. Vision Res 44:1453–1467. doi:10.1016/j.visres.2003.10.025
Schoenfeld MA, Neuer G, Tempelmann C, Schussler K, Noesselt T, Hopf JM, Heinze HJ (2004) Functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex. Neuroscience 127:347–353. doi:10.1016/j.neuroscience.2004.05.024
Scott TR, Plata-Salaman CR (1999) Taste in the monkey cortex. Physiol Behav 67:489–511
Small DM (2010) Taste representation in the human insula. Brain Struct Funct 214:551–561. doi:10.1007/s00429-010-0266-9
Small DM, Prescott J (2005) Odor/taste integration and the perception of flavor. Exp Brain Res 166:345–357. doi:10.1007/s00221-005-2376-9
Small DM, Zald DH, Jones-Gotman M, Zatorre RJ, Pardo JV, Frey S, Petrides M (1999) Human cortical gustatory areas: a review of functional neuroimaging data. NeuroReport 10:7–14
Smits M, Peeters RR, van Hecke P, Sunaert S (2007) A 3 T event-related functional magnetic resonance imaging (fMRI) study of primary and secondary gustatory cortex localization using natural tastants. Neuroradiology 49:61–71. doi:10.1007/s00234-006-0160-6
Stephan KE, Penny WD, Daunizeau J, Moran RJ, Friston KJ (2009) Bayesian model selection for group studies. Neuroimage 46:1004–1017. doi:10.1016/j.neuroimage.2009.03.025
Stephani C, Fernandez-Baca Vaca G, Maciunas R, Koubeissi M, Luders HO (2011) Functional neuroanatomy of the insular lobe. Brain Struct Funct 216:137–149. doi:10.1007/s00429-010-0296-3
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289. doi:10.1006/nimg.2001.0978
Veldhuizen MG, Small DM (2011) Modality-specific neural effects of selective attention to taste and odor. Chem Senses. doi:10.1093/chemse/bjr043
Veldhuizen MG, Bender G, Constable RT, Small DM (2007) Trying to detect taste in a tasteless solution: modulation of early gustatory cortex by attention to taste. Chem Senses 32:569–581. doi:10.1093/chemse/bjm025
Veldhuizen MG, Nachtigal D, Teulings L, Gitelman DR, Small DM (2010) The insular taste cortex contributes to odor quality coding. Front Hum Neurosci 4:58. doi:10.3389/fnhum.2010.00058
Veldhuizen MG, Albrecht J, Zelano C, Boesveldt S, Breslin P, Lundstrom JN (2011) Identification of human gustatory cortex by activation likelihood estimation. Hum Brain Mapp 32:2256–2266. doi:10.1002/hbm.21188
Veldhuizen MG, Gitelman D, Small DM (2012) An fMRI study of the interactions between the attention and the gustatory networks. Chem Percept 5:117–127. doi:10.1007/s12078-012-9122-z
Verhagen JV, Engelen L (2006) The neurocognitive bases of human multimodal food perception: sensory integration. Neurosci Biobehav Rev 30:613–650. doi:10.1016/j.neubiorev.2005.11.003
Wagner A, Aizenstein H, Frank GK, Figurski J, May JC, Putnam K, Fischer L, Bailer UF, Henry SE, McConaha C, Vogel V, Kaye WH (2006) Neural correlates of habituation to taste stimuli in healthy women. Psychiatry Res 147:57–67. doi:10.1016/j.pscychresns.2005.11.005
Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds) Functional MRI: an introduction to methods. Oxford University Press, Oxford, pp 251–270
Yaxley S, Rolls ET, Sienkiewicz ZJ (1990) Gustatory responses of single neurons in the insula of the macaque monkey. J Neurophysiol 63:689–700
Zald DH, Pardo JV (2000) Cortical activation induced by intraoral stimulation with water in humans. Chem Senses 25:267–275
Acknowledgments
We thank Prof. Yuzo Ninomiya, Section of Oral Neuroscience, Graduate School of Dental Sciences, Kyushu University.
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Nakamura, Y., Tokumori, K., Tanabe, H.C. et al. Localization of the primary taste cortex by contrasting passive and attentive conditions. Exp Brain Res 227, 185–197 (2013). https://doi.org/10.1007/s00221-013-3499-z
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DOI: https://doi.org/10.1007/s00221-013-3499-z