Most functional magnetic resonance imaging (fMRI) studies of taste deliver small quantities of liquids over roughly 45 min to repeatedly sample brain response to tastants. Within this time participants frequently report that their need to urinate increases.
Since both gustatory and interoceptive information are represented in the anterior insular cortex, we evaluated whether perceived need to urinate influenced insular responses to the receipt of a small bolus of milkshake in two datasets (n = 45).
Change in pre- to post-scan ratings of desire to urinate was inversely related to anterior insular response to milkshake.
This finding demonstrates that micturition drive influences insular response to milkshake and supports previous reports of overlapping gustatory and visceral representation within human anterior insular cortex.
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Avery JA, Kerr KL, Ingeholm JE, Burrows K, Bodurka J, Simmons WK (2015) A common gustatory and interoceptive representation in the human mid-insula. Hum Brain Mapp 36:2996–3006. doi:10.1002/hbm.22823
Babbs RK, Sun X, Felsted J, Chouinard-Decorte F, Veldhuizen MG, Small DM (2013) Decreased caudate response to milkshake is associated with higher body mass index and greater impulsivity. Physiol Behav 121:103–111. doi:10.1016/j.physbeh.2013.03.025
Bartoshuk LM, Duffy VB, Green BG, Hoffman HJ, Ko CW, Lucchina LA, Marks LE, Snyder DJ, Weiffenbach JM (2004) Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching. Physiol Behav 82:109–114. doi:10.1016/j.physbeh.2004.02.033
Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666. doi:10.1038/nrn894
Craig AD (2009) How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70. doi:10.1038/nrn2555
Craig AD, Chen K, Bandy D, Reiman EM (2000) Thermosensory activation of insular cortex. Nat Neurosci 3:184–190. doi:10.1038/nrn2555
Critchley HD, Wiens S, Rotshtein P, Öhman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195. doi:10.1038/nn1176
de Araujo IE, Simon SA (2009) The gustatory cortex and multisensory integration. Int J Obes 33:S34–S43. doi:10.1038/ijo.2009.70
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
Drake M, Fowler C, Griffiths D, Mayer E, Paton J, Birder L (2010) Neural control of the lower urinary and gastrointestinal tracts: supraspinal CNS mechanisms. Neurourol Urodyn 29:119–127. doi:10.1002/nau.20841
Green BG, Shaffer GS, Gilmore MM (1993) Derivation and evaluation of a semantic scale of oral sensation magnitude with apparent ratio properties. Chem Senses 18:683–702. doi:10.1093/chemse/21.3.323
Green BG, Dalton P, Cowart B, Shaffer G, Rankin K, Higgins J (1996) Evaluating the ‘labeled magnitude scale’ for measuring sensations of taste and smell. Chem Senses 21:323–334
Griffiths D, Tadic SD (2008) Bladder control, urgency, and urge incontinence: evidence from functional brain imaging. Neurourol Urodyn 27:466–474. doi:10.1002/nau.20549
Griffiths D, Tadic SD, Schaefer W, Resnick NM (2007) Cerebral control of the bladder in normal and urge-incontinent women. NeuroImage 37:1–7. doi:10.1016/j.neuroimage.2007.04.061
Haase L, Green E, Murphy C (2011) Males and females show differential brain activation to taste when hungry and sated in gustatory and reward areas. Appetite 57:421–434. doi:10.1016/j.appet.2011.06.009
Hanamori T, Kunitake T, Kato K, Kannan H (1998) Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats. J Neurophysiol 79:2535–2545
Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324:646–648. doi:10.1126/science.1168450
Kong J, White NS, Kwong KK, Vangel MG, Rosman IS, Gracely RH, Gollub RL (2006) Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity. Hum Brain Mapp 27:715–721. doi:10.1002/hbm.20213
Kuhtz-Buschbeck J, Gilster R, Van der Horst C, Hamann M, Wolff S, Jansen O (2009) Control of bladder sensations: an fMRI study of brain activity and effective connectivity. NeuroImage 47:18–27. doi:10.1016/j.neuroimage.2009.04.020
Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534. doi:10.1007/s00429-010-0255-z
Lim J, Wood A, Green BG (2009) Derivation and evaluation of a labeled hedonic scale. Chem Senses 34:739–751. doi:10.1093/chemse/bjp054
Macey PM, Macey KE, Kumar R, Harper RM (2004) A method for removal of global effects from fMRI time series. NeuroImage 22:360–366. doi:10.1016/j.neuroimage.2003.12.042
Nolan-Poupart S, Veldhuizen MG, Geha P, Small DM (2013) Midbrain response to milkshake correlates with ad libitum milkshake intake in the absence of hunger. Appetite 60:168–174. doi:10.1016/j.appet.2012.09.032
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
Olausson H, Lamarre Y, Backlund H, Morin C, Wallin B, Starck G, Ekholm S, Strigo I, Worsley K, Vallbo Å (2002) Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5:900–904. doi:10.1038/nn896
Olausson H, Charron J, Marchand S, Villemure C, Strigo I, Bushnell M (2005) Feelings of warmth correlate with neural activity in right anterior insular cortex. Neurosci Lett 389:1–5. doi:10.1016/j.neulet.2005.06.065
Small DM (2010) Taste representation in the human insula. Brain Struct Funct 214:551–561. doi:10.1007/s00429-010-0266-9
Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M (2001) Changes in brain activity related to eating chocolate. Brain 124:1720–1733. doi:10.1093/brain/124.9.1720
Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T (2003) Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39:701–711. doi:10.1016/S0896-6273(03)00467-7
Smeets PA, de Graaf C, Stafleu A, van Osch MJ, Nievelstein RA, van der Grond J (2006) Effect of satiety on brain activation during chocolate tasting in men and women. Am J Clin Nutr 83:1297–1305
Stice E, Spoor S, Bohon C, Small D (2008) Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322:449–452. doi:10.1126/science.1161550
Sun X, Veldhuizen MG, Wray AE, de Araujo IE, Sherwin RS, Sinha R, Small DM (2014) The neural signature of satiation is associated with ghrelin response and triglyceride metabolism. Physiol Behav 136:63–73. doi:10.1016/j.physbeh.2014.04.017
Terasawa Y, Shibata M, Moriguchi Y, Umeda S (2012) Anterior insular cortex mediates bodily sensibility and social anxiety. Soc Cogn Affect Neurosci 8:259–266. doi:10.1093/scan/nss108
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, Albrecht J, Zelano C, Boesveldt S, Breslin P, Lundström JN (2011) Identification of human gustatory cortex by activation likelihood estimation. Hum Brain Mapp 32:2256–2266. doi:10.1002/hbm.21188
Zaki J, Davis JI, Ochsner KN (2012) Overlapping activity in anterior insula during interoception and emotional experience. NeuroImage 62:493–499. doi:10.1016/j.neuroimage.2012.05.012
This work was funded by funding from the National Institutes of Health grant R01 DK085579.
This study was funded by the National Institutes of Health grant to Dana Small (#R01 DK085579).
Conflict of Interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study. Informed consent to participate in our study was approved by Yale University School of Medicine Human Investigation Committee.
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Gao, X., Sun, X., Veldhuizen, M.G. et al. Micturition Drive is Associated with Decreased Brain Response to Palatable Milkshake in the Human Anterior Insular Cortex. Chem. Percept. 9, 174–181 (2016). https://doi.org/10.1007/s12078-016-9215-1