Abstract
Objective:
There is evidence of altered neural taste response in female adolescents who are obese (OB), and in adolescents who are at risk for obesity. To further understand risk factors for the development of overeating and obesity, we investigated response to tastes of sucrose and water in 23 OB and healthy weight (HW) children.
Methods and design:
Thirteen HW and 10 OB 8–12-year-old children underwent functional magnetic resonance imaging while tasting sucrose and water. Additionally, children completed an eating in the absence of hunger paradigm and a sucrose-liking task.
Results:
A region of interest analysis revealed an elevated BOLD response to taste (sucrose and water) within the bilateral insula and amygdala in OB children relative to HW children. Whole-brain analyses revealed a group by condition interaction within the paracingulate, medial frontal, middle frontal gyri and right amygdala: post hoc analyses suggested an increased response to sucrose for OB relative to HW children, whereas HW children responded more strongly to water relative to sucrose. In addition, OB children, relative to HW, tended to recruit the right putamen as well as medial and lateral frontal and temporal regions bilaterally.
Conclusion:
This study showed increased reactivity in the amygdala and insula in the OB compared with HW children, but no functional differentiation in the striatum, despite differences in the striatum previously seen in older samples. These findings support the concept of the association between increased neural processing of food reward in the development of obesity, and raise the possibility that emotional and interoceptive sensitivity could be an early vulnerability in obesity.
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References
Ogden CL, Carroll MD, Kit BK, Flegal KM . Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014; 311: 806–814.
Biro F, Wien M . Childhood obesity and adult morbidities. Am J Clin Nut 2010; 91: 1499S–1505S.
Franks P, Hanson R, Knowler W, Sievers M, Bennett H, Looker H . Childhood obesity, other cardiovascular risk factors, and premature death. New England J of Med 2010; 362: 485–493.
Lobstein T, Bauer L, Uauy R . Obesity in children and young people: a crisis in public health. Obes Rev 2004; 5: 4–104.
Reilly J, Kelly J . Long-term impact of overweight and obesity in childhood and adolescence on morbidity and premature mortality in adulthood: Systematic review. Int J Obes 2011; 35: 891–898.
Herman K, Craig C, Gauvin L, Katzmarzyk P . Tracking of obesity and physical activity from childhood to adulthood: The Physical Activity Longitudinal Study. Int J Obes 2009; 4: 281–288.
Nielsen S, Siega-Riz A, Popkin B . Trends in energy intake in U.S. between 1977 and 1996: similar shifts seen across age groups. Obes Res 2002; 10: 370–378.
Tataranni P, DelParigi A . Functional neuroimaging: a new generation of human brain studies in obesity research. Obes Rev 2003; 4: 229–238.
Berthoud H . Homeostatic and non-homeostatic pathways involved in the control of food intake and energy balance. Obesity 2006; 14: 197S–200S.
Volkow N, Wang G, Baler R . Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 2011; 15: 37–46.
Wang G, Volkow N, Logan J, Pappas N, Wong C, Zhu W et al. Brain dopamine and obesity. Lancet 2001; 357: 354–357.
Dawe S, Loxton N . The role of impulsivity in the development of substance use and eating disorders. Neurosci Biobehav Rev 2004; 28: 343–351.
Burger KS, Stice E . Variability in reward responsivity and obesity: evidence from brain imaging studies. Curr Drug Abuse Rev 2011; 4: 182–189.
Smith DG, Robbins TW . The neurobiological underpinnings of obesity and binge eating: a rationale for adopting the food addiction model. Biol Psychiatry 2013; 73: 804–810.
Volkow N, Wang G, Tomasi D, Baler R . Obesity and addiction: neurobiological overlaps. Obes Rev 2012; 14: 2–18.
Wise R . Roles for nigrostriatal—not just mesocorticolimbic—dopamine in reward and addiction. Trends Neurosci 2009; 32: 517–524.
Critchley HD, Mathias CJ, Dolan RJ . Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 2001; 29: 537–545.
Volz KG, Schubotz RI, von Cramon DY . Predicting events of varying probability: uncertainty investigated by fMRI. Neuroimage 2003; 19: 271–280.
Devinsky O, Morrell MJ, Vogt BA . Contributions of anterior cingulate cortex to behaviour. Brain 1995; 118: 279–306.
Haber SN, Kim K, Mailly P, Calzavara R . Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 2006; 26: 8368–8376.
Kaye W, Fudge J, Paulus M . New insight into symptoms and neurocircuit function of anorexia nervosa. Nat Rev Neurosci 2009; 10: 573–584.
Rolls ET . Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol Behav 2005; 85: 45–56.
Davids S, Lauffer H, Thoms K, Jagdhuhn M, Hirschfeld H, Domin M et al. Increased dorsolateral prefrontal cortex activation in obese children during observation of food stimuli. Int J Obes 2010; 34: 94–104.
Bruce A, Holsen L, Chambers R, Martin L, Brooks W, Zarcone J et al. Obese children show hyperactivation to food pictures in brain networks linked to motivation, reward and cognitive control. Int J Obes 2010; 34: 1494–1500.
Stice E, Spoor S, Bohon C, Veldhuizen MG, Small DM . Relation of reward from food intake and anticipated food intake to obesity: a functional magnetic resonance imaging study. J Abnorm Psychol 2008; 117: 924–935.
Stice E, Yokum S, Burger KS, Epstein LH, Small DM . Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. J Neurosci 2011; 31: 4360–4366.
Galvan A . Adolescent development of the reward system. Front Hum Neurosci 2010; 4: 6.
Steinberg L, Graham S, O'Brien L, Woolard J, Cauffman E, Banich M . Age differences in future orientation and delay discounting. Child Dev 2009; 80: 28–44.
Chambers R, Potenza M . Neurodevelopment, impulsivity, and adolescent gambling. Journal of gambling studies. J Gambl Stud 2003; 19: 53–84.
Post G, Kemper H . Nutrient intake and biological maturation during adolescence. The Amsterdam growth and health longitudinal study. Europ J of Clin Nutr 1993; 47: 400–408.
Watkins B, Frampton I, Lask B, Bryant-Waugh R . Reliability and validity of the child version of the eating disorder examination: A preliminary investigation. Int J of Eat Dis 2005; 38: 183–187.
Sheehan D, Sheehan K, Shytle R, Janavs J, Bannon Y, Rogers J et al. Reliability and validity of the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID). J Clin Psychiatry 2010; 71: 313–326.
Kuczmarski R, Ogden C, Grummer-Strawn L, Flegal K, Guo S, Wei R et al. CDC growth charts: United States. Adv Data 2000; 324: 1–27.
Fisher JO, Birch LL . Eating in the absence of hunger and overweight in girls from 5 to 7 y of age. Am J of Clin Nutr 2002; 76: 226–231.
Boutelle KN, Zucker NL, Peterson CB, Rydell SA, Cafri G, Harnack L . Two novel treatments to reduce overeating in overweight children: A randomized controlled trial. J Consult Clin Psychol 2011; 79: 759–771.
Nolan-Poupart S, Veldhuizen M, Geha P, Small D . Midbrain response to milkshake correlates with ad libitum milkshake intake in the absence of hunger. Appetite 2013; 60: 168–174.
Mennella J, Lukasewycz L, Griffith J, Beauchamp G . Evaluation of the Monell forced-choice, paired-comparison tracking procedure for determining sweet taste preferences across the lifespan. Chem Senses 2011; 36: 345–355.
Wagner A, Aizenstein H, Frank GK, Figurski J, May JC, Putnam K et al. Altered insula response to a taste stimulus in individuals recovered from restricting-type anorexia nervosa. Neuropsychopharmacology 2008; 33: 513–523.
Frank G, Kaye W, Carter C, Brooks S, May C, Fissel K et al. The evaluation of brain activity in response to taste stimuli—a pilot study and method for central taste activation as assessed by event related fMRI. J Neurosci Methods 2003; 131: 99–105.
Kwong K, Belliveau J, Chesler D, Goldberg I, Weisskoff R, Poncelet B et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 1992; 89: 5675–5679.
Ogawa S, Tank D, Menon R, Ellermann J, Kim S, Merkle H et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 1992; 89: 5951–5955.
Rolls E . Brain mechanisms underlying flavour and appetite. Philos Trans R Soc Lond B Biol Sci 2006; 361: 1123–1136.
Small D . Individual differences in the neurophysiology of reward and the obesity epidemic. Int J Obes 2009; 33: S44–S48.
Desikan R, Segonne F, Fischl B, Quinn B, Dickerson B, Blacker D et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006; 31: 968–980.
Cox RW . AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996; 29: 162–173.
Saad Z, Glen D, Chen G, Beauchamp M, Desai R, Cox R . A new method for improving functional-to-structural MRI alignment using local Pearson correlation. Neuroimage 2009; 44: 839–848.
Zhang Y, Brady M, Smith S . Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 2001; 20: 45–57.
Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Development Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-109. 2013.
Benjamini Y, Hochberg Y . Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statist Soc B-Methodological 1995; 57: 289–300.
Stice E, Spoor S, Bohon C, Small DM . Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008; 322: 449–452.
Zald D, Pardo J . Cortical activation induced by intraoral stimulation with water in humans. Chem Senses 2000; 25: 267–275.
Haycock J, Becker L, Ang L, Furukawa Y, Hornykiewicz O, Kish S . Marked disparity between age-related changes in dopamine and other presynaptic dopaminergic markers in human striatum. J Neurochem 2003; 87: 574–585.
Seeman P, Bzowej N, Guan H, Bergeron C, Becker L, Reynolds G et al. Human brain dopamine receptors in children and aging adults. Synapse 1987; 1: 399–404.
Giedd J, Rapoport J . Structural MRI of pediatric brain development: what have we learned and where are we going? Neuron 2010; 67: 728–734.
Muzik O, Chugani D, Juhasz C, shen C, Chugani H . Statistical parametric mapping: assessment of application in children. NeuroImage 2000; 12: 538–549.
Burgund E, Kang H, Kelly J, Buckner R, Snyder A, Petersen S et al. Feasibility of a common stereotactic space for children and adults in fMRI studies of development. NeuroImage 2002; 17: 184–200.
Acknowledgements
Supported by grants to KB (R01DK094475; R01 DK075861; K02HL112042; Department of Pediatrics, UCSD) and WK (MH046001, MH042984, MH066122; MH001894; MH092793), the Price Foundation and the Davis/Wismer Foundation.
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Boutelle, K., Wierenga, C., Bischoff-Grethe, A. et al. Increased brain response to appetitive tastes in the insula and amygdala in obese compared with healthy weight children when sated. Int J Obes 39, 620–628 (2015). https://doi.org/10.1038/ijo.2014.206
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DOI: https://doi.org/10.1038/ijo.2014.206
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