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  • Original Article
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Excessive body fat linked to blunted somatosensory cortex response to general reward in adolescents

Abstract

Background and aims:

The brain reward system is key to understanding adolescent obesity in the current obesogenic environment, rich in highly appetising stimuli, to which adolescents are particularly sensitive. We aimed to examine the association between body fat levels and brain reward system responsivity to general (monetary) rewards in male and female adolescents.

Methods:

Sixty-eight adolescents (34 females; mean age (s.d.)= 16.56 (1.35)) were measured for body fat levels with bioelectric impedance, and underwent a functional magnetic resonance imaging (fMRI) scan during the Monetary Incentive Delay (MID) task. The MID task reliably elicits brain activations associated with two fundamental aspects of reward processing: anticipation and feedback. We conducted regression analyses to examine the association between body fat and brain reward system responsivity during reward anticipation and feedback, while controlling for sex, age and socioeconomic status. We also analysed the moderating impact of sex on the relationship between fat levels and brain responsivity measures. Brain imaging analyses were corrected for multiple comparisons, with a cluster-defining threshold of P<0.001, and minimum cluster size of 38 contiguous voxels.

Results:

Higher body fat levels were associated with lower activation of the primary somatosensory cortex (S1) and the supramarginal gyrus during reward feedback after controlling for key sociodemographic variables. Although we did not find significant associations between body fat and brain activations during reward anticipation, S1/supramarginal gyrus activation during feedback was linked to increased negative prediction error, that is, less reward than expected, in illustrative post hoc analyses. Sex did not significantly moderate the association between body fat and brain activation in the MID task.

Conclusions:

In adolescents, higher adiposity is linked to hypo-responsivity of somatosensory regions during general (monetary) reward feedback. Findings suggest that adolescents with excess weight have blunted activation in somatosensory regions involved in reward feedback learning.

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References

  1. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384: 766–781.

    PubMed  PubMed Central  Google Scholar 

  2. Vandevijvere S, Chow CC, Hall KD, Umali E, Swinburn BA . Increased food energy supply as a major driver of the obesity epidemic: A global analysis. Bull World Health Organ 2015; 93: 446–456.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML et al. The global obesity pandemic: Shaped by global drivers and local environments. Lancet 2011; 378: 804–814.

    Article  PubMed  Google Scholar 

  4. Stice E, Figlewicz DP, Gosnell BA, Levine AS, Pratt WE . The contribution of brain reward circuits to the obesity epidemic. Neurosci Biobehav Rev 2013; 37: 2047–2058.

    Article  PubMed  Google Scholar 

  5. Stice E, Yokum S . Neural vulnerability factors that increase risk for future weight gain. Psychol Bull 2016; 142: 447–471.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Volkow N, Wang G, Baler B . Reward, dopamine and the control of food intake: Implications for obesity. Trends Cogn Sci 2011; 15: 27–46.

    Article  Google Scholar 

  7. Knutson B, Fong GW, Adams CM, Varner JL, Hommer D . Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 2001; 12: 3683–3687.

    Article  CAS  PubMed  Google Scholar 

  8. Knutson B, Westdorp A, Kaiser E, Hommer D . FMRI visualization of brain activity during a Monetary Incentive Delay Task. Neuroimage 2000; 12: 20–27.

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Müller MJ, Lagerpusch M, Enderle J, Schautz B, Heller M, Bosy-Westphal A . Beyond the body mass index: Tracking body composition in the pathogenesis of obesity and the metabolic syndrome. Obes Rev 2012; 13: 6–13.

    Article  PubMed  Google Scholar 

  12. Goodwin K, Syme C, Abrahamowicz M, Leonard GT, Richer L, Perron M et al. Routine clinical measures of adiposity as predictors of visceral fat in adolescence: A population-based magnetic resonance imaging study. PLoS One 2013; 8: e79896.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Loomba-Albrecht LA, Styne DM . Effect of puberty on body composition. Curr Opin Endocrinol Diabetes Obes 2009; 16: 10–15.

    Article  CAS  PubMed  Google Scholar 

  14. Rapuano KM, Huckins JF, Sargent JD, Heatherton TF, Kelley WM . Individual differences in reward and somatosensory-motor brain regions correlate with adiposity in adolescents. Cereb Cortex 2016; 26: 2602–2611.

    Article  PubMed  Google Scholar 

  15. Kringelbach ML, Stein A, van Hartevelt TJ . The functional human neuroanatomy of food pleasure cycles. Physiol Behav 2012; 106: 307–316.

    Article  CAS  PubMed  Google Scholar 

  16. Wang GJ, Volkow ND, Thanos PK, Fowler JS . Imaging of brain dopamine pathways: Implications for understanding obesity. J Addict Med 2009; 3: 8–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Pleger B, Ruff CC, Blankenburg F, Klöppel S, Driver J, Dolan RJ . Influence of dopaminergically mediated reward on somatosensory decision-making. PLoS Biol 2009; 7: e1000164.

    Article  PubMed  PubMed Central  Google Scholar 

  18. van Duin EDA, Goossens L, Hernaus D, da Silva Alves F, Schmitz N, Schruers K et al. Neural correlates of reward processing in adults with 22q11 deletion syndrome. J Neurodev Disord 2016; 8: 25.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Alarcón G, Cservenka A, Nagel BJ . Adolescent neural response to reward is related to participant sex and task motivation. Brain Cogn 2016; 111: 51–62.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH . Establishing a standard definition for child overweight and obesity worldwide: International survey. BMJ 2000; 320: 7244.

    Article  Google Scholar 

  21. Jebb SA, Cole TJ, Doman D, Murgatroyd PR, Prentice AM . Evaluation of the novel Tanita body-fat analyser to measure body composition by comparison with a four-compartment model. Br J Nutr 2000; 83: 115–122.

    Article  CAS  PubMed  Google Scholar 

  22. Vicente-Rodríguez G, Rey-López JP, Mesana MI, Poortvliet E, Ortega FB, Polito A et al. Reliability and intermethod agreement for body fat assessment among two field and two laboratory methods in adolescents. Obesity 2012; 20: 221–228.

    Article  PubMed  Google Scholar 

  23. Verdejo-Román J, Vilar-López R, Navas JF, Soriano-Mas C, Verdejo-García A . Brain reward system’s alterations in response to food and monetary stimuli in overweight and obese individuals. Hum Brain Mapp 2016; 38: 666–677.

    Article  PubMed  PubMed Central  Google Scholar 

  24. McCarthy HD, Cole TJ, Fry T, Jebb SA, Prentice AM . Body fat reference curves for children. Int J Obes 2006; 30: 598–602.

    Article  CAS  Google Scholar 

  25. Sescousse G, Caldú X, Segura B, Dreher JC . Processing of primary and secondary rewards: A quantitative meta-analysis and review of human functional neuroimaging studies. Neurosci Biobehav Rev 2013; 37: 681–696.

    Article  PubMed  Google Scholar 

  26. Liu X, Hairston J, Schrier M, Fan J . Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 2011; 35: 1219–1236.

    Article  PubMed  Google Scholar 

  27. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH . An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003; 19: 1233–1239.

    Article  PubMed  Google Scholar 

  28. Song X, Dong Z, Long X, Li S, Zuo X . REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 2011; 6: e25031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pleger B, Blankenburg F, Ruff CC, Driver J, Dolan RJ . Reward facilitates tactile judgments and modulates hemodynamic responses in human primary somatosensory cortex. J Neurosci 2008; 28: 8161–8168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Haggard P, de Boer L . Oral somatosensory awareness. Neurosci Biobehav Rev 2014; 47: 469–484.

    Article  PubMed  Google Scholar 

  31. Wang G-J, Volkow ND, Felder C, Fowler JS, Levy AV, Pappas NR et al. Enhanced resting activity of the oral somatosensory cortex in obese subjects. Neuroreport 2002; 13: 1151–1155.

    Article  PubMed  Google Scholar 

  32. Schultz W. Dopamine reward prediction error coding. Dialogues Clin Neurosci 2016; 18: 23–32.

  33. Robinson TE, Berridge KC . The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Rev 1993; 18: 247–291.

    Article  CAS  PubMed  Google Scholar 

  34. Robinson TE, Berridge KC . The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc London Biol Sci 2008; 363: 3137–3146.

    Article  Google Scholar 

  35. Carter A, Hendrikse J, Lee N, Yücel M, Verdejo-Garcia A, Andrews Z et al. The neurobiology of ‘Food Addiction’ and its implications for obesity treatment and policy. Annu Rev Nutr 2016; 36: 105–128.

    Article  CAS  PubMed  Google Scholar 

  36. Volkow ND, Wang GJ, Fowler JS, Telang F . Overlapping neuronal circuits in addiction and obesity: Evidence of systems pathology. Philos Trans R Soc B Biol Sci 2008; 363: 3191–3200.

    Article  Google Scholar 

  37. Shulman EP, Harden KP, Chein JM, Steinberg L . Sex differences in the developmental trajectories of impulse control and sensation-seeking from early adolescence to early adulthood. J Youth Adolesc 2015; 44: 1–17.

    Article  PubMed  Google Scholar 

  38. Cho C, Smith DV, Delgado MR . Reward sensitivity enhances ventrolateral prefrontal cortex activation during free choice. Front Neurosci 2016; 10: 529.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Verdejo-Garcia A, Clark L, Verdejo-Román J, Albein-Urios N, Martinez-Gonzalez JM, Gutierrez B et al. Neural substrates of cognitive flexibility in cocaine and gambling addictions. Br J Psychiatry 2015; 207: 158–164.

    Article  PubMed  Google Scholar 

  40. Poldrack RA, Baker CI, Durnez J, Gorgolewski KJ, Matthews PM, Mufanò MR et al. Scanning the horizon: Towards transparent and reproducible neuroimaging research. Nat Rev Neurosci 2017; 18: 115–126..

  41. Woo CW, Krishnan A, Wager TD . Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations. Neuroimage 2014; 91: 412–419.

    Article  PubMed  Google Scholar 

  42. Schultz W . Dopamine reward prediction error coding. Dialogues Clin Neurosci 2016; 18: 23–32.

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The research described in this paper has been funded by the project grant Neuroecobe (HUM-6635) from the Andalusian Council of Innovation, Science and Industry (Andalusia, Spain) to AVG. JFN is supported by a grant from the Spanish Ministry of Education, Culture and Sport (FPU13/00669). JVR is supported by a postdoctoral fellowship linked to the Neuroecobe project grant.

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Correspondence to A Verdejo-García.

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Navas, J., Barrós-Loscertales, A., Costumero-Ramos, V. et al. Excessive body fat linked to blunted somatosensory cortex response to general reward in adolescents. Int J Obes 42, 88–94 (2018). https://doi.org/10.1038/ijo.2017.207

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