Relation of regional gray and white matter volumes to current BMI and future increases in BMI: a prospective MRI study

Objective:This study tested whether global and regional brain volumes correlated with body mass index (BMI) and increases in BMI over 1-year follow-up.Methods:A total of 83 young females (M age=18.4, s.d.=2.8; BMI range=17.3–38.9) were scanned using magnetic resonance imaging. Voxel-based morphometry was used to assess global brain volume and regional gray matter (GM) and white matter (WM) volumes in regions implicated in taste, reward and inhibitory control.Results:Obese participants had less total GM volume than lean and overweight participants. Obese participants had lower total WM volume than overweight participants. BMI correlated with higher WM volumes in the middle temporal gyrus, fusiform gyrus, parahippocampal gyrus, Rolandic operculum and dorsal striatum. Trend-level reduced GM volumes in the superior frontal gyrus and middle frontal gyrus were related to increases in BMI over 1-year follow-up.Conclusion:Findings suggest that BMI is related to global and regional differences in brain matter volume in female adolescents. Most importantly, findings suggest that low GM volume in regions implicated in inhibitory control are related to future weight gain. Results taken in conjunction with prior findings suggest that abnormalities in regional GM volumes, but not WM volumes, increase the risk for future weight gain and abnormalities in regional WM volumes, but not GM volumes, are secondary to weight gain.

[1]  John P Hatch,et al.  A voxel‐based morphometry study of frontal gray matter correlates of impulsivity , 2009, Human brain mapping.

[2]  K. Flegal,et al.  Prevalence of high body mass index in US children and adolescents, 2007-2008. , 2010, JAMA.

[3]  L. Epstein,et al.  Youth at Risk for Obesity Show Greater Activation of Striatal and Somatosensory Regions to Food , 2011, The Journal of Neuroscience.

[4]  Sterling C. Johnson,et al.  The effect of body mass index on global brain volume in middle-aged adults: a cross sectional study , 2005, BMC neurology.

[5]  L. Diergaarde,et al.  Trait impulsivity predicts escalation of sucrose seeking and hypersensitivity to sucrose-associated stimuli. , 2009, Behavioral neuroscience.

[6]  Kewei Chen,et al.  Brain abnormalities in human obesity: A voxel-based morphometric study , 2006, NeuroImage.

[7]  G. Rebel,et al.  Brain myelin of genetically obese mice , 1985, Journal of the Neurological Sciences.

[8]  Max A. Viergever,et al.  The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues , 2011, NeuroImage.

[9]  A. Gratton,et al.  Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food , 1994, Brain Research.

[10]  J. Parkinson,et al.  Neural contributions to the motivational control of appetite in humans , 2004, The European journal of neuroscience.

[11]  Jean Logan,et al.  Brain dopamine and obesity , 2001, The Lancet.

[12]  小谷 一晃 Sexual dimorphism of age-related changes in whole-body fat distribution in the obese , 1994 .

[13]  Alain Dagher,et al.  Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers , 2003, NeuroImage.

[14]  Karl J. Friston,et al.  Voxel-based morphometry of the human brain: Methods and applications , 2005 .

[15]  J. Tiihonen,et al.  Dopamine D2 receptors and transporters in type 1 and 2 alcoholics , 2002, European Psychiatry.

[16]  H. Schiöth,et al.  Dopamine D1 receptor gene expression decreases in the nucleus accumbens upon long-term exposure to palatable food and differs depending on diet-induced obesity phenotype in rats , 2010, Neuroscience.

[17]  Eric Stice,et al.  Reward circuitry responsivity to food predicts future increases in body mass: Moderating effects of DRD2 and DRD4 , 2010, NeuroImage.

[18]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[19]  D R Jacobs,et al.  Comparison of body fatness measurements by BMI and skinfolds vs dual energy X-ray absorptiometry and their relation to cardiovascular risk factors in adolescents , 2005, International Journal of Obesity.

[20]  Wenzhen Duan,et al.  Neuroprotective and neurorestorative signal transduction mechanisms in brain aging: modification by genes, diet and behavior , 2002, Neurobiology of Aging.

[21]  Kewei Chen,et al.  Relationships between plasma leptin concentrations and human brain structure: A voxel-based morphometric study , 2007, Neuroscience Letters.

[22]  A. Malhotra,et al.  Effects of Diabetes and Obesity on Vascular Reactivity, Inflammatory Cytokines, and Growth Factors , 2011, Obesity.

[23]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[24]  Joachim Spranger,et al.  Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. , 2003, Diabetes.

[25]  Xiaoyan Leng,et al.  Lifelong caloric restriction and interleukin-6 secretion from adipose tissue: effects on physical performance decline in aged rats. , 2007, The journals of gerontology. Series A, Biological sciences and medical sciences.

[26]  Kewei Chen,et al.  Sex differences in the human brain's response to hunger and satiation. , 2002, The American journal of clinical nutrition.

[27]  A. Convit,et al.  Disinhibited Eating in Obese Adolescents Is Associated With Orbitofrontal Volume Reductions and Executive Dysfunction , 2011, Obesity.

[28]  Karl J. Friston,et al.  Why Voxel-Based Morphometry Should Be Used , 2001, NeuroImage.

[29]  Y Schutz,et al.  Assessment of free-living physical activity in humans: an overview of currently available and proposed new measures. , 2001, Obesity research.

[30]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[31]  J. Michael Schurr,et al.  Relation Between Obesity and Blunted Striatal Response to Food Is Moderated by Taq IA A 1 Allele , 2022 .

[32]  K. Blum,et al.  Weight Gain Is Associated with Reduced Striatal Response to Palatable Food , 2010, The Journal of Neuroscience.

[33]  F. Fazio,et al.  Role of Integrated 18-F FDG PET/CT in Recurrent Ovarian Cancer , 2005 .

[34]  Michael Karin,et al.  A central role for JNK in obesity and insulin resistance , 2002, Nature.

[35]  B. Wandell Computational neuroimaging of human visual cortex. , 1999, Annual review of neuroscience.

[36]  A F Roche,et al.  CDC growth charts: United States. , 2000, Advance data.

[37]  K. Flegal,et al.  Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. , 2004, JAMA.

[38]  Hans-Christian Bauknecht,et al.  Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals , 2007, NeuroImage.

[39]  C. Summerbell,et al.  Obesity in middle age and future risk of dementia , 2005 .

[40]  C. Nederkoorn,et al.  Why obese children cannot resist food: the role of impulsivity. , 2006, Eating behaviors.

[41]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[42]  Dan Mungas,et al.  Central obesity and the aging brain. , 2005, Archives of neurology.

[43]  Donald B. Twieg,et al.  Widespread reward-system activation in obese women in response to pictures of high-calorie foods , 2008, NeuroImage.

[44]  R. Wing,et al.  Differential functional magnetic resonance imaging response to food pictures in successful weight-loss maintainers relative to normal-weight and obese controls. , 2009, The American journal of clinical nutrition.

[45]  D. Small,et al.  Relation of reward from food intake and anticipated food intake to obesity: a functional magnetic resonance imaging study. , 2008, Journal of abnormal psychology.

[46]  T. Cole,et al.  Body fat reference curves for children , 2006, International Journal of Obesity.

[47]  Riitta Parkkola,et al.  Brain white matter expansion in human obesity and the recovering effect of dieting. , 2007, The Journal of clinical endocrinology and metabolism.

[48]  Nader Rifai,et al.  Inflammatory markers and risk of developing type 2 diabetes in women. , 2004, Diabetes.

[49]  C. DeCarli,et al.  Inflammatory biomarkers are associated with total brain volume , 2007, Neurology.

[50]  Lee Ryan,et al.  Structural brain differences and cognitive functioning related to body mass index in older females , 2009, Human brain mapping.

[51]  P. Tataranni,et al.  Functional neuroimaging: a new generation of human brain studies in obesity research , 2003, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[52]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[53]  Nora D Volkow,et al.  The role of dopamine in motivation for food in humans: implications for obesity , 2002, Expert opinion on therapeutic targets.

[54]  John Kornak,et al.  Body mass index and magnetic resonance markers of brain integrity in adults , 2008, Annals of neurology.

[55]  M. Gail,et al.  Efficacy and Tolerability of Long-Acting Injectable Naltrexone for Alcohol Dependence: A Randomized Controlled Trial , 2005, Gynecologic oncology.

[56]  J. Flier,et al.  A Transgenic Model of Visceral Obesity and the Metabolic Syndrome , 2001, Science.

[57]  S. Haber,et al.  Restricted daily consumption of a highly palatable food (chocolate Ensure®) alters striatal enkephalin gene expression , 2003, The European journal of neuroscience.

[58]  J. Gray,et al.  Personality and reinforcement: An exploration using a maze-learning task , 1995 .

[59]  J. Wu,et al.  D2 dopamine receptor polymorphism and brain regional glucose metabolism. , 1997, American journal of medical genetics.

[60]  T. Robinson,et al.  Use of the body mass index (BMI) as a measure of overweight in children and adolescents. , 1998, The Journal of pediatrics.

[61]  A. Villringer,et al.  Obesity-Related Differences between Women and Men in Brain Structure and Goal-Directed Behavior , 2011, Front. Hum. Neurosci..

[62]  Angelo Pietrobelli,et al.  Validity of body mass index compared with other body-composition screening indexes for the assessment of body fatness in children and adolescents. , 2002, The American journal of clinical nutrition.

[63]  A. Pocai,et al.  Restoration of hypothalamic lipid sensing normalizes energy and glucose homeostasis in overfed rats. , 2006, The Journal of clinical investigation.

[64]  Sterling C. Johnson,et al.  Age-related changes in neural volume and microstructure associated with interleukin-6 are ameliorated by a calorie-restricted diet in old rhesus monkeys , 2010, NeuroImage.

[65]  Noriaki Hattori,et al.  Functional Imaging of Gustatory Perception and Imagery: Btop-downq Processing of Gustatory Signals , 2004 .

[66]  Richard N Bergman,et al.  Why Visceral Fat is Bad: Mechanisms of the Metabolic Syndrome , 2006, Obesity.

[67]  Jason R. Tregellas,et al.  Sex-based differences in the behavioral and neuronal responses to food , 2010, Physiology & Behavior.

[68]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[69]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[70]  P. Kenny,et al.  Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats , 2010, Nature Neuroscience.

[71]  E. Stice,et al.  Attentional Bias to Food Images Associated With Elevated Weight and Future Weight Gain: An fMRI Study , 2011, Obesity.

[72]  Eric Stice,et al.  Body mass correlates inversely with inhibitory control in response to food among adolescent girls: An fMRI study , 2010, NeuroImage.

[73]  Hiroshi Fukuda,et al.  Relationship Between Body Mass Index and Gray Matter Volume in 1,428 Healthy Individuals , 2008, Obesity.

[74]  Ahmad R. Hariri,et al.  Interleukin-6 Covaries Inversely with Hippocampal Grey Matter Volume in Middle-Aged Adults , 2008, Biological Psychiatry.

[75]  A. Prentice,et al.  Beyond body mass index , 2001, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[76]  Seul-Ki Jeong,et al.  Interactive Effect of Obesity Indexes on Cognition , 2005, Dementia and Geriatric Cognitive Disorders.

[77]  AW Toga,et al.  Brain Structure and Obesity , 2009, NeuroImage.

[78]  N. Volkow,et al.  Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[79]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.