Abstract
Background:
Excessive adipose tissue, particularly with a centralized distribution, propagates hormonal and metabolic disturbance. The detrimental effects of adiposity may extend beyond the periphery and target the central nervous system, increasing vulnerability to cognitive decline. The aim of the current study was to determine how central adiposity impacts the brain at midlife by examining the blood oxygen level-dependent (BOLD) response to a challenging cognitive task.
Methods:
Seventy-three adults, aged 40–60 years, completed a 2-back verbal working memory task during functional magnetic resonance imaging. Central adiposity was assessed with waist circumference. The association between waist circumference and task-related activation in a priori regions of interest was modeled using bootstrapping regression models corrected for multiple-comparisons.
Results:
Larger waist circumference was associated with diminished working-memory-related BOLD response in the right superior frontal gyrus (β=−0.008, P=0.001, 95% CI: −0.012 to −0.004) and left middle frontal gyrus (β=−0.009, P=0.002, 95% CI: −0.015 to −0.003), statistically adjusting for age, sex, systolic blood pressure and total cholesterol. Reduced task-related activation in the right superior frontal gyrus (r=−0.369, P=0.002) and left middle frontal gyrus (r=−0.266, P=0.025) were related to slower reaction time on the task, controlling for age and education.
Conclusions:
Larger waist circumference predicted alterations in the BOLD response that coupled with decrements in task performance. While future studies are necessary, the results suggest that similar to its role in the periphery, central adiposity may be a robust predictor of metabolic and hormonal alterations that impinge upon central nervous system functioning.
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References
World Health Organization. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organization: Geneva, Switzerland, 2000.
Kopelman PG . Obesity as a medical problem. Nature 2000; 404: 635–643.
Gustafson D, Lissner L, Bengtsson C, Bjorkelund C, Skoog I . A 24-year follow-up of body mass index and cerebral atrophy. Neurology 2004; 63: 1876–1881.
Walther K, Birdsill AC, Glisky EL, Ryan L . Structural brain differences and cognitive functioning related to body mass index in older females. Hum Brain Mapp 2009; 31: 1052–1064.
Ward M, Carlsson C, Trivedi M, Sager M, Johnson S . The effect of body mass index on global brain volume in middle-aged adults: a cross sectional study. BMC Neurol 2005; 5: 23.
Whitmer RA, Gustafson DR, Barrett-Connor E, Haan MN, Gunderson EP, Yaffe K . Central obesity and increased risk of dementia more than three decades later. Neurology 2008; 71: 1057–1064.
Gustafson D, Rothenberg E, Blennow K, Steen B, Skoog I . An 18-year follow-up of overweight and risk of Alzheimer disease. Arch Inter Med 2003; 163: 1524–1528.
Gustafson DR . Adiposity hormones and dementia. J Neurol Sci 2010; 299: 30–34.
Cereda E, Sansone V, Meola G, Malavazos AE . Increased visceral adipose tissue rather than BMI as a risk factor for dementia. Age Ageing 2007; 36: 488–491.
Ibrahim MM . Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 2010; 11: 11–18.
Wisse BE . The inflammatory syndrome: the role of adipose tissue cytokines in metabolic disorders linked to obesity. J Am Soc Nephrol 2004; 15: 2792–2800.
Wolf PA, Beiser A, Elias MF, Au R, Vasan RS, Seshadri S . Relation of obesity to cognitive function: importance of central obesity and synergistic influence of concomitant hypertension. The Framingham Heart Study. Curr Alzheimer Res 2007; 4: 111–116.
Gustafson D . A life course of adiposity and dementia. Eur J Pharmacol 2008; 585: 163–175.
Bondi MW, Houston WS, Eyler LT, Brown GG . fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology 2005; 64: 501–508.
Braskie MN, Small GW, Bookheimer SY . Vascular health risks and fMRI activation during a memory task in older adults. Neurobiol Aging 2010; 31: 1532–1542.
Gonzales M, Tarumi T, Miles S, Tanaka H, Shah F, Haley A . Insulin Sensitivity as a mediator of the relationship between body mass index and working memory-related brain activation. Obesity 2010; 18: 2131–2137.
Volkow ND, Wang GJ, Telang F, Fowler JS, Goldstein RZ, Alia-Klein N et al. Inverse association between BMI and prefrontal metabolic activity in healthy adults. Obesity 2008; 17: 60–65.
Haley AP, Sweet LH, Gunstad J, Forman DE, Poppas A, Paul RH et al. Verbal working memory and atherosclerosis in patients with cardiovascular disease: an fMRI study. J Neuroimaging 2007; 17: 227–233.
Owen AM, McMillan KM, Laird AR, Bullmore E . N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 2005; 25: 46–59.
Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC . A parametric study of prefrontal cortex involvement in human working memory. Neuroimage 1997; 5: 49–62.
Pouliot M-C, Després J-P, Lemieux S, Moorjani S, Bouchard C, Tremblay A et al. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994; 73: 460–468.
World Health Organization. Waist Circumference and Waist-Hip Ratio: Report of a WHO Expert Consulation. World Health Organization: Geneva, Switzerland, 2008.
Folstein MF, Folstein SE, McHugh PR . Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12: 189–198.
Wechsler D . WASI II: Wechsler Abbreviated Scale of Intelligence. 2nd edn. Psychological Corporation: San Antonio, TX, USA, 2011.
Delis DC, Kramer JH, Kaplan E, Ober BA . California Verbal Learning Test. 2nd edn. The Psychological Corporation: San Antonio, TX, USA, 2000.
Reitan RM . Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills 1958; 8: 271–276.
Ruff RM, Light RH, Parker SB, Levin HS . Benton Controlled Oral Word Association Test: reliability and updated norms. Arch Clin Neuropsychol 1996; 11: 329–338.
Wechsler D . Wechsler Adult Intelligence Scale. 4th edn. Psychological Corporation: San Antonio, TX, USA, 2008.
Golden CJ . Stroop Color and Word Test: A Manual for Clinical and Experimental Uses. Skoelting: Chicago, IL, USA, 1978.
Jenkinson M, Bannister P, Brady M, Smith S . Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002; 17: 825–841.
Smith SM . Fast robust automated brain extraction. Hum Brain Mapp 2002; 17: 143–155.
Jaeggi SM, Buschkuehl M, Perrig WJ, Meier B . The concurrent validity of the N-back task as a working memory measure. Memory 2010; 18: 394–412.
Laird AR, Robinson JL, McMillan KM, Tordesillas-Gutiérrez D, Moran ST, Gonzales SM et al. Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: Validation of the Lancaster transform. Neuroimage 2010; 51: 677–683.
Galioto RM, Alosco ML, Spitznagel MB, Stanek KM, Gunstad J . Cognitive reserve preserves cognitive function in obese individuals. Aging Neuropsychol C 2013; 20: 684–699.
Baddeley A . Working memory. Science 1992; 255: 556–559.
Cabeza R, Anderson ND, Locantore JK, McIntosh AR . Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 2002; 17: 1394–1402.
Rypma B, D’Esposito M . Isolating the neural mechanisms of age-related changes in human working memory. Nat Neurosci 2000; 3: 509–515.
Malavazos AE, Corsi MM, Ermetici F, Coman C, Sardanelli F, Rossi A et al. Proinflammatory cytokines and cardiac abnormalities in uncomplicated obesity: relationship with abdominal fat deposition. Nutr Metab Cardiovasc Dis 2007; 17: 294–302.
Banks WA, Kastin AJ, Broadwell RD . Passage of cytokines across the blood-brain barrier. Neuroimmunomodulation 1995; 2: 241–248.
Koutsilieri E, Scheller C, Tribl F, Riederer P . Degeneration of neuronal cells due to oxidative stress—microglial contribution. Parkinsonism Relat Disord 2002; 8: 401–406.
Weaver JD, Huang M-H, Albert M, Harris T, Rowe JW, Seeman TE . Interleukin-6 and risk of cognitive decline MacArthur Studies of Successful Aging. Neurology 2002; 59: 371–378.
Jefferson AL, Massaro JM, Wolf PA, Seshadri S, Au R, Vasan RS et al. Inflammatory biomarkers are associated with total brain volume The Framingham Heart Study. Neurology 2007; 68: 1032–1038.
Satizabal CL, Zhu YC, Mazoyer B, Dufouil C, Tzourio C . Circulating IL-6 and CRP are associated with MRI findings in the elderly The 3C-Dijon Study. Neurology 2012; 78: 720–727.
Tan ZS, Beiser AS, Vasan RS, Roubenoff R, Dinarello CA, Harris TB et al. Inflammatory markers and the risk of Alzheimer disease The Framingham Study. Neurology 2007; 68: 1902–1908.
Hull M, Strauss S, Berger M, Volk B, Bauer J . The participation of interleukin-6, a stress-inducible cytokine, in the pathogenesis of Alzheimer’s disease. Behav Brain Res 1996; 78: 37–41.
Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1995; 1: 1155–1161.
Banks WA, Kastin AJ, Huang W, Jaspan JB, Maness LM . Leptin enters the brain by a saturable system independent of insulin. Peptides 1996; 17: 305–311.
Oomura Y, Aou S, Fukunaga K . Prandial increase of leptin in the brain activates spatial learning and memory. Pathophysiology 2010; 17: 119–127.
Banerji MA, Buckley MC, Chaiken RL, Gordon D, Lebovitz HE, Kral JG . Liver fat, serum triglycerides and visceral adipose tissue in insulin-sensitive and insulin-resistant black men with NIDDM. Int J Obes Relat Metab Disord 1995; 19: 846–850.
Banks WA, Coon AB, Robinson SM, Moinuddin A, Shultz JM, Nakaoke R et al. Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 2004; 53: 1253–1260.
Holden KF, Lindquist K, Tylavsky FA, Rosano C, Harris TB, Yaffe K . Serum leptin level and cognition in the elderly: Findings from the Health ABC Study. Neurobiol Aging 2009; 30: 1483–1489.
Pannacciulli N, Le DSN, Chen K, Reiman EM, Krakoff J . Relationships between plasma leptin concentrations and human brain structure: a voxel-based morphometric study. Neurosci Lett 2007; 412: 248–253.
Huang X-F, Zavitsanou K, Huang X, Yu Y, Wang H, Chen F et al. Dopamine transporter and D2 receptor binding densities in mice prone or resistant to chronic high fat diet-induced obesity. Behav Brain Res 2006; 175: 415–419.
Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W et al. Brain dopamine and obesity. Lancet 2001; 357: 354–357.
Brunetti L, Orlando G, Recinella L, Michelotto B, Ferrante C, Vacca M . Resistin, but not adiponectin, inhibits dopamine and norepinephrine release in the hypothalamus. Eur J Pharmacol 2004; 493: 41–44.
Brunetti L, Michelotto B, Orlando G, Vacca M . Leptin inhibits norepinephrine and dopamine release from rat hypothalamic neuronal endings. Eur J Pharmacol 1999; 372: 237–240.
Vernaleken I, Buchholz H-G, Kumakura Y, Siessmeier T, Stoeter P, Bartenstein P et al. ‘Prefrontal’ cognitive performance of healthy subjects positively correlates with cerebral FDOPA influx: An exploratory [18F]-fluoro-L-DOPA-PET investigation. Hum Brain Mapp 2007; 28: 931–939.
Mozley LH, Gur RC, Mozley PD, Gur RE . Striatal dopamine transporters and cognitive functioning in healthy men and women. Am J Psychiatry 2001; 158: 1492–1499.
Seamans JK, Yang CR . The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 2004; 74: 1–58.
Bäckman L, Karlsson S, Fischer H, Karlsson P, Brehmer Y, Rieckmann A et al. Dopamine D(1) receptors and age differences in brain activation during working memory. Neurobiol Aging 2011; 32: 1849–1856.
Acknowledgements
This work was funded in part by grants from the National Institute of Neurological Disorders and Stroke (R01NS75565, APH) and the National Institute on Aging (F31AG040890, MMG).
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Gonzales, M., Kaur, S., Eagan, D. et al. Central adiposity and the functional magnetic resonance imaging response to cognitive challenge. Int J Obes 38, 1193–1199 (2014). https://doi.org/10.1038/ijo.2014.5
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DOI: https://doi.org/10.1038/ijo.2014.5
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