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Socioeconomic status is positively correlated with frontal white matter integrity in aging

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Abstract

Socioeconomic status (SES) is an important reserve variable which has been shown to benefit the aging brain’s macrostructure. However, it remains unknown whether SES affects age-related changes in the brain’s white matter (WM) microstructure. Here, we used diffusion tensor imaging to explore the relationship between SES and three components of the diffusion tensor [fractional anisotropy (FA), axial diffusivity, and radial diffusivity (DR)]. Participants were 40 (16 male) cognitively normal young adults (mean age = 33.3 years, SD = 4.27) and 44 (19 male) cognitively normal community dwelling seniors (mean age = 66.2 years, SD = 7.5). Age-related FA declines were observed across a large portion of the WM skeleton. However, seniors with high SES showed lower age-related WM integrity declines in three frontal tracts: the right anterior corona radiata and bilateral portions of WM underlying the superior frontal gyri (SFG–WM). Positive SES–FA correlations were primarily driven by negative DR–SES correlations, suggesting that SES may buffer age-related declines in myelin. The functional significance of high SES in these frontal tracts was demonstrated through positive correlations with working memory performance. Possible mechanisms through which SES may attenuate the effects of age on frontal WM integrity are discussed.

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References

  • Abe O, Aoki S, Hayashi N, Yamada H, Kunimatsu A, Mori H, Yoshikawa T, Okubo T, Ohtomo K (2002) Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 23(3):433–441

    Article  PubMed  Google Scholar 

  • Andersen I, Burr H, Kristensen TS, Gamborg M, Osler M, Prescott E, Diderichsen F (2004) Do factors in the psychosocial work environment mediate the effect of socioeconomic position on the risk of myocardial infarction? Study from the Copenhagen Centre for Prospective Population Studies. Occup Environ Med 61(11):886–892

    Article  PubMed  CAS  Google Scholar 

  • Anttila T, Helkala EL, Viitanen M, Kareholt I, Fratiglioni L, Winblad B, Soininen H, Tuomilehto J, Nissinen A, Kivipelto M (2004) Alcohol drinking in middle age and subsequent risk of mild cognitive impairment and dementia in old age: a prospective population based study. BMJ 329(7465):539

    Article  PubMed  Google Scholar 

  • Arenaza-Urquijo EM, Bosch B, Sala-Llonch R, Sole-Padulles C, Junque C, Fernandez-Espejo D, Bargallo N, Rami L, Molinuevo JL, Bartres-Faz D (2011) Specific anatomic associations between white matter integrity and cognitive reserve in normal and cognitively impaired elders. Am J Geriatr Psychiatr Off J Am Assoc Geriatri Psychiatr 19(1):33–42

    Article  Google Scholar 

  • Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34(1):51–61

    Article  PubMed  CAS  Google Scholar 

  • Babcock RL, Salthouse TA (1990) Effects of increased processing demands on age differences in working memory. Psychol Aging 5(3):421–428

    Article  PubMed  CAS  Google Scholar 

  • Baddeley A (2000) The episodic buffer: a new component of working memory? Trends Cogn Sci 4(11):417–423

    Article  PubMed  Google Scholar 

  • Bartres-Faz D, Sole-Padulles C, Junque C, Rami L, Bosch B, Bargallo N, Falcon C, Sanchez-Valle R, Molinuevo JL (2009) Interactions of cognitive reserve with regional brain anatomy and brain function during a working memory task in healthy elders. Biol Psychol 80(2):256–259

    Article  PubMed  Google Scholar 

  • Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111(3):209–219

    Article  PubMed  CAS  Google Scholar 

  • Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632

    Article  PubMed  CAS  Google Scholar 

  • Bradl M, Lassmann H (2010) Oligodendrocytes: biology and pathology. Acta Neuropathol 119(1):37–53

    Article  PubMed  Google Scholar 

  • Brayne C, Ince PG, Keage HA, McKeith IG, Matthews FE, Polvikoski T, Sulkava R (2010) Education, the brain and dementia: neuroprotection or compensation? Brain J Neurol 133(Pt 8):2210–2216

    Article  Google Scholar 

  • Burzynska AZ, Preuschhof C, Backman L, Nyberg L, Li SC, Lindenberger U, Heekeren HR (2010) Age-related differences in white matter microstructure: region-specific patterns of diffusivity. NeuroImage 49(3):2104–2112

    Article  PubMed  CAS  Google Scholar 

  • Cattell RB, Cattell AKS (1960) Handbook for the individual or group culture fair intelligence test. In: U.S.A. IfPaAT, editor

  • Chiang MC, McMahon KL, de Zubicaray GI, Martin NG, Hickie I, Toga AW, Wright MJ, Thompson PM (2011) Genetics of white matter development: a DTI study of 705 twins and their siblings aged 12 to 29. NeuroImage 54(3):2308–2317

    Article  PubMed  Google Scholar 

  • Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF (2006) Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 61(11):1166–1170

    Article  PubMed  Google Scholar 

  • Deary IJ, Leaper SA, Murray AD, Staff RT, Whalley LJ (2003) Cerebral white matter abnormalities and lifetime cognitive change: a 67-year follow-up of the Scottish Mental Survey of 1932. Psychol Aging 18(1):140–148

    Article  PubMed  Google Scholar 

  • den Heijer T, Vermeer SE, van Dijk EJ, Prins ND, Koudstaal PJ, van Duijn CM, Hofman A, Breteler MM (2004) Alcohol intake in relation to brain magnetic resonance imaging findings in older persons without dementia. Am J Clin Nutr 80(4):992–997

    Google Scholar 

  • D'Esposito M, Detre JA, Alsop DC, Shin RK, Atlas S, Grossman M (1995) The neural basis of the central executive system of working memory. Nature 378(6554):279–281

    Article  PubMed  Google Scholar 

  • Dobbs AR, Rule BG (1989) Adult age differences in working memory. Psychol Aging 4(4):500–503

    Article  PubMed  CAS  Google Scholar 

  • Dufouil C, Tzourio C, Brayne C, Berr C, Amouyel P, Alperovitch A (2000) Influence of apolipoprotein E genotype on the risk of cognitive deterioration in moderate drinkers and smokers. Epidemiology 11(3):280–284

    Article  PubMed  CAS  Google Scholar 

  • Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth O, Larsen VA, Walhovd KB (2011) Memory training impacts short-term changes in aging white matter: a longitudinal diffusion tensor imaging study. Hum Brain Mapp 33(10):2390–2406

    Article  PubMed  Google Scholar 

  • Gold BT, Powell DK, Andersen AH, Smith CD (2010) Alterations in multiple measures of white matter integrity in normal women at high risk for Alzheimer's disease. NeuroImage 52(4):1487–1494

    Article  PubMed  Google Scholar 

  • Gold BT, Johnson NF, Powell DK, Smith CD (2012) White matter integrity and vulnerability to Alzheimer's disease: preliminary findings and future directions. Biochim Biophys Acta 1822(3):416–422

    Article  PubMed  CAS  Google Scholar 

  • Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 14(1 Pt 1):21–36

    Article  PubMed  CAS  Google Scholar 

  • Groeger JA, Field D, Hammond SM (1999) Measuring memory span. Int J Psychol 34(5–6):359–363

    Article  Google Scholar 

  • Gyllensten L, Malmfors T (1963) Myelinization of the optic nerve and its dependence on visual function—a quantitative investigation in mice. J Embryol Exp Morpholog 11:255–266

    CAS  Google Scholar 

  • Hackman DA, Farah MJ (2009) Socioeconomic status and the developing brain. Trends Cogn Sci 13(2):65–73

    Article  PubMed  Google Scholar 

  • Hackman DA, Farah MJ, Meaney MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat Rev Neurosci 11(9):651–659

    Article  PubMed  CAS  Google Scholar 

  • Head D, Buckner RL, Shimony JS, Williams LE, Akbudak E, Conturo TE, McAvoy M, Morris JC, Snyder AZ (2004) Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cereb Cortex 14(4):410–423

    Article  PubMed  Google Scholar 

  • Hollingshead AB (1958) Social class and mental illness. Wiley, New York

    Book  Google Scholar 

  • Johnson NF, Kim C, Clasey JL, Bailey A, Gold BT (2012) Cardiorespiratory fitness is positively correlated with cerebral white matter integrity in healthy seniors. NeuroImage 59(2):1514–1523

    Article  PubMed  Google Scholar 

  • Kristensen TS, Borg V, Hannerz H (2002) Socioeconomic status and psychosocial work environment: results from a Danish national study. Scand J Public Health 59:41–8

    Google Scholar 

  • Le Bihan D (2003) Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4(6):469–480

    Article  PubMed  Google Scholar 

  • Lovden M, Bodammer NC, Kuhn S, Kaufmann J, Schutze H, Tempelmann C, Heinze HJ, Duzel E, Schmiedek F, Lindenberger U (2010) Experience-dependent plasticity of white-matter microstructure extends into old age. Neuropsychologia 48(13):3878–3883

    Article  PubMed  Google Scholar 

  • Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. NeuroImage 21(3):1174–1181

    Article  PubMed  Google Scholar 

  • Marengoni A, Fratiglioni L, Bandinelli S, Ferrucci L (2011) Socioeconomic status during lifetime and cognitive impairment no-dementia in late life: the population-based aging in the Chianti Area (InCHIANTI) Study. J Alzheimers Dis JAD 24(3):559–568

    Google Scholar 

  • Omlin FX (1997) Optic disc and optic nerve of the blind cape mole-rat (Georychus capensis): a proposed model for naturally occurring reactive gliosis. Brain Res Bull 44(5):627–632

    Article  PubMed  CAS  Google Scholar 

  • O'Sullivan M, Jones DK, Summers PE, Morris RG, Williams SC, Markus HS (2001) Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 57(4):632–638

    Article  PubMed  Google Scholar 

  • Park DC, Hertzog C, Kidder DP, Morrell RW, Mayhorn CB (1997) Effect of age on event-based and time-based prospective memory. Psychol Aging 12(2):314–327

    Article  PubMed  CAS  Google Scholar 

  • Pfefferbaum A, Sullivan EV, Hedehus M, Lim KO, Adalsteinsson E, Moseley M (2000) Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn Reson Med 44(2):259–268

    Article  PubMed  CAS  Google Scholar 

  • Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637–648

    PubMed  CAS  Google Scholar 

  • Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, Hawkes DJ (1999) Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 18(8):712–721

    Article  PubMed  CAS  Google Scholar 

  • Salat DH, Tuch DS, Greve DN, van der Kouwe AJ, Hevelone ND, Zaleta AK, Rosen BR, Fischl B, Corkin S, Rosas HD, Dale AM (2005a) Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol Aging 26(8):1215–1227

    Article  PubMed  CAS  Google Scholar 

  • Salat DH, Tuch DS, Hevelone ND, Fischl B, Corkin S, Rosas HD, Dale AM (2005b) Age-related changes in prefrontal white matter measured by diffusion tensor imaging. Ann N Y Acad Sci 1064:37–49

    Article  PubMed  CAS  Google Scholar 

  • Salmon E, Van der Linden M, Collette F, Delfiore G, Maquet P, Degueldre C, Luxen A, Franck G (1996) Regional brain activity during working memory tasks. Brain J Neurol 119(Pt 5):1617–1625

    Article  Google Scholar 

  • Satz P (1993) Brain reserve capacity on symptom onset after brain injury: a formation and review of evidence for threshold theory. Neuropsychology 7(3):273–295

    Article  Google Scholar 

  • Schretlen D, Pearlson GD, Anthony JC, Aylward EH, Augustine AM, Davis A, Barta P (2000) Elucidating the contributions of processing speed, executive ability, and frontal lobe volume to normal age-related differences in fluid intelligence. J Int Neuropsychol Soc: JINS 6(1):52–61

    PubMed  CAS  Google Scholar 

  • Sen PN, Basser PJ (2005) A model for diffusion in white matter in the brain. Biophys J 89(5):2927–2938

    Article  PubMed  CAS  Google Scholar 

  • Singh-Manoux A, Marmot MG, Glymour M, Sabia S, Kivimaki M, Dugravot A (2011) Does cognitive reserve shape cognitive decline? Ann Neurol 70(2):296–304

    Article  PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31(4):1487–1505

    Article  PubMed  Google Scholar 

  • Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Markesbery WR (2007) Age and gender effects on human brain anatomy: a voxel-based morphometric study in healthy elderly. Neurobiol Aging 28(7):1075–1087

    Article  PubMed  Google Scholar 

  • Smith CD, Chebrolu H, Andersen AH, Powell DA, Lovell MA, Xiong S, Gold BT (2010) White matter diffusion alterations in normal women at risk of Alzheimer's disease. Neurobiol Aging 31(7):1122–1131

    Article  PubMed  Google Scholar 

  • Sole-Padulles C, Bartres-Faz D, Junque C, Vendrell P, Rami L, Clemente IC, Bosch B, Villar A, Bargallo N, Jurado MA, Barrios M, Molinuevo JL (2009) Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 30(7):1114–1124

    Article  PubMed  CAS  Google Scholar 

  • Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 17(3):1429–1436

    Article  PubMed  Google Scholar 

  • Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage 26(1):132–140

    Article  PubMed  Google Scholar 

  • Stern Y (2009) Cognitive reserve. Neuropsychologia 47(10):2015–2028

    Article  PubMed  Google Scholar 

  • Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R (1994) Influence of education and occupation on the incidence of Alzheimer's disease. JAMA: J Am Med Assoc 271(13):1004–1010

    Article  CAS  Google Scholar 

  • Stern Y, Alexander GE, Prohovnik I, Stricks L, Link B, Lennon MC, Mayeux R (1995a) Relationship between lifetime occupation and parietal flow: implications for a reserve against Alzheimer's disease pathology. Neurology 45(1):55–60

    Article  PubMed  CAS  Google Scholar 

  • Stern Y, Tang MX, Denaro J, Mayeux R (1995b) Increased risk of mortality in Alzheimer's disease patients with more advanced educational and occupational attainment. Ann Neurol 37(5):590–595

    Article  PubMed  CAS  Google Scholar 

  • Teipel SJ, Meindl T, Wagner M, Kohl T, Burger K, Reiser MF, Herpertz S, Moller HJ, Hampel H (2009) White matter microstructure in relation to education in aging and Alzheimer's disease. J Alzheimers Dis: JAD 17(3):571–583

    PubMed  Google Scholar 

  • Valenzuela MJ, Sachdev P (2006) Brain reserve and dementia: a systematic review. Psychol Med 36(4):441–454

    Article  PubMed  Google Scholar 

  • Wechsler DS (1997) Wechsler adult intelligence scale, 3rd edn. (WAIS-3®). Harcourt Assessment, San Antonio

    Google Scholar 

  • Wheeler-Kingshott CA, Cercignani M (2009) About "axial" and "radial" diffusivities. Mag Reson Med: Off J Soc Mag Reson Med / Soc Mag Reson Med 61(5):1255–1260

    Article  Google Scholar 

  • Wiegersma S, Meertse K (1990) Subjective ordering, working memory, and aging. Exp Aging Res 16(1–2):73–77

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by NIH grant AG033036 and NSF grant BCS 0814302. We thank Sara E. Cilles for her assistance in recruiting, scanning, and testing participants. In addition, we gratefully acknowledge our collaborators at the Sanders-Brown Center on Aging at the University of Kentucky.

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Correspondence to Brian T. Gold.

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Johnson, N.F., Kim, C. & Gold, B.T. Socioeconomic status is positively correlated with frontal white matter integrity in aging. AGE 35, 2045–2056 (2013). https://doi.org/10.1007/s11357-012-9493-8

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