Socioeconomic status and structural brain development

Natalie H Brito, Kimberly G Noble, Natalie H Brito, Kimberly G Noble

Abstract

Recent advances in neuroimaging methods have made accessible new ways of disentangling the complex interplay between genetic and environmental factors that influence structural brain development. In recent years, research investigating associations between socioeconomic status (SES) and brain development have found significant links between SES and changes in brain structure, especially in areas related to memory, executive control, and emotion. This review focuses on studies examining links between structural brain development and SES disparities of the magnitude typically found in developing countries. We highlight how highly correlated measures of SES are differentially related to structural changes within the brain.

Keywords: brain development; environmental variation; socioeconomic status; structural imaging.

Figures

Figure 1
Figure 1
Hypothesized mechanisms by which SES operates to influence structural and functional brain development.

References

    1. Adler N. E., Boyce T., Chesney M. A., Cohen S., Folkman S., Kahn R. L., et al. (1994). Socioeconomic status and health: the challenge of the gradient. Am. Psychol. 49:15 10.1037/0003-066X.49.1.15
    1. Adler N. E., Epel E. S., Castellazzo G., Ickovics J. R. (2000). Relationship of subjective and objective social status with psychological and physiological functioning: preliminary data in healthy white women. Health Psychol. 19, 586–592 10.1037/0278-6133.19.6.586
    1. Anderson N. B., Armstead C. A. (1995). Toward understanding the association of socioeconomic status and health: a new challenge for the biopsychosocial approach. Psychosom. Med. 57, 213–225 10.1097/00006842-199505000-00003
    1. Bradley R. H., Corwyn R. F. (2002). Socioeconomic status and child development. Annu. Rev. Psychol. 53, 371–399 10.1146/annurev.psych.53.100901.135233
    1. Bradley R. H., Corwyn R. F., Burchinal M., McAdoo H. P., García Coll C. (2001). The home environments of children in the United States Part II: relations with behavioral development through age thirteen. Child Dev. 72, 1868–1886 10.1111/1467-8624.t01-1-00383
    1. Brain Development Cooperative Group. (2012). Total and regional brain volumes in a population-based normative sample from 4 to 18 years: the NIH MRI study of normal brain development. Cereb. Cortex 22, 1–12 10.1093/cercor/bhr018
    1. Brooks-Gunn J., Duncan G. J. (1997). The effects of poverty on children. Future Child. 7, 55–71 10.2307/1602387
    1. Buss C., Lord C., Wadiwalla M., Hellhammer D. H., Lupien S. J., Meaney M. J., et al. (2007). Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men. J. Neurosci. 27, 2592–2595 10.1523/JNEUROSCI.3252-06.2007
    1. Butterworth P., Cherbuin N., Sachdev P., Anstey K. J. (2012). The association between financial hardship and amygdala and hippocampal volumes: results from the PATH through life project. Soc. Cogn. Affect. Neurosci. 7, 548–556 10.1093/scan/nsr027
    1. Cavanagh J., Krishnadas R., Batty G. D., Burns H., Deans K. A., Ford I., et al. (2013). Socioeconomic status and the cerebellar grey matter volume. Data from a well-characterized population sample. Cerebellum 12, 882–891 10.1007/s12311-013-0497-4
    1. Chiang M. C., McMahon K. L., de Zubicaray G. I., Martin N. G., Hickie I., Toga A. W., et al. (2011). Genetics of white matter development: a DTI study of 705 twins and their siblings aged 12 to 29. Neuroimage 54, 2308–2317 10.1016/j.neuroimage.2010.10.015
    1. Conboy B. T., Kuhl P. K. (2007). Early speech perception: developing a culturally specific way of listening through social interaction, in On Being Moved: From Mirror Neurons to Empathy, ed Braten S. (Amsterdam: John Benjamins; ), 175–199 10.1075/aicr.68.15con
    1. Duncan G., Brooks-Gunn J., Yeung J., Smith J. (1998). How much does childhood poverty affect the life chances of children? Am. Sociol. Rev. 63, 406–423
    1. Duncan G. J. (1988). The volatility of family income over the life course, in Life-Span Development and Behavior, eds Baltes P., Featherman D., Lerner R. M. (Hillsdale, NJ: Lawrence Erlbaum Associates; ), 317–358
    1. Duncan G. J., Brooks-Gunn J., Klebanov P. K. (1994). Economic deprivation and early childhood development. Child Dev. 65, 296–318 10.2307/1131385
    1. Duncan G. J., Magnuson K. (2012). Socioeconomic status and cognitive functioning: moving from correlation to causation. Wiley Interdiscip. Rev. Cogn. Sci. 3, 377–386 10.1002/wcs.1176
    1. Duncan G. J., Magnuson K. A. (2003). Off with Hollingshead: socioeconomic resources, parenting, and child development, in Socioeconomic Status, Parenting, and Child Development, eds Bornstein M. H., Bradley R. H. (Mahwah, NJ: Lawrence Erlbaum; ), 83–106
    1. Eckert M. A., Lombardino L. J., Leonard C. M. (2001). Planar asymmetry tips the phonological playground and environment raises the bar. Child Dev. 72, 988–1002 10.1111/1467-8624.00330
    1. Evans G. W. (2006). Child development and the physical environment. Annu. Rev. Psychol. 57, 423–451 10.1146/annurev.psych.57.102904.190057
    1. Evans G. W., English K. (2002). The environment of poverty: multiple stressor exposure, psychophysiological stress, and socioemotional adjustment. Child Dev. 73, 1238–1248 10.1111/1467-8624.00469
    1. Gianaros P. J., Horenstein J. A., Cohen S., Matthews K. A., Brown S. M., Flory J. D., et al. (2007). Perigenual anterior cingulate morphology covaries with perceived social standing. Soc. Cogn. Affect. Neurosci. 2, 161–173 10.1093/scan/nsm013
    1. Gianaros P. J., Marsland A. L., Sheu L. K., Erickson K. I., Verstynen T. D. (2012). Inflammatory pathways link socioeconomic inequalities to white matter architecture. Cereb. Cortex 23, 2058–2071 10.1093/cercor/bhs191
    1. Giedd J. N., Rapoport J. L. (2010). Structural MRI of pediatric brain development: what have we learned and where are we going? Neuron 67, 728–734 10.1016/j.neuron.2010.08.040
    1. Gottfried A. W., Gottfried A. E., Bathurst K., Guerin D. W., Parramore M. M. (2003). Socioeconomic status in children's development and family environment: infancy through adolescence, in Socioeconomic Status, Parenting and Child Development, eds Bornstein M. H., Bradley R. H. (Mahwah, NJ: Lawrence Erlbaum; ), 189–207
    1. Grieve S. M., Korgaonkar M. S., Clark C. R., Williams L. M. (2011). Regional heterogeneity in limbic maturational changes: evidence from integrating cortical thickness, volumetric and diffusion tensor imaging measures. Neuroimage 55, 868–879 10.1016/j.neuroimage.2010.12.087
    1. Guryan J., Hurst E., Kearney M. (2008). Parental education and parental time with children. J. Econ. Perspect. 22, 23–46 10.1257/jep.22.3.23
    1. Hackman D. A., Betancourt L. M., Gallop R., Romer D., Brodsky N. L., Hurt H., et al. (2014). Mapping the trajectory of socioeconomic disparity in working memory: parental and neighborhood factors. Child Dev. 85, 1433–1445 10.1111/cdev.12242
    1. Hackman D. A., Farah M. J. (2009). Socioeconomic status and the developing brain. Trends Cogn. Sci. 13, 65–73 10.1016/j.tics.2008.11.003
    1. Hanson J. L., Chandra A., Wolfe B. L., Pollak S. D. (2011). Association between income and the hippocampus. PLoS ONE 6:e18712 10.1371/journal.pone.0018712
    1. Hanson J. L., Hair N., Shen D. G., Shi F., Gilmore J. H., Wolfe B. L., et al. (2013). Family poverty affects the rate of human infant brain growth. PLoS ONE 8:e80954 10.1371/journal.pone.0080954
    1. Hart B., Risley T. R. (1995). Meaningful Differences in the Everyday Experience of Young American Children. Baltimore, MD: Paul H Brookes Publishing
    1. Hoff E. (2003). The specificity of environmental influence: socioeconomic status affects early vocabulary development via maternal speech. Child Dev. 74, 1368–1378 10.1111/1467-8624.00612
    1. Hoff-Ginsberg E., Tardif T. (1995). Socioeconomic status and parenting, in Handbook of Parenting, Volume 2: Biology and Ecology of parenting, ed Bornstein M. H. (Hillsdale, NJ: Lawrence Erlbaum Associates; ), 161–188
    1. Hollingshead A. A. (1975). Four-Factor Index of Social Status. New Haven, CT: Yale University
    1. Hu P., Adler N. E., Goldman N., Weinstein M., Seeman T. E. (2005). Relationship between subjective social status and measures of health in older Taiwanese persons. J. Am. Geriatr. Soc. 53, 483–488 10.1111/j.1532-5415.2005.53169.x
    1. Jednoróg K., Altarelli I., Monzalvo K., Fluss J., Dubois J., Billard C., et al. (2012). The influence of socioeconomic status on children's brain structure. PLoS ONE 7:e42486 10.1371/journal.pone.0042486
    1. Jencks C., Perman L., Rainwater L. (1988). What is a good job? A new measure of labor-market success. Am. J. Sociol. 93, 1322–1357 10.1086/228903
    1. Kopp M., Skrabski Á., Réthelyi J., Kawachi I., Adler N. E. (2004). Self-rated health, subjective social status, and middle-aged mortality in a changing society. Behav. Med. 30, 65–72 10.3200/BMED.30.2.65-72
    1. Krishnadas R., Kim J., McLean J., Batty G. D., McLean J. S., Millar K., et al. (2013). The environment and the connectome: exploring the structural noise in the human brain associated with socioeconomic deprivation. Front. Hum. Neurosci. 7:722 10.3389/fnhum.2013.00722
    1. Kuhl P. K. (2007). Is speech learning “gated” by the social brain? Dev. Sci. 10, 110–120 10.1111/j.1467-7687.2007.00572.x
    1. Kuhl P. K., Tsao F.-M., Liu H.-M. (2003). Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. Proc. Natl. Acad. Sci. U.S.A. 100, 9096–9101 10.1073/pnas.1532872100
    1. Lange N., Froimowitz M. P., Bigler E. D., Lainhart J. E., Brain Development Cooperative Group. (2010). Associations between IQ, total and regional brain volumes, and demography in a large normative sample of healthy children and adolescents. Dev. Neuropsychol. 35, 296–317 10.1080/87565641003696833
    1. Lawson G. M., Duda J. T., Avants B. B., Wu J., Farah M. J. (2013). Associations between children's socioeconomic status and prefrontal cortical thickness. Dev. Sci. 16, 641–652 10.1111/desc.12096
    1. Lenroot R. K., Giedd J. N. (2006). Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci. Biobehav. Rev. 30, 718–729 10.1016/j.neubiorev.2006.06.001
    1. Leventhal T., Brooks-Gunn J. (2000). The neighborhoods they live in: the effects of neighborhood residence on child and adolescent outcomes. Psychol. Bull. 126, 309–337 10.1037/0033-2909.126.2.309
    1. Lipina S. J., Simonds J., Segretin M. S. (2011). Recognizing the child in child poverty. Vulnerable Child. Youth Stud. 6, 8–17 10.1080/17450128.2010.521598
    1. Liston C., McEwen B. S., Casey B. J. (2009). Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc. Natl. Acad. Sci. U.S.A. 106, 912–917 10.1073/pnas.0807041106
    1. Liu Y., Julkunen V., Paajanen T., Westman E., Wahlund L. O., Aitken A., et al. (2012). Education increases reserve against Alzheimer's disease—evidence from structural MRI analysis. Neuroradiology 54, 929–938 10.1007/s00234-012-1005-0
    1. Luby J., Belden A., Botteron K., Marrus N., Harms M. P., Babb C., et al. (2013). The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatr. 167, 1135–1142 10.1001/jamapediatrics.2013.3139
    1. McEwen B. S., Gianaros P. J. (2010). Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease. Ann. N.Y. Acad. Sci. 1186, 190–222 10.1111/j.1749-6632.2009.05331.x
    1. McLoyd V. C. (1997). The impact of poverty and low socioeconomic status on the socioemotional functioning of African-American children and adolescents: mediating effects, in Social and Emotional Adjustment and Family Relations in Ethnic Minority Families, eds Taylor R. D., Wang M. (Mahwah, NJ: Erlbaum; ), 7–34
    1. McLoyd V. C. (1998). Socioeconomic disadvantage and child development. Am. Psychol. 53:185 10.1037/0003-066X.53.2.185
    1. Minujin A., Delamonica E., Davidziuk A., Gonzalez E. D. (2006). The definition of child poverty: a discussion of concepts and measurement. Environ. Urban. 18, 481–500 10.1177/0956247806069627
    1. Mutlu A. K., Schneider M., Debbané M., Badoud D., Eliez S., Schaer M. (2013). Sex differences in thickness, and folding developments throughout the cortex. Neuroimage 82, 200–207 10.1016/j.neuroimage.2013.05.076
    1. National Institute of Child Health Human Development Early Child Care Research Network (2005). Duration and developmental timing of poverty and children's cognitive and social development from birth through third grade. Child Dev. 76, 795–810 10.1111/j.1467-8624.2005.00878.x
    1. Noble K. G., Grieve S. M., Korgaonkar M. S., Engelhardt L. E., Griffith E. Y., Williams L. M., et al. (2012b). Hippocampal volume varies with educational attainment across the life-span. Front. Hum. Neurosci. 6:307 10.3389/fnhum.2012.00307
    1. Noble K. G., Houston S. M., Kan E., Sowell E. R. (2012a). Neural correlates of socioeconomic status in the developing human brain. Dev. Sci. 15, 516–527 10.1111/j.1467-7687.2012.01147.x
    1. Noble K. G., Korgaonkar M. S., Grieve S. M., Brickman A. M. (2013). Higher education is an age-independent predictor of white matter integrity and cognitive control in late adolescence. Dev. Sci. 16, 653–664 10.1111/desc.12077
    1. Panizzon M. S., Fennema-Notestine C., Eyler L. T., Jernigan T. L., Prom-Wormley E., Neale M., et al. (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cereb. Cortex 19, 2728–2735 10.1093/cercor/bhp026
    1. Paus T. (2005). Mapping brain maturation and cognitive development during adolescence. Trends Cogn. Sci. 9, 60–68 10.1016/j.tics.2004.12.008
    1. Paus T., Zijdenbos A., Worsley K., Collins D. L., Blumenthal J., Giedd J. N., et al. (1999). Structural maturation of neural pathways in children and adolescents: in vivo study. Science 283, 1908–1911
    1. Pickett K. E., Pearl M. (2001). Multilevel analyses of neighbourhood socioeconomic context and health outcomes: a critical review. J. Epidemiol. Community Health 55, 111–122 10.1136/jech.55.2.111
    1. Piras F., Cherubini A., Caltagirone C., Spalletta G. (2011). Education mediates microstructural changes in bilateral hippocampus. Hum. Brain Mapp. 32, 282–289 10.1002/hbm.21018
    1. Porter J. N., Collins P. F., Muetzel R. L., Lim K. O., Luciana M. (2011). Associations between cortical thickness and verbal fluency in childhood, adolescence, and young adulthood. Neuroimage 55, 1865–1877 10.1016/j.neuroimage.2011.01.018
    1. Raizada R. D., Richards T. L., Meltzoff A., Kuhl P. K. (2008). Socioeconomic status predicts hemispheric specialization of the left inferior frontal gyrus in young children. Neuroimage 40, 1392–1401 10.1016/j.neuroimage.2008.01.021
    1. Rakic P. (2009). Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724–735 10.1038/nrn2719
    1. Raznahan A., Lee Y., Stidd R., Long R., Greenstein D., Clasen L., et al. (2010). Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. Proc. Natl. Acad. Sci. U.S.A. 107, 16988–16993 10.1073/pnas.1006025107
    1. Raznahan A., Shaw P., Lalonde F., Stockman M., Wallace G. L., Greenstein D., et al. (2011). How does your cortex grow? J. Neurosci. 31, 7174–7177 10.1523/JNEUROSCI.0054-11.2011
    1. Rowe M. L., Goldin-Meadow S. (2009). Early gesture selectively predicts later language learning. Dev. Sci. 12, 182–187 10.1111/j.1467-7687.2008.00764.x
    1. Sampson R. J., Sharkey P., Raudenbush S. W. (2008). Durable effects of concentrated disadvantage on verbal ability among African-American children. Proc. Natl. Acad. Sci. 105, 845–852 10.1073/pnas.0710189104
    1. Schnack H. G., van Haren N. E., Brouwer R. M., Evans A., Durston S., Boomsma D. I., et al. (2014). Changes in Thickness and Surface Area of the Human Cortex and Their Relationship with Intelligence. Cereb. Cortex. [Epub ahead of print]. 10.1093/cercor/bht357
    1. Shaw P., Gilliam M., Liverpool M., Weddle C., Malek M., Sharp W., et al. (2011). Cortical development in typically developing children with symptoms of hyperactivity and impulsivity: support for a dimensional view of attention deficit hyperactivity disorder. American Journal of Psychiatry, 168,143–151 10.1176/appi.ajp.2010.10030385
    1. Smith J. R., Brooks-Gunn J., Klebanov P. (1997). The consequences of living in poverty for young children's cognitive and verbal ability and early school achievement, in Consequences of Growing Up Poor, eds Duncan G. J., Brooks-Gunn J. (New York, NY: Russell Sage Foundation; ), 132–189
    1. Sowell E. R., Peterson B. S., Thompson P. M., Welcome S. E., Henkenius A. L., Toga A. W. (2003). Mapping cortical change across the human life span. Nat. Neurosci. 6, 309–315 10.1038/nn1008
    1. Sowell E. R., Thompson P. M., Leonard C. M., Welcome S. E., Kan E., Toga A. W. (2004). Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 24, 8223–8231 10.1523/JNEUROSCI.1798-04.2004
    1. Staff R. T., Murray A. D., Ahearn T. S., Mustafa N., Fox H. C., Whalley L. J. (2012). Childhood socioeconomic status and adult brain size: childhood socioeconomic status influences adult hippocampal size. Ann. Neurol. 71, 653–660 10.1002/ana.22631
    1. Tottenham N., Sheridan M. (2010). A review of adversity, the amygdala, and the hippocampus: a consideration of developmental timing. Front. Hum. Neurosci. 3:68 10.3389/neuro.09.068.2009
    1. United States Census Bureau. (2012). Income, Poverty and Health Insurance in the United States: 2012 – Highlights. Available online at:
    1. Wight R. G., Aneshensel C. S., Miller-Martinez D., Botti- cello A. L., Cummings J. R., Karlamangla A. S., et al. (2006). Urban neighborhood context, educational attainment, and cognitive function among older adults. Am. J. Epidemiol. 163, 1071–1078 10.1093/aje/kwj176
    1. Winkler A. M., Kochunov P., Blangero J., Almasy L., Zilles K., Fox P. T., et al. (2010). Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 53, 1135–1146 10.1016/j.neuroimage.2009.12.028

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