Brain network coupling associated with cognitive performance varies as a function of a child’s environment in the ABCD study

1.Semega, J., Kollar, M., Creamer, J. & Mohanty, A. Income and poverty in the United States: 2018. Report P60–266. Current Population Reports https://www.census.gov/content/dam/Census/library/publications/2019/demo/p60-266.pdf (2019).2.Reardon, S. F. School segregation and racial academic achievement gaps. RSF Russell Sage Found. J. Soc. Sci. 2, 34–57 (2016). Google Scholar  3.Hoynes, H. W. & Schanzenbach, D. W. Safety net investments in children. Brookings Pap. Econ. Act. 89–150 https://doi.org/10.1353/eca.2018.0001 (2018).4.Farah, M. J. The neuroscience of socioeconomic status: Correlates, causes, and consequences. Neuron 96, 56–71 (2017).CAS  PubMed  Google Scholar  5.Johnson, S. B., Riis, J. L. & Noble, K. G. State of the art review: Poverty and the developing brain. Pediatrics 137, 1–17 (2016). Google Scholar  6.Hanson, J. L. et al. Family poverty affects the rate of human infant brain growth. PLoS One 8, 1–9 (2013). Google Scholar  7.Tooley, U. A., Bassett, D. S. & Mackey, A. P. Environmental influences on the pace of brain development. Nat. Rev. Neurosci. 22, 372–384 (2021).CAS  PubMed  Google Scholar  8.McLaughlin, K. A., Sheridan, M. A. & Lambert, H. K. Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neurosci. Biobehav. Rev. 47, 578–591 (2014).PubMed  PubMed Central  Google Scholar  9.Humphreys, K. L. & Zeanah, C. H. Deviations from the expectable environment in early childhood and emerging psychopathology. Neuropsychopharmacology 40, 1–59 (2015). Google Scholar  10.Mittal, C., Griskevicius, V., Simpson, J. A., Sung, S. & Young, E. S. Cognitive adaptations to stressful environments: When childhood adversity enhances adult executive function. J. Pers. Soc. Psychol. 109, 604–621 (2015).PubMed  Google Scholar  11.Frankenhuis, W. E., De Vries, S. A., Bianchi, J. & Ellis, B. J. Hidden talents in harsh conditions? A preregistered study of memory and reasoning about social dominance. 1–14 https://doi.org/10.1111/desc.12835 (2019).12.Young, E. S., Griskevicius, V., Simpson, J. A. & Waters, T. E. A. Can an unpredictable childhood environment enhance working memory? Test. Sensitized-Specialization Hypothesis. 114, 891–908 (2018). Google Scholar  13.Edelman, G. M. & Gally, J. A. Degeneracy and complexity in biological systems. Proc. Natl. Acad. Sci. U.S.A. https://doi.org/10.1073/pnas.231499798 (2001).14.Sheridan, M. A., Sarsour, K., Jutte, D., D’Esposito, M. & Boyce, W. T. The impact of social disparity on prefrontal function in childhood. PLoS One 7, 1–13 (2012). Google Scholar  15.Finn, A. S. et al. Functional brain organization of working memory in adolescents varies in relation to family income and academic achievement. Dev. Sci. 20, 1–15 (2017).ADS  Google Scholar  16.Merz, E. C., Wiltshire, C. A. & Noble, K. G. Socioeconomic inequality and the developing brain: Spotlight on language and executive function. Child Dev. Perspect. 13, 15–20 (2019). Google Scholar  17.Uddin, L. Q., Yeo, B. T. T. & Spreng, R. N. Towards a universal taxonomy of macro-scale functional human brain networks. Brain Topogr. 32, 926–942 (2019).PubMed  PubMed Central  Google Scholar  18.Power, J. D., Fair, D. A., Schlaggar, B. L. & Petersen, S. E. The development of human functional brain networks. Neuron 67, 735–748 (2010).CAS  PubMed  PubMed Central  Google Scholar  19.Grayson, D. S. & Fair, D. A. Development of large-scale functional networks from birth to adulthood: a guide to neuroimaging literature. Neuroimage https://doi.org/10.1016/j.neuroimage.2017.01.079 (2017).20.Guerra-Carrillo, B., Mackey, A. P. & Bunge, S. A. Resting-state fMRI: A window into human brain plasticity. Neuroscientist 20, 522–533 (2014).PubMed  Google Scholar  21.Vendetti, M. S. & Bunge, S. A. Evolutionary and developmental changes in the lateral frontoparietal network: A little goes a long way for higher-level cognition. Neuron 84, 906–917 (2014).CAS  PubMed  PubMed Central  Google Scholar  22.Vincent, J. L., Kahn, I., Snyder, A. Z., Raichle, M. E. & Buckner, R. L. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J. Neurophysiol. 100, 3328–3342 (2008).PubMed  PubMed Central  Google Scholar  23.Raichle, M. E. et al. A default mode of brain function. Proc. Natl Acad. Sci. U.S.A. 98, 676–682 (2001).ADS  CAS  PubMed  PubMed Central  Google Scholar  24.Spreng, R. N. The fallacy of a ‘task-negative’ network. Front. Psychol. 3, 1–5 (2012). Google Scholar  25.Satterthwaite, T. D. et al. Functional maturation of the executive system during adolescence. J. Neurosci. 33, 16249–16261 (2013).CAS  PubMed  PubMed Central  Google Scholar  26.Kelly, A. M. C., Uddin, L. Q., Biswal, B. B., Castellanos, F. X. & Milham, M. P. Competition between functional brain networks mediates behavioral variability. Neuroimage 39, 527–537 (2008).PubMed  Google Scholar  27.Weissman, D. H., Roberts, K. C., Visscher, K. M. & Woldorff, M. G. The neural bases of momentary lapses in attention. Nat. Neurosci. 9, 971–978 (2006).CAS  PubMed  Google Scholar  28.Hampson, M., Driesen, N., Roth, J. K., Gore, J. C. & Constable, R. T. Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. Magn. Reson. Imaging 28, 1051–1057 (2010).PubMed  PubMed Central  Google Scholar  29.Barber, A. D., Caffo, B. S., Pekar, J. J. & Mostofsky, S. H. Developmental changes in within- and between-network connectivity between late childhood and adulthood. Neuropsychologia https://doi.org/10.1016/j.neuropsychologia.2012.11.011 (2013).30.Keller, J. B. et al. Resting-state anticorrelations between medial and lateral prefrontal cortex: Association with working memory, aging, and individual differences. Cortex https://doi.org/10.1016/j.cortex.2014.12.001 (2015).31.Simpson, J. R., Snyder, A. Z., Gusnard, D. A. & Raichle, M. E. Emotion-induced changes in human medial prefrontal cortex: I. During cognitive task performance. Proc. Natl Acad. Sci. U.S.A. 98, 683–687 (2001).ADS  CAS  PubMed  PubMed Central  Google Scholar  32.Simpson, J. R., Snyder, A. Z., Gusnard, D. A. & Raichle, M. E. Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. Proc. Natl Acad. Sci. U.S.A. 98, 688–693 (2001).ADS  CAS  PubMed  PubMed Central  Google Scholar  33.Chai, X. J., Ofen, N., Gabrieli, J. D. E. & Whitfield-Gabrieli, S. Selective development of anticorrelated networks in the intrinsic functional organization of the human brain. J. Cogn. Neurosci. https://doi.org/10.1162/jocn_a_00517 (2014).34.Sherman, L. E. et al. Development of the default mode and central executive networks across early adolescence: A longitudinal study. Dev. Cogn. Neurosci. https://doi.org/10.1016/j.dcn.2014.08.002 (2014).35.Whitfield-Gabrieli, S. et al. Association of intrinsic brain architecture with changes in attentional and mood symptoms during development. JAMA Psychiatry. 77, 378–386 (2020).PubMed  Google Scholar  36.Kam, J. W. Y. et al. Default network and frontoparietal control network theta connectivity supports internal attention. Nat. Hum. Behav. 3, 1263–1270 (2019).PubMed  Google Scholar  37.Christoff, K., Gordon, A. M., Smallwood, J., Smith, R. & Schooler, J. W. Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proc. Natl Acad. Sci. U.S.A. 106, 8719–8724 (2009).ADS  CAS  PubMed  PubMed Central  Google Scholar  38.Buckner, R. L. & Carroll, D. C. Self-projection and the brain. Trends Cogn. Sci. https://doi.org/10.1016/j.tics.2006.11.004 (2007).39.Marshall, N. A. et al. Socioeconomic disadvantage and altered corticostriatal circuitry in urban youth. Hum. Brain Mapp. 39, 1982–1994 (2018).PubMed  PubMed Central  Google Scholar  40.Weissman, D. G., Conger, R. D., Robins, R. W., Hastings, P. D. & Guyer, A. E. Income change alters default mode network connectivity for adolescents in poverty. Dev. Cogn. Neurosci. 30, 93–99 (2018).PubMed  PubMed Central  Google Scholar  41.Casey, B. J. et al. The Adolescent Brain Cognitive Development (ABCD) study: Imaging acquisition across 21 sites. Dev. Cogn. Neurosci. 32, 43–54 (2018).CAS  PubMed  PubMed Central  Google Scholar  42.Fox, L. The Supplemental Poverty Measure: 2016. Current Population Reports (2017).43.Noble, K. G. et al. Family income, parental education and brain structure in children and adolescents. Nat. Neurosci. 18, 773 (2015).CAS  PubMed  PubMed Central  Google Scholar  44.Duncan, G. J. & Magnuson, K. Socioeconomic status and cognitive functioning: Moving from correlation to causation. Wiley Interdiscip. Rev. Cogn. Sci. 3, 377–386 (2012).PubMed  Google Scholar  45.Farah, M. J. Socioeconomic status and the brain: Prospects for neuroscience-informed policy. Nat. Rev. Neurosci. 19, 428–438 (2018).CAS  PubMed  Google Scholar  46.Sridharan, D., Levitin, D. J. & Menon, V. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl Acad. Sci. U.S.A. 105, 12569–12574 (2008).ADS  CAS  PubMed  PubMed Central  Google Scholar  47.Menon, V. & Uddin, L. Q. Saliency, switching, attention and control: A network model of insula function. Brain Struct. Funct. 214, 655–667 (2010).PubMed  PubMed Central  Google Scholar  48.Vincent, J. L. et al. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 96, 3517–3531 (2006).PubMed  Google Scholar  49.Ghetti, S. & Bunge, S. A. Neural changes underlying the development of episodic memory during middle childhood. Dev. Cogn. Neurosci. 2, 381–395 (2012).PubMed  PubMed Central  Google Scholar  50.Badre, D. & Wagner, A. D. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia https://doi.org/10.1016/j.neuropsychologia.2007.06.015 (2007).51.Blumenfeld, R. S. & Ranganath, C. Prefrontal cortex and long-term memory encoding: An integrative review of findings from neuropsychology and neuroimaging. Neuroscientist https://doi.org/10.1177/1073858407299290 (2007).52.Andrews-Hanna, J. R., Smallwood, J. & Spreng, R. N. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann. N. Y. Acad. Sci. 1316, 29–52 (2014).ADS  PubMed  PubMed Central  Google Scholar  53.Kaboodvand, N., Bäckman, L., Nyberg, L. & Salami, A. The retrosplenial cortex: A memory gateway between the cortical default mode network and the medial temporal lobe. Hum. Brain Mapp. https://doi.org/10.1002/hbm.23983 (2018).54.Chai, X. J., Ofen, N., Gabrieli, J. D. E. & Whitfield-Gabrieli, S. Development of deactivation of the default-mode network during episodic memory formation. Neuroimage 84, 932–938 (2014).PubMed  Google Scholar  55.Fornito, A., Harrison, B. J., Zalesky, A. & Simons, J. S. Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proc. Natl Acad. Sci. U.S.A. 109, 12788–12793 (2012).ADS  CAS  PubMed  PubMed Central  Google Scholar  56.Prado, J. & Weissman, D. H. Heightened interactions between a key default-mode region and a key task-positive region are linked to suboptimal current performance but to enhanced future performance. Neuroimage 56, 2276–2282 (2011).PubMed  Google Scholar  57.Langeslag, S. J. E. et al. Functional connectivity between parietal and frontal brain regions and intelligence in young children: The Generation R study. Hum. Brain Mapp. 34, 3299–3307 (2013).PubMed  Google Scholar  58.Li, C. & Tian, L. Association between resting-state coactivation in the parieto-frontal network and intelligence during late childhood and adolescence. Am. J. Neuroradiol. 35, 1150–1156 (2014).CAS  PubMed  PubMed Central  Google Scholar  59.Song, M. et al. Brain spontaneous functional connectivity and intelligence. Neuroimage https://doi.org/10.1016/j.neuroimage.2008.02.036 (2008).60.DeJoseph, M. L., Sifre, R. D., Raver, C. C., Blair, C. B. & Berry, D. Capturing dimensions of material deprivation, sociocognitive stimulation, and emotional threat in the context of poverty: A moderated nonlinear factor model in a population-based sample of low-income children measured across infancy through early adolesce. PsyArXiv 21 (2020).61.Simmons, C. et al. Responsible use of open-access developmental data: The adolescent brain cognitive development (ABCD) study. Psychol. Sci. 095679762110035 https://doi.org/10.1177/09567976211003564 (2021).62.Nweze, T., Nwoke, M. B., Nwufo, J. I., Aniekwu, R. I. & Lange, F. Working for the future: Parentally deprived Nigerian children have enhanced working memory ability. J. Child Psychol. Psychiatry Allied Discip. https://doi.org/10.1111/jcpp.13241 (2020).63.Desmond, M. Evicted: Poverty and profit in the American city. (Broadway Books, 2016).64.Kraus, M. W., Onyeador, I. N., Daumeyer, N. M., Rucker, J. M. & Richeson, J. A. The misperception of racial economic inequality. Perspect. Psychol. Sci. https://doi.org/10.1177/1745691619863049 (2019).65.Shedd, C. Unequal city: Race, schools, and perceptions of injustice. (Russell Sage Foundation, 2015).66.Desmond, M. & Kimbro, R. T. Eviction’s fallout: Housing, hardship, and health. Soc. Forces https://doi.org/10.1093/sf/sov044 (2015).67.Alexander, M. The new Jim Crow: Mass incarceration in the age of colorblindness. (The New Press, 2012).68.Chetty, R., Hendren, N., Jones, M. & Porter, S. Race and Economic Opportunity in the United States: An Intergenerational Perspective. Natl. Bur. Econ. Res. Work. Pap. Ser. https://doi.org/10.3386/w24441 (2018).69.Varner, F. A. et al. Racial discrimination experiences and African American youth adjustment: The role of parenting profiles based on racial socialization and involved-vigilant parenting. Cult. Divers. Ethn. Minor. Psychol. 24, 173–186 (2018). Google Scholar  70.Simons, R. L. et al. Discrimination, crime, ethnic identity, and parenting as correlates of depressive symptoms among African American children: A multilevel analysis. Dev. Psychopathol. 14, 371–393 (2002).PubMed  Google Scholar  71.Chen, S. H. et al. Effortful control and early academic achievement of Chinese American children in immigrant families. Early Child. Res. Q. https://doi.org/10.1016/j.ecresq.2014.08.004 (2015).72.Costigan, C. L., Koryzma, C. M., Hua, J. M. & Chance, L. J. Ethnic Identity, Achievement, and Psychological Adjustment: Examining Risk and Resilience Among Youth From Immigrant Chinese Families in Canada. Cult. Divers. Ethn. Minor. Psychol. https://doi.org/10.1037/a0017275 (2010).73.Cardoso, J. B. & Thompson, S. J. Common themes of resilience among latino immigrant families: A systematic review of the literature. Fam. Soc. https://doi.org/10.160
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