Abstract
Preterm birth (PTB) is associated with increased risk for unfavorable outcomes such as deficits in attentional control and related brain structure alterations. Crucially, PTB is more likely to occur within the context of poverty. The current study examined associations between PTB and inhibitory control (IC) implicated brain regions/tracts and task performance, as well as the moderating role of early life poverty on the relation between PTB and IC-implicated regions/tracts/task performance. 2,899 children from the ABCD study were sampled for this study. Mixed effects models examined the relation between PTB and subsequent IC performance as well as prefrontal gray matter volume, white matter fractional anisotropy (FA), and mean diffusivity (MD). Household income was examined as a moderator. PTB was significantly associated with less improvement in IC task performance over time and decreased FA in left uncinate fasciculus (UF) and cingulum bundle (CB). Early life poverty moderated the relation between PTB and both CB FA and UF MD.
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Data availability
Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive DevelopmentSM (ABCD) Study (https://abcdstudy.org), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and additional federal partners under award numbers U01DA041048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortium_members/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators.
References
Aarnoudse-Moens CSH, Duivenvoorden HJ, Weisglas-Kuperus N, Van Goudoever JB, Oosterlaan J (2012) The profile of executive function in very preterm children at 4 to 12 years: Executive Function in Very Preterm Children. Dev Med Child Neurol 54(3):247–253. https://doi.org/10.1111/j.1469-8749.2011.04150.x
Adrian JA, Bakeman R, Akshoomoff N, Haist F (2020) Cognitive functions mediate the effect of preterm birth on mathematics skills in young children. Child Neuropsychol 26(6):834–856. https://doi.org/10.1080/09297049.2020.1761313
Barfield WD (2018) Public Health Implications of Very Preterm Birth. Clin Perinatol 45(3):565–577. https://doi.org/10.1016/j.clp.2018.05.007
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2014). Fitting Linear Mixed-Effects Models using lme4. https://doi.org/10.48550/ARXIV.1406.5823
Beauregard JL, Drews-Botsch C, Sales JM, Flanders WD, Kramer MR (2018) Does socioeconomic status modify the association between preterm birth and children’s early cognitive ability and kindergarten academic achievement in the United States? Am J Epidemiol 187(8):1704–1713. https://doi.org/10.1093/aje/kwy068
Benavente-Fernández I, Synnes A, Grunau RE, Chau V, Ramraj C, Glass T, Cayam-Rand D, Siddiqi A, Miller SP (2019) Association of socioeconomic status and brain injury with neurodevelopmental outcomes of very preterm children. JAMA Netw Open 2(5):e192914. https://doi.org/10.1001/jamanetworkopen.2019.2914
Brenner RG, Smyser CD, Lean RE, Kenley JK, Smyser TA, Cyr PEP, Shimony JS, Barch DM, Rogers CE (2021) Microstructure of the dorsal anterior cingulum bundle in very preterm neonates predicts the preterm behavioral phenotype at 5 years of age. Biol Psychiat 89(5):433–442. https://doi.org/10.1016/j.biopsych.2020.06.015
Brumbaugh J, Hodel A, Thomas K (2013) The impact of late preterm birth on executive function at preschool age. Am J Perinatol 31(04):305–314. https://doi.org/10.1055/s-0033-1348950
Brumberg HL, Shah SI (2015) Born early and born poor: An eco-bio-developmental model for poverty and preterm birth. Journal of Neonatal-Perinatal Medicine 8(3):179–187. https://doi.org/10.3233/NPM-15814098
Burnett AC, Scratch SE, Anderson PJ (2013) Executive function outcome in preterm adolescents. Early Human Dev 89(4):215–220. https://doi.org/10.1016/j.earlhumdev.2013.01.013
Cascio CN, Lauharatanahirun N, Lawson GM, Farah MJ, Falk EB (2022) Parental education is associated with differential engagement of neural pathways during inhibitory control. Sci Rep 12(1):260. https://doi.org/10.1038/s41598-021-04152-4
Casey BJ, Getz S, Galvan A (2008) The adolescent brain. Dev Rev 28(1):62–77. https://doi.org/10.1016/j.dr.2007.08.003
Chevrier AD, Noseworthy MD, Schachar R (2007) Dissociation of response inhibition and performance monitoring in the stop signal task using event-related fMRI. Hum Brain Mapp 28(12):1347–1358. https://doi.org/10.1002/hbm.20355
Constable RT, Ment LR, Vohr BR, Kesler SR, Fulbright RK, Lacadie C, Delancy S, Katz KH, Schneider KC, Schafer RJ, Makuch RW, Reiss AR (2008) Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: an investigation of group and gender effects. Pediatrics 121(2):306–316. https://doi.org/10.1542/peds.2007-0414
Counsell SJ, Boardman JP (2005) Differential brain growth in the infant born preterm: Current knowledge and future developments from brain imaging. Semin Fetal Neonatal Med 10(5):403–410. https://doi.org/10.1016/j.siny.2005.05.003
Daamen M, Bäuml JG, Scheef L, Sorg C, Busch B, Baumann N, Bartmann P, Wolke D, Wohlschläger A, Boecker H (2015) Working memory in preterm-born adults: Load-dependent compensatory activity of the posterior default mode network: Working Memory in Preterm-Born Adults. Hum Brain Mapp 36(3):1121–1137. https://doi.org/10.1002/hbm.22691
De Kieviet JF, Zoetebier L, van Elburg RM, Vermeulen RJ, Oosterlaan J (2012) Brain development of very preterm and very low-birthweight children in childhood and adolescence: a meta-analysis: review. Develop Med Child Neurol 54(4):313–323. https://doi.org/10.1111/j.1469-8749.2011.04216.x
Deater-Deckard K, Li M, Lee J, King-Casas B, Kim-Spoon J (2019) Poverty and puberty: a neurocognitive study of inhibitory control in the transition to adolescence. Psychol Sci 30(11):1573–1583. https://doi.org/10.1177/0956797619863780
DeFranco EA, Lian M, Muglia LJ, Schootman M (2008) Area-level poverty and preterm birth risk: A population-based multilevel analysis. BMC Public Health 8(1):316. https://doi.org/10.1186/1471-2458-8-316
Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53(1):1–15. https://doi.org/10.1016/j.neuroimage.2010.06.010
Durston S, Thomas KM, Yang Y, Ulug AM, Zimmerman RD, Casey BJ (2002) A neural basis for the development of inhibitory control. Dev Sci 5(4):F9–F16. https://doi.org/10.1111/1467-7687.00235
Friedman NP, Robbins TW (2022) The role of prefrontal cortex in cognitive control and executive function. Neuropsychopharmacology 47(1):72–89. https://doi.org/10.1038/s41386-021-01132-0
Garavan H, Hester R, Murphy K, Fassbender C, Kelly C (2006) Individual differences in the functional neuroanatomy of inhibitory control. Brain Res 1105(1):130–142. https://doi.org/10.1016/j.brainres.2006.03.029
Garavan H, Ross TJ, Stein EA (1999) Right hemispheric dominance of inhibitory control: An event-related functional MRI study. Proc Natl Acad Sci 96(14):8301–8306. https://doi.org/10.1073/pnas.96.14.8301
Gershon RC, Cook KF, Mungas D, Manly JJ, Slotkin J, Beaumont JL, Weintraub S (2014) Language measures of the NIH toolbox cognition battery. J Int Neuropsychol Soc 20(6):642–651. https://doi.org/10.1017/S1355617714000411
Giedd JN (2004) Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 1021(1):77–85. https://doi.org/10.1196/annals.1308.009
Giménez M, Junqué C, Narberhaus A, Bargalló N, Botet F, Mercader JM (2006) White matter volume and concentration reductions in adolescents with history of very preterm birth: A voxel-based morphometry study. Neuroimage 32(4):1485–1498. https://doi.org/10.1016/j.neuroimage.2006.05.013
Goyal NK, Fiks AG, Lorch SA (2011) association of late-preterm birth with asthma in young children: practice-based study. Pediatrics 128(4):e830–e838. https://doi.org/10.1542/peds.2011-0809
Gruner P, Vo A, Ikuta T, Mahon K, Peters BD, Malhotra AK, Uluğ AM, Szeszko PR (2012) White matter abnormalities in pediatric obsessive-compulsive disorder. Neuropsychopharmacology 37(12):2730–2739. https://doi.org/10.1038/npp.2012.138
Hagler DJ, Ahmadi ME, Kuperman J, Holland D, McDonald CR, Halgren E, Dale AM (2009) Automated white-matter tractography using a probabilistic diffusion tensor atlas: Application to temporal lobe epilepsy. Hum Brain Mapp 30(5):1535–1547. https://doi.org/10.1002/hbm.20619
Hagler DJ, Hatton SeanN, Cornejo MD, Makowski C, Fair DA, Dick AS, Sutherland MT, Casey BJ, Barch DM, Harms MP, Watts R, Bjork JM, Garavan HP, Hilmer L, Pung CJ, Sicat CS, Kuperman J, Bartsch H, Xue F, Dale AM (2019) Image processing and analysis methods for the adolescent brain cognitive development study. Neuroimage 202:116091. https://doi.org/10.1016/j.neuroimage.2019.116091
Hair NL, Hanson JL, Wolfe BL, Pollak SD (2015) Association of child poverty, brain development, and academic achievement. JAMA Pediatr 169(9):822. https://doi.org/10.1001/jamapediatrics.2015.1475
Heeringa SG, Berglund PA (2020) A guide for population-based analysis of the adolescent brain cognitive development (ABCD) study baseline data [Preprint]. Neuroscience. https://doi.org/10.1101/2020.02.10.942011
Jaekel J, Eryigit-Madzwamuse S, Wolke D (2016) Preterm toddlers’ inhibitory control abilities predict attention regulation and academic achievement at age 8 years. J Pediatr 169:87-92.e1. https://doi.org/10.1016/j.jpeds.2015.10.029
Janssen T, Larsen H, Peeters M, Boendermaker WJ, Vollebergh WAM, Wiers RW (2015) Do online assessed self-report and behavioral measures of impulsivity-related constructs predict onset of substance use in adolescents? Addictive Behaviors Reports 1:12–18. https://doi.org/10.1016/j.abrep.2015.01.002
Johnson S (2007) Cognitive and behavioural outcomes following very preterm birth. Semin Fetal Neonatal Med 12(5):363–373. https://doi.org/10.1016/j.siny.2007.05.004
Johnson S, Evans TA, Draper ES, Field DJ, Manktelow BN, Marlow N, Matthews R, Petrou S, Seaton SE, Smith LK, Boyle EM (2015) Neurodevelopmental outcomes following late and moderate prematurity: A population-based cohort study. Arch Dis Childhood 100(4):F301–F308. https://doi.org/10.1136/archdischild-2014-307684
Johnson S, Marlow N (2011) Preterm birth and childhood psychiatric disorders. Pediatr Res. https://doi.org/10.1203/PDR.0b013e318212faa0
Jongbloed-Pereboom M, Janssen AJWM, Steenbergen B, Nijhuis-van der Sanden MWG (2012) Motor learning and working memory in children born preterm: A systematic review. Neurosci Biobehav Rev 36(4):1314–1330. https://doi.org/10.1016/j.neubiorev.2012.02.005
Koini M, Rombouts SARB, Veer IM, Van Buchem MA, Huijbregts SCJ (2017) White matter microstructure of patients with neurofibromatosis type 1 and its relation to inhibitory control. Brain Imaging Behav 11(6):1731–1740. https://doi.org/10.1007/s11682-016-9641-3
Kramer MS, Goulet L, Lydon J, Seguin L, McNamara H, Dassa C, Platt RW, Fong Chen M, Gauthier H, Genest J, Kahn S, Libman M, Rozen R, Masse A, Miner L, Asselin G, Benjamin A, Klein J, Koren G (2001) Socio-economic disparities in preterm birth: Causal pathways and mechanisms. Paediatr Perinat Epidemiol 15(s2):104–123. https://doi.org/10.1046/j.1365-3016.2001.00012.x
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw. https://doi.org/10.18637/jss.v082.i13
Latendresse G (2009) The interaction between chronic stress and pregnancy: preterm birth from a biobehavioral perspective. J Midwifery Women Health 54(1):8–17. https://doi.org/10.1016/j.jmwh.2008.08.001
Lautarescu A, Pecheva D, Nosarti C, Nihouarn J, Zhang H, Victor S, Craig M, Edwards AD, Counsell SJ (2020) Maternal prenatal stress is associated with altered uncinate fasciculus microstructure in premature neonates. Biol Psychiat 87(6):559–569. https://doi.org/10.1016/j.biopsych.2019.08.010
Lemola S, Oser N, Urfer-Maurer N, Brand S, Holsboer-Trachsler E, Bechtel N, Grob A, Weber P, Datta AN (2017) Effects of gestational age on brain volume and cognitive functions in generally healthy very preterm born children during school-age: A voxel-based morphometry study. PLoS ONE 12(8):e0183519. https://doi.org/10.1371/journal.pone.0183519
Luo Z-C (2006) Effect of neighbourhood income and maternal education on birth outcomes: A population-based study. Can Med Assoc J 174(10):1415–1420. https://doi.org/10.1503/cmaj.051096
Luu TM, Ment LR, Schneider KC, Katz KH, Allan WC, Vohr BR (2009) Lasting effects of preterm birth and neonatal brain hemorrhage at 12 years of age. Pediatrics 123(3):1037–1044. https://doi.org/10.1542/peds.2008-1162
Marlow N, Hennessy EM, Bracewell MA, Wolke D, for the EPICure Study Group (2007) Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics 120(4):793–804. https://doi.org/10.1542/peds.2007-0440
Melville JM, Moss TJM (2013) The immune consequences of preterm birth. Front Neurosci. https://doi.org/10.3389/fnins.2013.00079
Ment LR, Vohr BR (2008) Preterm birth and the developing brain. Lancet Neurol 7(5):378–379. https://doi.org/10.1016/S1474-4422(08)70073-5
Messer LC, Vinikoor LC, Laraia BA, Kaufman JS, Eyster J, Holzman C, Culhane J, Elo I, Burke JG, O’Campo P (2008) Socioeconomic domains and associations with preterm birth. Soc Sci Med 67(8):1247–1257. https://doi.org/10.1016/j.socscimed.2008.06.009
Montagna A, Nosarti C (2016) Socio-emotional development following very preterm birth: pathways to psychopathology. Front Psychol. https://doi.org/10.3389/fpsyg.2016.00080
Mueller SC, Maheu FS, Dozier M, Peloso E, Mandell D, Leibenluft E, Pine DS, Ernst M (2010) Early-life stress is associated with impairment in cognitive control in adolescence: An fMRI study. Neuropsychologia 48(10):3037–3044. https://doi.org/10.1016/j.neuropsychologia.2010.06.013
Mullen KM, Vohr BR, Katz KH, Schneider KC, Lacadie C, Hampson M, Makuch RW, Reiss AL, Constable RT, Ment LR (2011) Preterm birth results in alterations in neural connectivity at age 16 years. Neuroimage 54(4):2563–2570. https://doi.org/10.1016/j.neuroimage.2010.11.019
Mürner-Lavanchy I, Ritter BC, Spencer-Smith MM, Perrig WJ, Schroth G, Steinlin M, Everts R (2014) Visuospatial working memory in very preterm and term born children—Impact of age and performance. Dev Cogn Neurosci 9:106–116. https://doi.org/10.1016/j.dcn.2014.02.004
Nkansah-Amankra S, Luchok KJ, Hussey JR, Watkins K, Liu X (2010) Effects of maternal stress on low birth weight and preterm birth outcomes across neighborhoods of South Carolina, 2000–2003. Matern Child Health J 14(2):215–226. https://doi.org/10.1007/s10995-009-0447-4
Noble KG, Houston SM, Brito NH, Bartsch H, Kan E, Kuperman JM, Akshoomoff N, Amaral DG, Bloss CS, Libiger O, Schork NJ, Murray SS, Casey BJ, Chang L, Ernst TM, Frazier JA, Gruen JR, Kennedy DN, Van Zijl P, Sowell ER (2015) Family income, parental education and brain structure in children and adolescents. Nat Neurosci 18(5):773–778. https://doi.org/10.1038/nn.3983
Noble KG, Korgaonkar MS, Grieve SM, Brickman AM (2013) Higher education is an age-independent predictor of white matter integrity and cognitive control in late adolescence. Dev Sci 16(5):653–664. https://doi.org/10.1111/desc.12077
Peterson BS (2000) Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 284(15):1939. https://doi.org/10.1001/jama.284.15.1939
Platt MJ (2014) Outcomes in preterm infants. Public Health 128(5):399–403. https://doi.org/10.1016/j.puhe.2014.03.010
Ponce NA, Hoggatt KJ, Wilhelm M, Ritz B (2005) Preterm birth: the interaction of traffic-related air pollution with economic hardship in los angeles neighborhoods. Am J Epidemiol 162(2):140–148. https://doi.org/10.1093/aje/kwi173
Porter TR, Kent ST, Su W, Beck HM, Gohlke JM (2014) Spatiotemporal association between birth outcomes and coke production and steel making facilities in Alabama, USA: A cross-sectional study. Environ Health 13(1):85. https://doi.org/10.1186/1476-069X-13-85
Rogers CE, Lean RE, Wheelock MD, Smyser CD (2018) Aberrant structural and functional connectivity and neurodevelopmental impairment in preterm children. J Neurodev Disord 10(1):38. https://doi.org/10.1186/s11689-018-9253-x
Rose SA, Feldman JF, Jankowski JJ (2011) Modeling a cascade of effects: The role of speed and executive functioning in preterm/full-term differences in academic achievement: Executive function in preterm adolescents. Dev Sci 14(5):1161–1175. https://doi.org/10.1111/j.1467-7687.2011.01068.x
Silva MJ, Barr DB, Reidy JA, Malek NA, Hodge CC, Caudill SP, Brock JW, Needham LL, Calafat AM (2004) Urinary levels of seven phthalate metabolites in the US population from the National Health and Nutrition Examination Survey (NHANES) 1999–2000. Environ Health Perspect 112(3):331–338. https://doi.org/10.1289/ehp.6723
Smith LK, Draper ES, Manktelow BN, Dorling JS, Field DJ (2007) Socioeconomic inequalities in very preterm birth rates. Arch Dis Childhood 92(1):F11–F14. https://doi.org/10.1136/adc.2005.090308
Spielberg JM, Galarce EM, Ladouceur CD, McMakin DL, Olino TM, Forbes EE, Silk JS, Ryan ND, Dahl RE (2015) Adolescent development of inhibition as a function of SES and gender: Converging evidence from behavior and fMRI: SES and inhibition development in adolescence. Hum Brain Mapp 36(8):3194–3203. https://doi.org/10.1002/hbm.22838
Strahle JM, Triplett RL, Alexopoulos D, Smyser TA, Rogers CE, Limbrick DD, Smyser CD (2019) Impaired hippocampal development and outcomes in very preterm infants with perinatal brain injury. Neuroimage 22:101787. https://doi.org/10.1016/j.nicl.2019.101787
Tanya Nagahawatte N, Goldenberg RL (2008) Poverty, maternal health, and adverse pregnancy outcomes. Ann N Y Acad Sci 1136(1):80–85. https://doi.org/10.1196/annals.1425.016
Utendale WT, Hastings PD (2011) Developmental changes in the relations between inhibitory control and externalizing problems during early childhood. Infant Child Dev 20(2):181–193. https://doi.org/10.1002/icd.691
Wong HS, Edwards P (2013) Nature or nurture: a systematic review of the effect of socio-economic status on the developmental and cognitive outcomes of children born preterm. Matern Child Health J 17(9):1689–1700. https://doi.org/10.1007/s10995-012-1183-8
Yuan W, Duffner AM, Chen L, Hunt LP, Sellers SM, Bernal AL (2010) Analysis of preterm deliveries below 35 weeks’ gestation in a tertiary referral hospital in the UK A case-control survey. BMC Res Notes 3(1):119. https://doi.org/10.1186/1756-0500-3-119
Zelazo, P. D., Carlson, S. M., & Kesek, A. (2008). The development of executive function in childhood. In C. A. Nelson & M. Luciana (Eds.). Handbook of Developmental Cognitive Neuroscience, 553–574.
Acknowledgements
The authors would like to thank all of the ABCD Study participants and their families, as well as the members of the ABCD Study research teams across for their dedication and hard work.
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R. L. Taylor is funded by the National Science Foundation (Grant #s DGE-1745038 and DGE-2139839). C. E. Rogers, C. D. Smyser, and D. M. Barch are funded by the National Institutes of Health (Grant #s GR0026407 and U01 DA041120).
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RL Taylor generated hypotheses, conducted the analyses, wrote the main manuscript, and prepared tables and figures. DMB provided guidance in conducting statistical analyses. CER, CDS, and DMB thoroughly reviewed initial hypotheses and written manuscript and offered suggestions for edits.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Ethics Committee of Washington University in St. Louis (201708123).
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Taylor, R.L., Rogers, C.E., Smyser, C.D. et al. Associations Between Preterm Birth, Inhibitory Control-Implicated Brain Regions and Tracts, and Inhibitory Control Task Performance in Children: Consideration of Socioeconomic Context. Child Psychiatry Hum Dev (2023). https://doi.org/10.1007/s10578-023-01531-y
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DOI: https://doi.org/10.1007/s10578-023-01531-y