Early child stimulation and attention-related executive functions at 11 years: 2004 Pelotas birth cohort study

  • Alicia Matijasevich
  • Rebecca M. Pearson
  • Christian Loret de Mola
  • Jessica Mayumi MaruyamaEmail author
  • Carolina La Maison
  • Tiago N. Munhoz
  • Fernando C. Barros
  • Iná S. Santos
  • Aluísio J. D Barros
Original Contribution


The study aimed to explore associations between socioeconomic position (SEP) indicators, early child stimulation (ECS) and attention-related executive functions (EF) at age 11. Children born in Pelotas, Brazil, in 2004, were recruited to a birth cohort (n = 4231, non-response rate at recruitment < 1%) and followed from birth to age 11. SEP variables were family income and maternal schooling. At the 24 and 48-month follow-ups, five markers of cognitive stimulation and social interaction were recorded and positive answers were summed to a score ranging from 0 to 5. At age 11, attentional-switching and control, and selective-attention were assessed using the adapted Test-of-Everyday-Attention-for-Children (TEA-Ch). We used multivariable logistic regression models and mediation analysis to investigate potential mediator role of ECS in the association between SEP and EF. 3106 children were included in the analyses. Less than 7% of the more stimulated individuals showed low performance in attention-related EFs at age 11 compared with almost 20% in the bottom groups of stimulation. Higher child stimulation scores were associated with fewer impairments in attentional-control (OR adj 0.84; CI 95% 0.72–0.98) and attentional-switching (OR adj 0.85; CI 95% 0.73–0.99). Mediation analysis suggested that for attentional-switching, ECS mediated almost 20% of the total protective effect of maternal schooling for impaired EF. Assuming causal relationships, if maximum stimulation was provided to all children, the advantageous effect of maternal schooling on EF would be reduced by 47%. ECS may represent a protective factor for cognitive impairments in childhood and can be easily implemented at relatively low cost.


Cohort Cognitive impairments Stimulation Early adolescence Mediation analysis 



The authors would like to thank the participating families and staff who collaborated in the various stages of the 2004 Pelotas Birth Cohort study.

Author contributions

AM, RMP, CLM and AJDB participated in the design of the study, undertook the analysis, interpreted the results and drafted the first version of the article. JMM, CLM, TNM, ISS and FCB collaborated in the interpretation of the findings and writing of the article. All authors approved the final version of the manuscript submitted.


This article was conducted with data from the Pelotas (Brazil) birth cohort study, conducted by the Postgraduate Program in Epidemiology of the Federal University of Pelotas, with the support of the Brazilian Association of Public Health (Abrasco). Previous phases of the study were funded by the World Health Organization, Program of Support to Nucleus of Excellence (PRONEX), Brazilian National Research Council (CNPq), Ministry of Health and Pastoral of the Child. The mental health component in the 11-year follow-up was funded by the São Paulo Research Foundation (FAPESP; Grant number 2014/13864-6). The present analyses were funded by the CNPq (Grant no. 426024/2016-8).AM, FCB, ISS and AJDB are supported by the CNPq. JM is supported by São Paulo Research Foundation (FAPESP; Grant number 2017/22723-5).

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Supplementary material

787_2019_1440_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 kb)


  1. 1.
    Bailey CE (2007) Cognitive accuracy and intelligent executive function in the brain and in business. Ann N Y Acad Sci 1118:122–141PubMedCrossRefGoogle Scholar
  2. 2.
    Baker-Henningham H, Bóo LF (2010) Early childhood stimulation interventions in developing countries: a comprehensive literature review. IZA Discussion Paper No. 5282. Accessed 10 Oct 2019
  3. 3.
    Barros AJ, Matijasevich A, Santos IS, Halpern R (2010) Child development in a birth cohort: effect of child stimulation is stronger in less educated mothers. Int J Epidemiol 39:285–294PubMedCrossRefGoogle Scholar
  4. 4.
    Ben-Shlomo Y, Kuh D (2002) A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int J Epidemiol 31:285–293PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Best JR, Miller PH (2010) A developmental perspective on executive function. Child Dev 81:1641–1660PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Blair C, Granger DA, Willoughby M, Mills-Koonce R, Cox M, Greenberg MT, Kivlighan KT, Fortunato CK, Investigators FLP (2011) Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood. Child Dev 82:1970–1984PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Brito NH, Noble KG (2014) Socioeconomic status and structural brain development. Front Neurosci 8:276PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Brown TE, Landgraf JM (2010) Improvements in executive function correlate with enhanced performance and functioning and health-related quality of life: evidence from 2 large, double-blind, randomized, placebo-controlled trials in ADHD. Postgrad Med 122:42–51PubMedCrossRefGoogle Scholar
  9. 9.
    Campbell FA, Wasik BH, Pungello E, Burchinal M, Barbarin O, Kainz K, Sparling JJ, Ramey CT (2008) Young adult outcomes of the Abecedarian and CARE early childhood educational interventions. Early Child Res Q 23:452–466CrossRefGoogle Scholar
  10. 10.
    Center on the Developing Child at Harvard University (2011) Building the Brain´s “Air Traffic Control" System: How Early Experiences Shape the Development of Executive Function: Working Paper Nº 11. Accessed 10 June 2019
  11. 11.
    Center on the Developing Child at Harvard University (2007) A science-based framework for ealy childhood policy: using evidence to improve outcomes in learning, behavior, and health for vulnerable children. Accessed 10 June 2019
  12. 12.
    Conger KJ, Rueter MA, Conger RD (2000) The role of economic pressure in the lives of parents and their adolescents: the family stress model. In: Crockett LJ, Silbereisen K (eds) Negotiating adolescence in times of social change. Cambridge University Press, New YorkGoogle Scholar
  13. 13.
    Crosnoe R, Leventhal T, Wirth RJ, Pierce KM, Pianta RC, Network NECCR (2010) Family socioeconomic status and consistent environmental stimulation in early childhood. Child Dev 81:972–987PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Daniel RM, De Stavola BL, Cousens SN (2011) gformula: estimating causal effects in the presence of time-varying confounding or mediation using the g-computation formula. Stata J. 11:479–517CrossRefGoogle Scholar
  15. 15.
    DePrince AP, Weinzierl KM, Combs MD (2009) Executive function performance and trauma exposure in a community sample of children. Child Abuse Negl 33:353–361PubMedCrossRefGoogle Scholar
  16. 16.
    Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Diamond A, Lee K (2011) Interventions shown to aid executive function development in children 4 to 12 years old. Science 333:959–964PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Drevets WC, Raichle ME (1998) Suppression of regional cerebral blood during emotional versus higher cognitive implications for interactions between emotion and cognition. Cogn Emot 12:353–385CrossRefGoogle Scholar
  19. 19.
    Dubowitz LM, Dubowitz V, Goldberg C, Keith I (1976) Rapid assessment of gestational age at birth. Arch Dis Child 51:986–987PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Eakin L, Minde K, Hechtman L, Ochs E, Krane E, Bouffard R, Greenfield B, Looper K (2004) The marital and family functioning of adults with ADHD and their spouses. J Atten Disord 8:1–10PubMedCrossRefGoogle Scholar
  21. 21.
    Ersche KD, Clark L, London M, Robbins TW, Sahakian BJ (2006) Profile of executive and memory function associated with amphetamine and opiate dependence. Neuropsychopharmacology 31:1036–1047PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Factor-Litvak P (2013) Impact of early environmental exposures on mental disorders across the life course. In: Koenen KC, Rudenstine S, Susser E, Galea S (eds) A life course approach to mental disorders. Oxford University Press, OxfordGoogle Scholar
  23. 23.
    Garcia-Madruga JA, Gomez-Veiga I, Vila JO (2016) Executive functions and the improvement of thinking abilities: the intervention in reading comprehension. Front Psychol 7:58PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Garon N, Bryson SE, Smith IM (2008) Executive function in preschoolers: a review using an integrative framework. Psychol Bull 134:31–60PubMedCrossRefGoogle Scholar
  25. 25.
    Gertler P, Heckman J, Pinto R, Zanolini A, Vermeersch C, Walker S, Chang SM, Grantham-McGregor S (2014) Labor market returns to an early childhood stimulation intervention in Jamaica. Science 344:998–1001PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Hackman DA, Gallop R, Evans GW, Farah MJ (2015) Socioeconomic status and executive function: developmental trajectories and mediation. Dev Sci 18:686–702PubMedCrossRefGoogle Scholar
  27. 27.
    Haft SL, Hoeft F (2017) Poverty’s impact on children’s executive functions: global considerations. New Dir Child Adolesc Dev. PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Heckman JJ (2006) Skill formation and the economics of investing in disadvantaged children. Science 312:1900–1902PubMedCrossRefGoogle Scholar
  29. 29.
    Hoaken PN, Allaby DB, Earle J (2007) Executive cognitive functioning and the recognition of facial expressions of emotion in incarcerated violent offenders, non-violent offenders, and controls. Aggress Behav 33:412–421PubMedCrossRefGoogle Scholar
  30. 30.
    Hostinar CE, Stellern SA, Schaefer C, Carlson SM, Gunnar MR (2012) Associations between early life adversity and executive function in children adopted internationally from orphanages. Proc Natl Acad Sci USA 109(Suppl 2):17208–17212PubMedCrossRefGoogle Scholar
  31. 31.
    Huizinga M, Dolan CV, van der Molen MW (2006) Age-related change in executive function: developmental trends and a latent variable analysis. Neuropsychologia 44:2017–2036PubMedCrossRefGoogle Scholar
  32. 32.
    Karbach J, Kray J (2009) How useful is executive control training? Age differences in near and far transfer of task-switching training. Dev Sci 12:978–990PubMedCrossRefGoogle Scholar
  33. 33.
    Klingberg T (2010) Training and plasticity of working memory. Trends Cogn Sci 14:317–324PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Kolb B, Gibb R (2011) Brain plasticity and behaviour in the developing brain. J Can Acad Child Adolesc Psychiatry 20:265–276PubMedPubMedCentralGoogle Scholar
  35. 35.
    Lee V, Hoaken PN (2007) Cognition, emotion, and neurobiological development: mediating the relation between maltreatment and aggression. Child Maltreat 12:281–298PubMedCrossRefGoogle Scholar
  36. 36.
    Lengua LJ, Honorado E, Bush NR (2007) Contextual risk and parenting as predictors of effortful control and social competence in preschool children. J Appl Dev Psychol 28:40–55PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662PubMedCrossRefGoogle Scholar
  38. 38.
    Lovic V, Fleming AS (2004) Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task–reversal of effects with maternal-like licking stimulation. Behav Brain Res 148:209–219PubMedCrossRefGoogle Scholar
  39. 39.
    Lugo-Gil J, Tamis-LeMonda CS (2008) Family resources and parenting quality: links to children’s cognitive development across the first 3 years. Child Dev 79:1065–1085PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Maldonado G, Greenland S (1993) Simulation study of confounder-selection strategies. Am J Epidemiol 138:923–936PubMedCrossRefGoogle Scholar
  41. 41.
    Manly T, Anderson V, Nimmo-Smith I, Turner A, Watson P, Robertson IH (2001) The differential assessment of children’s attention: the Test of Everyday Attention for Children (TEA-Ch), normative sample and ADHD performance. J Child Psychol Psychiatry 42:1065–1081PubMedCrossRefGoogle Scholar
  42. 42.
    Maughan A, Cicchetti D (2002) Impact of child maltreatment and interadult violence on children’s emotion regulation abilities and socioemotional adjustment. Child Dev 73:1525–1542PubMedCrossRefGoogle Scholar
  43. 43.
    Miller HV, Barnes JC, Beaver KM (2011) Self-control and health outcomes in a nationally representative sample. Am J Health Behav 35:15–27PubMedCrossRefGoogle Scholar
  44. 44.
    Pechtel P, Pizzagalli DA (2011) Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 214:55–70PubMedCrossRefGoogle Scholar
  45. 45.
    Repetti RL, Taylor SE, Seeman TE (2002) Risky families: family social environments and the mental and physical health of offspring. Psychol Bull 128:330–366PubMedCrossRefGoogle Scholar
  46. 46.
    Riggs NR, Spruijt-Metz D, Sakuma KL, Chou CP, Pentz MA (2010) Executive cognitive function and food intake in children. J Nutr Educ Behav 42:398–403PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Robertson IH, Ward T, Ridgeway V, Nimmo-Smith I (1996) The structure of normal human attention: the test of everyday attention. J Int Neuropsychol Soc 2:525–534PubMedCrossRefGoogle Scholar
  48. 48.
    Rothman KJ, Greenland S (1998) Precision and validity in epidemiologic studies. In: Rothman KJ, Greenland S (eds) Modern epidemiology. Lippincott-Raven, Philadelphia, pp 115–134Google Scholar
  49. 49.
    Rueda MR, Posner MI, Rothbart MK (2005) The development of executive attention: contributions to the emergence of self-regulation. Dev Neuropsychol 28:573–594PubMedCrossRefGoogle Scholar
  50. 50.
    Santos IS, Barros AJ, Matijasevich A, Domingues MR, Barros FC, Victora CG (2011) Cohort profile: the 2004 Pelotas (Brazil) birth cohort study. Int J Epidemiol 40:1461–1468PubMedCrossRefGoogle Scholar
  51. 51.
    Santos IS, Barros AJ, Matijasevich A, Zanini R, Chrestani Cesar MA, Camargo-Figuera FA, Oliveira IO, Barros FC, Victora CG (2014) Cohort profile update: 2004 Pelotas (Brazil) Birth Cohort Study. Body composition, mental health and genetic assessment at the 6 years follow-up. Int J Epidemiol 43:1437PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Shonkoff JP (2011) Protecting brains, not simply stimulating minds. Science 333:982–983PubMedCrossRefGoogle Scholar
  53. 53.
    Tucker-Drob EM, Harden KP (2012) Early childhood cognitive development and parental cognitive stimulation: evidence for reciprocal gene-environment transactions. Dev Sci 15:250–259PubMedCrossRefGoogle Scholar
  54. 54.
    Ursache A, Noble KG, Pediatric Imaging N, Genetics S (2016) Socioeconomic status, white matter, and executive function in children. Brain Behav 6:e00531PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Victora CG, Barreto ML, do Carmo ML, Monteiro CA, Schmidt MI, Paim J, Bastos FI, Almeida C, Bahia L, Travassos C, Reichenheim M, Barros FC, Lancet Brazil Series Working G (2011) Health conditions and health-policy innovations in Brazil: the way forward. Lancet 377:2042–2053PubMedCrossRefGoogle Scholar
  56. 56.
    Wass SV, Scerif G, Johnson MH (2012) Training attentional control and working memory—is younger, better? Dev Rev 32:360–387CrossRefGoogle Scholar
  57. 57.
    Will Crescioni A, Ehrlinger J, Alquist JL, Conlon KE, Baumeister RF, Schatschneider C, Dutton GR (2011) High trait self-control predicts positive health behaviors and success in weight loss. J Health Psychol 16:750–759PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Zelazo PD (2004) The development of conscious control in childhood. Trends Cogn Sci 8:12–17PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Alicia Matijasevich
    • 1
    • 2
  • Rebecca M. Pearson
    • 3
    • 4
  • Christian Loret de Mola
    • 2
  • Jessica Mayumi Maruyama
    • 1
    Email author
  • Carolina La Maison
    • 1
  • Tiago N. Munhoz
    • 2
  • Fernando C. Barros
    • 2
    • 5
  • Iná S. Santos
    • 2
    • 6
  • Aluísio J. D Barros
    • 2
  1. 1.Departamento de Medicina Preventiva, Faculdade de Medicina FMUSPUniversidade de São PauloSão PauloBrazil
  2. 2.Post-Graduate Program in EpidemiologyFederal University of PelotasPelotasBrazil
  3. 3.Centre for Academic Mental Health, School of Social and Community MedicineUniversity of BristolBristolUK
  4. 4.Section of Child and Adolescent Psychiatry, Department of PsychiatryUniversity of OxfordOxfordUK
  5. 5.Post-Graduate Program in Health and BehaviourCatholic University of PelotasPelotasBrazil
  6. 6.Postgraduate Program in Pediatrics and Child Health, School of MedicinePontifical Catholic University of Rio Grande do SulPorto AlegreBrazil

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