Skip to main content

Advertisement

SpringerLink
Log in

Differential susceptibility to maternal expressed emotion in children with ADHD and their siblings? Investigating plasticity genes, prosocial and antisocial behaviour

  • Original Contribution
  • Published:
European Child & Adolescent Psychiatry Aims and scope Submit manuscript

An Erratum to this article was published on 04 August 2015

Abstract

The differential susceptibility theory states that children differ in their susceptibility towards environmental experiences, partially due to plasticity genes. Individuals carrying specific variants in such genes will be more disadvantaged in negative but, conversely, more advantaged in positive environments. Understanding gene–environment interactions may help unravel the causal mechanisms involved in multifactorial psychiatric disorders such as Attention-Deficit/Hyperactivity Disorder (ADHD). The differential susceptibility theory was examined by investigating the presence of interaction effects between maternal expressed emotion (EE; warmth and criticism) and the solitary and combined effects of plasticity genes (DAT1, DRD4, 5-HTT) on prosocial and antisocial behaviour (measured with parent- and self-reports) in children with ADHD and their siblings (N = 366, M = 17.11 years, 74.9 % male). Maternal warmth was positively associated with prosocial behaviour and negatively with antisocial behaviour, while maternal criticism was positively associated with antisocial behaviour and negatively with prosocial behaviour. No evidence of differential susceptibility was found. The current study found no evidence for differential susceptibility based on the selected plasticity genes, in spite of strong EE–behaviour associations. It is likely that additional factors play a role in the complex relationship between genes, environment and behaviour.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Wermter A-K, Laucht M, Schimmelmann BG, Banaschweski T, Sonuga-Barke EJS, Rietschel M, Becker K (2010) From nature versus nurture, via nature and nurture, to gene x environment interaction in mental disorders. Eur Child Adolesc Psychiatry 19:199–210. doi:10.1007/s00787-009-0082-z

    Article  PubMed  Google Scholar 

  2. Belsky J (1997) Variation in susceptibility to environmental influence: an evolutionary argument. Psychol Inq 8(3):182–186. doi:10.1207/s15327965pli0803_3

    Article  Google Scholar 

  3. Belsky J (2005) Differential susceptibility to rearing influences: an evolutionary hypothesis and some evidence. In: Ellis BJ, Bjorklund DF (eds) Origins of the social mind: evolutionary psychology and child development. Guilford Press, New York, pp 139–163

    Google Scholar 

  4. Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, Williams R (2009) Vulnerability genes or plasticity genes? Mol Psychiatry 14(8):746–754. doi:10.1038/mp.2009.44

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Ellis BJ, Boyce WT (2011) Differential susceptibility to the environment: toward an understanding of sensitivity to developmental experiences and context. Dev Psychopathol 23(1):1–5. doi:10.1017/S095457941000060X

    Article  PubMed  Google Scholar 

  6. Belsky J, Pluess M (2009) Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull 135(6):885–908. doi:10.1037/a0017376

    Article  PubMed  Google Scholar 

  7. Belsky J, Pluess M (2013) Beyond risk, resilience, and dysregulation: phenotypic plasticity and human development. Dev Psychopathol 25:1243–1261. doi:10.1017/S095457941300059X

    Article  PubMed  Google Scholar 

  8. Bakermans-Kranenburg MJ, van Ijzendoorn MH (2011) Differential susceptibility to rearing environment depending on dopamine-related genes: new evidence and a meta-analysis. Dev Psychopathol 23(1):39–52. doi:10.1017/S0954579410000635

    Article  PubMed  Google Scholar 

  9. Belsky J, Pluess M (2013) Genetic moderation of early child-care effects on social functioning across childhood: a developmental analysis. Child Dev 84(4):1209–1225. doi:10.1111/cdev.12058

    Article  PubMed Central  PubMed  Google Scholar 

  10. Knafo A, Israel S, Ebstein RP (2011) Heritability of children’s prosocial behavior and differential susceptibility to parenting by variation in the dopamine receptor D4 gene. Dev Psychopathol 23(1):53–67. doi:10.1017/S0954579410000647

    Article  PubMed  Google Scholar 

  11. Pluess M, Belsky J, Neuman RJ (2009) Prenatal smoking and attention-deficit/hyperactivity disorder: DRD4-7R as a plasticity gene. Biol Psychiatry 66:e5–e6. doi:10.1016/j.biopsych.2009.04.019

    Article  PubMed  Google Scholar 

  12. Drury SS, Gleason MM, Theall KP, Smyke AT, Nelson CA, Fox NA, Zeanah CH (2012) Genetic sensitivity to the caregiving context: the influence of 5httlpr and BDNF val66met on indiscriminate social behavior. Physiol Behav 106(5):728–735. doi:10.1016/j.physbeh.2011.11.014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Hankin BL, Nederhof E, Oppenheimer CW, Jenness J, Young JF, Abela JR, Smolen A, Ormel J, Oldehinkel AJ (2011) Differential susceptibility in youth: evidence that 5-HTTLPR × positive parenting is associated with positive affect ‘for better and worse’. Transl Psychiatry 1:e44. doi:10.1038/tp.2011.44

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Kochanska G, Kim S, Barry RA, Philibert RA (2011) Children’s genotypes interact with maternal responsive care in predicting children’s competence: diathesis-stress or differential susceptibility? Dev Psychopathol 23(2):605–616. doi:10.1017/S0954579411000071

    Article  PubMed Central  PubMed  Google Scholar 

  15. Pluess M, Belsky J, Way BM, Taylor SE (2010) 5-HTTLPR moderates effects of current life events on neuroticism: differential susceptibility to environmental influences. Prog Neuropsychopharmacol Biol Psychiatry 34(6):1070–1074. doi:10.1016/j.pnpbp.2010.05.028

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Retz W, Freitag CM, Retz-Junginger P, Wenzler D, Schneider M, Kissling C, Thome J, Rosler M (2008) A functional serotonin transporter promoter gene polymorphism increases ADHD symptoms in delinquents: interaction with adverse childhood environment. Psychiatry Res 158(2):123–131. doi:10.1016/j.psychres.2007.05.004

    Article  CAS  PubMed  Google Scholar 

  17. Sonuga-Barke EJ, Oades RD, Psychogiou L, Chen W, Franke B, Buitelaar J, Banaschewski T, Ebstein RP, Gil M, Anney R, Miranda A, Roeyers H, Rothenberger A, Sergeant J, Steinhausen HC, Thompson M, Asherson P, Faraone SV (2009) Dopamine and serotonin transporter genotypes moderate sensitivity to maternal expressed emotion: the case of conduct and emotional problems in attention deficit/hyperactivity disorder. J Child Psychol Psychiatry 50(9):1052–1063. doi:10.1111/j.1469-7610.2009.02095.x

    Article  PubMed  Google Scholar 

  18. Beaver KM, Belsky J (2012) Gene-environment interaction and the intergenerational transmission of parenting: testing the differential-susceptibility hypothesis. Psychiatr Q 83(1):29–40. doi:10.1007/s11126-011-9180-4

    Article  PubMed  Google Scholar 

  19. Caylak E (2012) Biochemical and genetic analyses of childhood attention deficit/hyperactivity disorder. Am J Hum Genet B: Neuropsychiatr Genet 159B(6):613–627. doi:10.1002/ajmg.b.32077

    Google Scholar 

  20. Psychogiou L, Daley DM, Thompson MJ, Sonuga-Barke EJS (2007) Mothers’ expressed emotion toward their school-aged sons. Associations with child and maternal symptoms of psychopathology. Eur Child Adolesc Psychiatry 16:458–464. doi:10.1007/s00787-007-0619-y

    Article  PubMed  Google Scholar 

  21. Cartwright KL, Bitsakou P, Daley D, Gramzow RH, Psychogiou L, Simonoff E, Thompson MJ, Sonuga-Barke EJS (2011) Disentangling child and family influences on maternal expressed emotion toward children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 50:1042–1053. doi:10.1016/j.jaac.2011.07.006

    Article  PubMed  Google Scholar 

  22. Pfiffner LJ, McBurnett K, Rathouz PJ, Judice S (2005) Family correlates of oppositional and conduct disorders in children with attention deficit/hyperactivity disorder. J Abnorm Child Psychol 33(5):551–563. doi:10.1007/s10802-005-6737-4

    Article  PubMed  Google Scholar 

  23. Richards JS, Arias Vásquez A, Rommelse NNJ, Oosterlaan J, Hoekstra PJ, Franke B, Hartman CA, Buitelaar JK (2014) A follow-up study of maternal expressed emotion toward children with attention-deficit/hyperactivity disorder: relation with severity and persistence of ADHD and comorbidity. J Am Acad Child Adolesc Psychiatry 53(3):311–319. doi:10.1016/j.jaac.2013.11.011

    Article  PubMed Central  PubMed  Google Scholar 

  24. Brookes K, Xu X, Chen W, Zhou K, Neale B, Lowe N, Anney R, Franke B, Gill M, Ebstein R, Buitelaar J, Sham P, Campbell D, Knight J, Andreou P, Altink M, Arnold R, Boer F, Buschgens C, Butler L, Christiansen H, Feldman L, Fleischman K, Fliers E, Howe-Forbes R, Goldfarb A, Heise A, Gabriels I, Korn-Lubetzki I, Johansson L, Marco R, Medad S, Minderaa R, Mulas F, Muller U, Mulligan A, Rabin K, Rommelse N, Sethna V, Sorohan J, Uebel H, Psychogiou L, Weeks A, Barrett R, Craig I, Banaschewski T, Sonuga-Barke E, Eisenberg J, Kuntsi J, Manor I, McGuffin P, Miranda A, Oades RD, Plomin R, Roeyers H, Rothenberger A, Sergeant J, Steinhausen HC, Taylor E, Thompson M, Faraone SV, Asherson P (2006) The analysis of 51 genes in DSM-IV combined type attention deficit hyperactivity disorder: association signals in DRD4, DAT1 and 16 other genes. Mol Psychiatry 11(10):934–953. doi:10.1038/sj.mp.4001869

    Article  CAS  PubMed  Google Scholar 

  25. van Widenfelt BM, Goedhart AW, Treffers PD, Goodman R (2003) Dutch version of the Strengths and Difficulties Questionnaire (SDQ). Eur Child Adolesc Psychiatry 12(6):281–289. doi:10.1007/s00787-003-0341-3

    Article  PubMed  Google Scholar 

  26. Muris P, Meesters C, van den Berg F (2003) The Strengths and Difficulties Questionnaire (SDQ)––further evidence for its reliability and validity in a community sample of Dutch children and adolescents. Eur Child Adolesc Psychiatry 12(1):1–8. doi:10.1007/s00787-003-0298-2

    Article  PubMed  Google Scholar 

  27. Goodman R, Renfrew D, Mullick M (2000) Predicting type of psychiatric disorder from Strengths and Difficulties Questionnaire (SDQ) scores in child mental health clinics in London and Dhaka. Eur Child Adolesc Psychiatry 9(2):129–134

    Article  CAS  PubMed  Google Scholar 

  28. Klasen H, Woerner W, Rothenberger A, Goodman R (2003) German version of the Strength and Difficulties Questionnaire (SDQ-German)––overview and evaluation of initial validation and normative results. Prax Kinderpsychol Kinderpsychiatr 52(7):491–502

    PubMed  Google Scholar 

  29. Brown GW (1966) The measurement of family activities and relationships: a methodological study. Hum Relat 19:241–263. doi:10.1177/001872676601900301

    Article  Google Scholar 

  30. Schachar R, Taylor E, Wieselberg M, Thorley G, Rutter M (1987) Changes in family function and relationships in children who respond to methylphenidate. J Am Acad Child Adolesc Psychiatry 26:728–732. doi:10.1097/00004583-198709000-00019

    Article  CAS  PubMed  Google Scholar 

  31. Chen W, Taylor E (2006) PACS interview and genetic research in ADHD. In: Oades R (ed) Attention-Deficit/Hyperactivity Disorder HKS: Current ideas and ways forward, 1st edn. Nova Science Publishers, New York, pp 3–20

    Google Scholar 

  32. Xu X, Duman EA, Anney R, Brookes K, Franke B, Zhou K, Buschgens C, Chen W, Christiansen H, Eisenberg J, Gabriels I, Manor I, Marco R, Muller UC, Mulligan A, Rommelse N, Thompson M, Uebel H, Banaschewski T, Buitelaar J, Ebstein R, Gill M, Miranda A, Mulas F, Oades RD, Roeyers H, Rothenberger A, Sergeant J, Sonuga-Barke E, Steinhausen HC, Taylor E, Faraone SV, Asherson P (2008) No association between two polymorphisms of the serotonin transporter gene and combined type attention deficit hyperactivity disorder. Am J Hum Genet Part B: Neuropsychiatr Genet 147B(7):1306–1309. doi:10.1002/ajmg.b.30737

    Article  CAS  Google Scholar 

  33. Buis ML (2010) Inequality of educational outcome and inequality of educational opportunity in the Netherlands during the 20th century. Scaling levels of education. Ph.D. thesis, Faculty of Social Sciences, VU-University Amsterdam, Amsterdam

  34. Gerris JRM, Houtmans MJM, Kwaaitaal-Roosen EMG, Schipper JC, Vermulst AA, Janssens JMAM (1998) Parents, adolescents, and young adults in Dutch families: a longitudinal study. Nijmegen: University of Nijmegen, Institute of Family Studies

  35. Goldberg LR (1992) The development of markers for the Big-Five factor structure. Psychol Assess 4:26–42

    Article  Google Scholar 

  36. Conners CK, Sitarenios G, Parker JD, Epstein JN (1998) The revised Conners’ Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity. J Abnorm Child Psychol 26:257–268

    Article  CAS  PubMed  Google Scholar 

  37. Knafo A, Jaffee SR (2013) Gene–environment correlation in developmental psychopathology. Dev Psychopathol 25(1):1–6. doi:10.1017/S0954579412000855

    Article  PubMed  Google Scholar 

  38. Li J, Ji L (2005) Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity (Edinb) 95(3):221–227. doi:10.1038/sj.hdy.6800717

    Article  CAS  Google Scholar 

  39. Asherson P, Brookes K, Franke B, Chen W, Gill M, Ebstein RP, Buitelaar J, Banaschewski T, Sonuga-Barke E, Eisenberg J, Manor I, Miranda A, Oades RD, Roeyers H, Rothenberger A, Sergeant J, Steinhausen HC, Faraone SV (2007) Confirmation that a specific haplotype of the dopamine transporter gene is associated with combined-type ADHD. Am J Psychiatry 164(4):674–677. doi:10.1176/appi.ajp.164.4.674

    Article  PubMed  Google Scholar 

  40. Franke B, Vasquez AA, Johansson S, Hoogman M, Romanos J, Boreatti-Hummer A, Heine M, Jacob CP, Lesch KP, Casas M, Ribases M, Bosch R, Sanchez-Mora C, Gomez-Barros N, Fernandez-Castillo N, Bayes M, Halmoy A, Halleland H, Landaas ET, Fasmer OB, Knappskog PM, Heister AJ, Kiemeney LA, Kooij JJ, Boonstra AM, Kan CC, Asherson P, Faraone SV, Buitelaar JK, Haavik J, Cormand B, Ramos-Quiroga JA, Reif A (2010) Multicenter analysis of the SLC6A3/DAT1 VNTR haplotype in persistent ADHD suggests differential involvement of the gene in childhood and persistent ADHD. Neuropsychopharmacology 35(3):656–664. doi:10.1038/npp.2009.170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Bakermans-Kranenburg MJ, van Ijzendoorn MH (2006) Gene–environment interaction of the dopamine D4 receptor (DRD4) and observed maternal insensitivity predicting externalizing behavior in preschoolers. Dev Psychobiol 48(5):406–409. doi:10.1002/dev.20152

    Article  CAS  PubMed  Google Scholar 

  42. Bakermans-Kranenburg MJ, Van IMH, Pijlman FT, Mesman J, Juffer F (2008) Experimental evidence for differential susceptibility: dopamine D4 receptor polymorphism (DRD4 VNTR) moderates intervention effects on toddlers’ externalizing behavior in a randomized controlled trial. Dev Psychol 44(1):293–300. doi:10.1037/0012-1649.44.1.293

    Article  PubMed  Google Scholar 

  43. Propper C, Willoughby M, Halpern CT, Carbone MA, Cox M (2007) Parenting quality, DRD4, and the prediction of externalizing and internalizing behaviors in early childhood. Dev Psychobiol 49(6):619–632. doi:10.1002/dev.20249

    Article  CAS  PubMed  Google Scholar 

  44. Hirshfeld DR, Biederman J, Brody L, Faraone SV, Rosenbaum JF (1997) Associations between expressed emotion and child behavioral inhibition and psychopathology: a pilot study. J Am Acad Child Adolesc Psychiatry 36:205–213. doi:10.1097/00004583-199702000-00011

    Article  CAS  PubMed  Google Scholar 

  45. Asarnow JR, Tompson M, Hamilton EB, Goldstein MJ, Guthrie D (1994) Family-expressed emotion, childhood-onset depression, and childhood-onset schizophrenia spectrum disorders: is expressed emotion a nonspecific correlate of child psychopathology or a specific risk factor for depression? J Abnorm Child Psychol 22(2):129–146

    Article  CAS  PubMed  Google Scholar 

  46. Hale WW 3rd, Keijsers L, Klimstra TA, Raaijmakers QA, Hawk S, Branje SJ, Frijns T, Wijsbroek SA, van Lier P, Meeus WH (2011) How does longitudinally measured maternal expressed emotion affect internalizing and externalizing symptoms of adolescents from the general community? J Child Psychol Psychiatry 52(11):1174–1183. doi:10.1111/j.1469-7610.2011.02400.x

    Article  PubMed  Google Scholar 

  47. Gauderman WJ, Morrison JM (2006) QUANTO 1.1: A computer program for power and sample size calculations for genetic-epidemiology studies. http://hydra.usc.edu/gxe

  48. Duncan LE, Keller MC (2011) A critical review of the first 10 years of candidate gene-by-environment interaction research in psychiatry. Am J Psychiatry 168(10):1041–1049. doi:10.1176/appi.ajp.2011.11020191

    Article  PubMed Central  PubMed  Google Scholar 

  49. Pluess M, Belsky J (2011) Prenatal programming of postnatal plasticity? Dev Psychopathol 23(1):29–38. doi:10.1017/S0954579410000623

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NIH Grant R01MH62873 (to Dr. Faraone, Department of Psychiatry and of Neuroscience and Physiology, SUNY Upstate Medical University, New York, USA), NWO Large Investment Grant 1750102007010 (to Dr. Buitelaar) and grants from Radboud University Medical Center, University Medical Center Groningen and Accare, and VU University Amsterdam.

Ethical standard

Informed consent was signed by all participants (parents signed informed consent for participants under 12 years of age) and the study was approved by the ethics committee (Centrale Commissie Mensgebonden Onderzoek).

Conflict of interest

In the past 3 years, Dr. Buitelaar has been a consultant to/member of advisory board of/and/or speaker for Janssen Cilag BV, Eli Lilly, Bristol-Myer Squibb, Shering Plough, UCB, Shire, Novartis and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, and royalties. In the past 3 years, Dr. Hoekstra has been a consultant to/member of advisory board of Shire. Dr. Oosterlaan has received an unrestricted investigator initiated research grant from Shire. Ms. Richards and Drs. Franke, Heslenfeld, Arias Vásquez and Hartman have no conflicts of interest do declare.

Author information

Authors and Affiliations

  1. Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, The Netherlands

    Jennifer S. Richards, Alejandro Arias Vásquez & Jan K. Buitelaar

  2. Karakter Child and Adolescent Psychiatry University Center, Nijmegen, The Netherlands

    Jennifer S. Richards & Jan K. Buitelaar

  3. Department of Psychiatry, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

    Catharina A. Hartman & Pieter J. Hoekstra

  4. Department of Human Genetics, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, The Netherlands

    Barbara Franke

  5. Department of Psychiatry, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, The Netherlands

    Barbara Franke & Alejandro Arias Vásquez

  6. Department of Clinical Neuropsychology, VU University Amsterdam, Amsterdam, The Netherlands

    Dirk J. Heslenfeld & Jaap Oosterlaan

Authors
  1. Jennifer S. Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catharina A. Hartman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara Franke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pieter J. Hoekstra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dirk J. Heslenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jaap Oosterlaan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alejandro Arias Vásquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jan K. Buitelaar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer S. Richards.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Richards, J.S., Hartman, C.A., Franke, B. et al. Differential susceptibility to maternal expressed emotion in children with ADHD and their siblings? Investigating plasticity genes, prosocial and antisocial behaviour. Eur Child Adolesc Psychiatry 24, 209–217 (2015). https://doi.org/10.1007/s00787-014-0567-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00787-014-0567-2

Keywords

Search

Navigation