1,829
Views
6
CrossRef citations to date
0
Altmetric
Original Investigation

Testing differential susceptibility: Plasticity genes, the social environment, and their interplay in adolescent response inhibition

, , , , , , , , , & show all
Pages 308-321 | Received 11 Apr 2015, Accepted 29 Mar 2016, Published online: 12 May 2016

References

  • Alderson RM, Rapport MD, Kofler MJ. 2007. Attention-deficit/hyperactivity disorder and behavioral inhibition: a meta-analytic review of the stop-signal paradigm. J Abnorm Child Psychol. 35:745–758.
  • Aron AR, Robbins TW, Poldrack RA. 2014. Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci. 18:177–185.
  • Baehne CG, Ehlis AC, Plichta MM, Conzelmann A, Pauli P, Jacob C, Gutknecht L, Lesch KP, Fallgatter AJ. 2009. Tph2 gene variants modulate response control processes in adult ADHD patients and healthy individuals. Mol Psychiatry. 14:1032–1039.
  • 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. 23:39–52.
  • Barkley RA. 1997. Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull. 121:65–94.
  • Beaver KM, Belsky J. 2012. Gene-environment interaction and the intergenerational transmission of parenting: testing the differential-susceptibility hypothesis. Psychiatr Q. 83:29–40.
  • Bekker EM, Overtoom CC, Kooij JJ, Buitelaar JK, Verbaten MN, Kenemans JL. 2005. Disentangling deficits in adults with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 62:1129–1136.
  • Belsky J. 1997. Variation in Susceptibility to Environmental Influence: An Evolutionary Argument. Psychol Inq. 8:182–186.
  • Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, Williams R. 2009. Vulnerability genes or plasticity genes? Mol Psychiatry. 14:746–754.
  • Belsky J, Pluess M. 2009. Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull. 135:885–908.
  • Belsky J, Pluess M. 2013. Beyond risk, resilience, and dysregulation: phenotypic plasticity and human development. Dev Psychopathol. 25:1243–1261.
  • Beydoun H, Saftlas AF. 2008. Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatr Perinat Epidemiol. 22:438–466.
  • Braet W, Johnson KA, Tobin CT, Acheson R, McDonnell C, Hawi Z, Barry E, Mulligan A, Gill M, Bellgrove MA, et al. 2011. fMRI activation during response inhibition and error processing: the role of the DAT1 gene in typically developing adolescents and those diagnosed with ADHD. Neuropsychologia. 49:1641–1650.
  • Brookes K, Xu X, Chen W, Zhou K, Neale B, Lowe N, Anney R, Franke B, Gill M, Ebstein R, et al. 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. 11:934–953.
  • Brown GW. 1966. The measurement of family activities and relationships: A methodological study. Hum Relations. 19:241–263.
  • Burt SA, Klump KL. 2014. Prosocial peer affiliation suppresses genetic influences on non-aggressive antisocial behaviors during childhood. Psychol Med. 44:821–830.
  • Burt SA, McGue M, Iacono WG. 2009. Nonshared environmental mediation of the association between deviant peer affiliation and adolescent externalizing behaviors over time: results from a cross-lagged monozygotic twin differences design. Dev Psychol. 45:1752–1760.
  • Chen W, Taylor E. 2006. PACS interview and genetic research in ADHD. In: Oades R, editor. Attention-deficit/hyperactivity disorder HKS: current ideas and ways forward. 1st ed. New York: Nova Science Publishers Inc.; p. 3–20.
  • Clark L, Roiser JP, Cools R, Rubinsztein DC, Sahakian BJ, Robbins TW. 2005. Stop signal response inhibition is not modulated by tryptophan depletion or the serotonin transporter polymorphism in healthy volunteers: implications for the 5-HT theory of impulsivity. Psychopharmacology (Berl). 182:570–578.
  • Colzato LS, van den Wildenberg WP, Van der Does AJ, Hommel B. 2010. Genetic markers of striatal dopamine predict individual differences in dysfunctional, but not functional impulsivity. Neuroscience. 170:782–788.
  • Congdon E, Canli T. 2008. A neurogenetic approach to impulsivity. J Pers. 76:1447–1484.
  • Congdon E, Constable RT, Lesch KP, Canli T. 2009. Influence of SLC6A3 and COMT variation on neural activation during response inhibition. Biol Psychol. 81:144–152.
  • Congdon E, Lesch KP, Canli T. 2008. Analysis of DRD4 and DAT polymorphisms and behavioral inhibition in healthy adults: implications for impulsivity. Am J Med Genet B Neuropsychiatr Genet. 147B:27–B32.
  • 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.
  • Cools R, Nakamura K, Daw ND. 2011. Serotonin and dopamine: unifying affective, activational, and decision functions. Neuropsychopharmacology. 36:98–113.
  • Cornish KM, Manly T, Savage R, Swanson J, Morisano D, Butler N, Grant C, Cross G, Bentley L, Hollis CP. 2005. Association of the dopamine transporter (DAT1) 10/10-repeat genotype with ADHD symptoms and response inhibition in a general population sample. Mol Psychiatry. 10:686–698.
  • Counts CA, Nigg JT, Stawicki JA, Rappley MD, von Eye A. 2005. Family adversity in DSM-IV ADHD combined and inattentive subtypes and associated disruptive behavior problems. J Am Acad Child Adolesc Psychiatry. 44:690–698.
  • Crosbie J, Arnold P, Paterson A, Swanson J, Dupuis A, Li X, Shan J, Goodale T, Tam C, Strug LJ, et al. 2013. Response inhibition and ADHD traits: correlates and heritability in a community sample. J Abnorm Child Psychol. 41:497–507.
  • Cummins TD, Hawi Z, Hocking J, Strudwick M, Hester R, Garavan H, Wagner J, Chambers CD, Bellgrove MA. 2012. Dopamine transporter genotype predicts behavioural and neural measures of response inhibition. Mol Psychiatry. 17:1086–1092.
  • de Zeeuw P, Aarnoudse-Moens C, Bijlhout J, Konig C, Post Uiterweer A, Papanikolau A, Hoogenraad C, Imandt L, de Been D, Sergeant JA, et al. 2008. Inhibitory performance, response speed, intraindividual variability, and response accuracy in ADHD. J Am Acad Child Adolesc Psychiatry. 47:808–816.
  • Dennis M, Francis DJ, Cirino PT, Schachar R, Barnes MA, Fletcher JM. 2009. Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. J Int Neuropsychol Soc. 15:331–343.
  • Diamond A. 2013. Executive functions. Annu Rev Psychol. 64:135–168.
  • Drueke B, Boecker M, Schlaegel S, Moeller O, Hiemke C, Grunder G, Gauggel S. 2010. Serotonergic modulation of response inhibition and re-engagement? Results of a study in healthy human volunteers. Hum Psychopharmacol. 25:472–480.
  • Ellis BJ, Boyce WT, Belsky J, Bakermans-Kranenburg MJ, van IJzendoorn MH. 2011. Differential susceptibility to the environment: an evolutionary-neurodevelopmental theory. Dev Psychopathol. 23:7–28.
  • Elton A, Tripathi SP, Mletzko T, Young J, Cisler JM, James GA, Kilts CD. 2014. Childhood maltreatment is associated with a sex-dependent functional reorganization of a brain inhibitory control network. Hum Brain Mapp. 35:1654–1667.
  • Fabes RA, Hanish LD, Martin CL, Moss A, Reesing A. 2012. The effects of young children's affiliations with prosocial peers on subsequent emotionality in peer interactions. Br J Dev Psychol. 30:569–585.
  • Fair DA, Bathula D, Nikolas MA, Nigg JT. 2012. Distinct neuropsychological subgroups in typically developing youth inform heterogeneity in children with ADHD. Proc Natl Acad Sci USA. 109:6769–6774.
  • Farley JP, Kim-Spoon J. 2014. The development of adolescent self-regulation: reviewing the role of parent, peer, friend, and romantic relationships. J Adolesc. 37:433–440.
  • Filbey FM, Claus ED, Morgan M, Forester GR, Hutchison K. 2012. Dopaminergic genes modulate response inhibition in alcohol abusing adults. Addict Biol. 17:1046–1056.
  • Friedman NP, Miyake A, Young SE, Defries JC, Corley RP, Hewitt JK. 2008. Individual differences in executive functions are almost entirely genetic in origin. J Exp Psychol Gen. 137:201–225.
  • Gifford-Smith M, Dodge KA, Dishion TJ, McCord J. 2005. Peer influence in children and adolescents: crossing the bridge from developmental to intervention science. J Abnorm Child Psychol. 33:255–265.
  • Hall FS, Perona MT. 2012. Have studies of the developmental regulation of behavioral phenotypes revealed the mechanisms of gene-environment interactions? Physiol Behav. 107:623–640.
  • Hampshire A. 2015. Putting the brakes on inhibitory models of frontal lobe function. Neuroimage. 113:340–355.
  • Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM. 2010. The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage. 50:1313–1319.
  • Hart H, Radua J, Nakao T, Mataix-Cols D, Rubia K. 2013. Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry. 70:185–198.
  • Hedden T, Gabrieli JD. 2010. Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control. Neuroimage. 51:421–431.
  • Heinzel S, Dresler T, Baehne CG, Heine M, Boreatti-Hummer A, Jacob CP, Renner TJ, Reif A, Lesch KP, Fallgatter AJ, et al. 2013. COMT x DRD4 epistasis impacts prefrontal cortex function underlying response control. Cereb Cortex. 23:1453–1462.
  • Hicks BM, South SC, Dirago AC, Iacono WG, McGue M. 2009. Environmental adversity and increasing genetic risk for externalizing disorders. Arch Gen Psychiatry. 66:640–648.
  • Holz NE, Boecker R, Baumeister S, Hohm E, Zohsel K, Buchmann AF, Blomeyer D, Jennen-Steinmetz C, Hohmann S, Wolf I, et al. 2014. Effect of prenatal exposure to tobacco smoke on inhibitory control: neuroimaging results from a 25-year prospective study. JAMA Psychiatry. 71:786–796.
  • Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N. 1997. Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry. 36:980–988.
  • Knafo A, Jaffee SR. 2013. Gene-environment correlation in developmental psychopathology. Dev Psychopathol. 25:1–6.
  • Kramer UM, Rojo N, Schule R, Cunillera T, Schols L, Marco-Pallares J, Cucurell D, Camara E, Rodriguez-Fornells A, Munte TF. 2009. ADHD candidate gene (DRD4 exon III) affects inhibitory control in a healthy sample. BMC Neurosci. 10:150.
  • Landro NI, Jonassen R, Clark L, Haug KB, Aker M, Bo R, Berg JP, Neumeister A, Stiles TC. 2014. Serotonin transporter polymorphisms predict response inhibition in healthy volunteers. Neurosci Lett. 584C:109–112.
  • Langley K, Marshall L, van den Bree M, Thomas H, Owen M, O'Donovan M, Thapar A. 2004. Association of the dopamine D4 receptor gene 7-repeat allele with neuropsychological test performance of children with ADHD. Am J Psychiatry. 161:133–138.
  • Laucht M, Skowronek MH, Becker K, Schmidt MH, Esser G, Schulze TG, Rietschel M. 2007. Interacting effects of the dopamine transporter gene and psychosocial adversity on attention-deficit/hyperactivity disorder symptoms among 15-year-olds from a high-risk community sample. Arch Gen Psychiatry. 64:585–590.
  • Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J, Muller CR, Hamer DH, Murphy DL. 1996. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science. 274:1527–1531.
  • Lewis EE, Dozier M, Ackerman J, Sepulveda-Kozakowski S. 2007. The effect of placement instability on adopted children's inhibitory control abilities and oppositional behavior. Dev Psychol. 43:1415–1427.
  • Li J, Ji L. 2005. Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity. 95:221–227.
  • Lipszyc J, Schachar R. 2010. Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. J Int Neuropsychol Soc. 16:1064–1076.
  • Logan GD, Cowan WB, Davis KA. 1984. On the ability to inhibit simple and choice reaction time responses: a model and a method. J Exp Psychol Hum Percept Perform. 10:276–291.
  • Lupien SJ, McEwen BS, Gunnar MR, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 10:434–445.
  • Mika A, Mazur GJ, Hoffman AN, Talboom JS, Bimonte-Nelson HA, Sanabria F, Conrad CD. 2012. Chronic stress impairs prefrontal cortex-dependent response inhibition and spatial working memory. Behav Neurosci. 126:605–619.
  • Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. 2000. The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cogn Psychol. 41:49–100.
  • Monroe SM, Simons AD. 1991. Diathesis-stress theories in the context of life stress research: implications for the depressive disorders. Psychol Bull 110(3):406–425.
  • Mulligan RC, Kristjansson SD, Reiersen AM, Parra AS, Anokhin AP. 2014. Neural correlates of inhibitory control and functional genetic variation in the dopamine D4 receptor gene. Neuropsychologia. 62:306–318.
  • Nigg J, Nikolas M, Friderici K, Park L, Zucker RA. 2007. Genotype and neuropsychological response inhibition as resilience promoters for attention-deficit/hyperactivity disorder, oppositional defiant disorder, and conduct disorder under conditions of psychosocial adversity. Dev Psychopathol. 19:767–786.
  • Nigg JT, Willcutt EG, Doyle AE, Sonuga-Barke EJ. 2005. Causal heterogeneity in attention-deficit/hyperactivity disorder: do we need neuropsychologically impaired subtypes? Biol Psychiatry. 57:1224–1230.
  • Nishikawa S, Nishitani S, Fujisawa TX, Noborimoto I, Kitahara T, Takamura T, Shinohara K. 2012. Perceived parental rejection mediates the influence of serotonin transporter gene (5-HTTLPR) polymorphisms on impulsivity in Japanese adults. PLoS One. 7:e47608.
  • Oosterlaan J, Logan GD, Sergeant JA. 1998. Response inhibition in AD/HD, CD, comorbid AD/HD + CD, anxious, and control children: a meta-analysis of studies with the stop task. J Child Psychol Psychiatry. 39:411–425.
  • Overtoom CC, Bekker EM, van der Molen MW, Verbaten MN, Kooij JJ, Buitelaar JK, Kenemans JL. 2009. Methylphenidate restores link between stop-signal sensory impact and successful stopping in adults with attention-deficit/hyperactivity disorder. Biol Psychiatry. 65:614–619.
  • Polanska K, Jurewicz J, Hanke W. 2012. Exposure to environmental and lifestyle factors and attention-deficit/hyperactivity disorder in children - a review of epidemiological studies. Int J Occup Med Environ Health. 25:330–355.
  • Richards JS, Vasquez AA, Rommelse NN, 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 (ADHD): relation with severity and persistence of ADHD and comorbidity. J Am Acad Child Adolesc Psychiatry. 53:311–319 e1.
  • Roisman GI, Newman DA, Fraley RC, Haltigan JD, Groh AM, Haydon KC. 2012. Distinguishing differential susceptibility from diathesis-stress: recommendations for evaluating interaction effects. Dev Psychopathol. 24:389–409.
  • Rommelse NN, Altink ME, Arias-Vasquez A, Buschgens CJ, Fliers E, Faraone SV, Buitelaar JK, Sergeant JA, Franke B, Oosterlaan J. 2008. A review and analysis of the relationship between neuropsychological measures and DAT1 in ADHD. Am J Med Genet B Neuropsychiatr Genet. 147B:1536–1546.
  • 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.
  • Schachar RJ, Forget-Dubois N, Dionne G, Boivin M, Robaey P. 2011. Heritability of response inhibition in children. J Int Neuropsychol Soc. 17:238–247.
  • Sjowall D, Roth L, Lindqvist S, Thorell LB. 2013. Multiple deficits in ADHD: executive dysfunction, delay aversion, reaction time variability, and emotional deficits. J Child Psychol Psychiatry. 54:619–627.
  • Smith JL, Mattick RP, Jamadar SD, Iredale JM. 2014. Deficits in behavioural inhibition in substance abuse and addiction: A meta-analysis. Drug Alcohol Depend. 145C:1–33.
  • Sonuga-Barke EJ, Oades RD, Psychogiou L, Chen W, Franke B, Buitelaar J, Banaschewski T, Ebstein RP, Gil M, Anney R, et al. 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. 50:1052–1063.
  • Stoltenberg SF, Glass JM, Chermack ST, Flynn HA, Li S, Weston ME, Burmeister M. 2006. Possible association between response inhibition and a variant in the brain-expressed tryptophan hydroxylase-2 gene. Psychiatr Genet 16:35–38.
  • Swanson J, Oosterlaan J, Murias M, Schuck S, Flodman P, Spence MA, Wasdell M, Ding Y, Chi HC, Smith M, et al. 2000. Attention deficit/hyperactivity disorder children with a 7-repeat allele of the dopamine receptor D4 gene have extreme behavior but normal performance on critical neuropsychological tests of attention. Proc Natl Acad Sci USA. 97:4754–4759.
  • Swick D, Ashley V, Turken AU. 2008. Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci. 9:102.
  • Tibu F, Sheridan MA, McLaughlin KA, Nelson CA, Fox NA, Zeanah CH. 2016. Disruptions of working memory and inhibition mediate the association between exposure to institutionalization and symptoms of attention deficit hyperactivity disorder. Psychol Med. 46:529–541.
  • Van den Bergh BR, Mennes M, Oosterlaan J, Stevens V, Stiers P, Marcoen A, Lagae L. 2005. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehav Rev. 29:259–269.
  • van der Meer D, Hartman CA, Richards J, Bralten JB, Franke B, Oosterlaan J, Heslenfeld DJ, Faraone SV, Buitelaar JK, Hoekstra PJ. 2014. The serotonin transporter gene polymorphism 5-HTTLPR moderates the effects of stress on attention-deficit/hyperactivity disorder. J Child Psychol Psychiatry. 55:1363–1371.
  • van IJzendoorn MH, Belsky J, Bakermans-Kranenburg MJ. 2012. Serotonin transporter genotype 5HTTLPR as a marker of differential susceptibility? A meta-analysis of child and adolescent gene-by-environment studies. Transl Psychiatry. 2:e147.
  • van Rooij D, Hartman C, van Donkelaar M, Bralten J, von Rhein D, Hakobjan M, Franke B, Heslenfeld D, Oosterlaan J, Rommelse N, et al. 2015a. Variation in serotonin neurotransmission genes affects neural activation during response inhibition in adolescents and young adults with ADHD and healthy controls. World J Biol Psychiatry. 16:625-634.
  • van Rooij D, Hoekstra PJ, Mennes M, von Rhein D, Thissen AJ, Heslenfeld D, Zwiers MP, Faraone SV, Oosterlaan J, Franke B, et al. 2015b. Distinguishing adolescents with ADHD from their unaffected siblings and healthy comparison subjects by neural activation patterns during response inhibition. Am J Psychiatry. 172:674–683.
  • van Velzen LS, Vriend C, de Wit SJ, van den Heuvel OA. 2014. Response inhibition and interference control in obsessive-compulsive spectrum disorders. Front Hum Neurosci. 8:419.
  • Vitaro F, Brendgen M, Boivin M, Cantin S, Dionne G, Tremblay RE, Girard A, Perusse D. 2011. A monozygotic twin difference study of friends' aggression and children's adjustment problems. Child Dev. 82:617–632.
  • von Rhein D, Mennes M, van Ewijk H, Groenman AP, Zwiers MP, Oosterlaan J, Heslenfeld D, Franke B, Hoekstra PJ, Faraone SV, et al. 2015. The NeuroIMAGE study: a prospective phenotypic, cognitive, genetic and MRI study in children with attention-deficit/hyperactivity disorder. Design and descriptives. Eur Child Adolesc Psychiatry. 24:265–281.
  • Wagner S, Baskaya O, Lieb K, Dahmen N, Tadic A. 2009. The 5-HTTLPR polymorphism modulates the association of serious life events (SLE) and impulsivity in patients with Borderline Personality Disorder. J Psychiatr Res. 43:1067–1072.
  • Walden B, McGue M, Lacono WG, Burt SA, Elkins I. 2004. Identifying shared environmental contributions to early substance use: the respective roles of peers and parents. J Abnorm Psychol. 113:440–450.
  • Warren SL, Crocker LD, Spielberg JM, Engels AS, Banich MT, Sutton BP, Miller GA, Heller W. 2013. Cortical organization of inhibition-related functions and modulation by psychopathology. Front Hum Neurosci. 7:271.
  • Wechsler D. 2000. WAIS-III Nederlandstalige bewerking. Technische handleiding. London: The Psychological Corperation.
  • Wechsler D. 2002. WISC-III Handleiding. London: The Psychological Corperation.
  • Willcutt EG, Pennington BF, Duncan L, Smith SD, Keenan JM, Wadsworth S, Defries JC, Olson RK. 2010. Understanding the complex etiologies of developmental disorders: behavioral and molecular genetic approaches. J Dev Behav Pediatr. 31:533–544.
  • Xu X, Duman EA, Anney R, Brookes K, Franke B, Zhou K, Buschgens C, Chen W, Christiansen H, Eisenberg J, et al. 2008. No association between two polymorphisms of the serotonin transporter gene and combined type attention deficit hyperactivity disorder. Am J Med Genet B Neuropsychiatr Genet. 147B:1306–1309.
  • Zubin J, Spring B. 1977. Vulnerability - a new view of schizophrenia. J Abnorm Psychol. 86:103–126.