Advertisement

The effects of childhood inattention and anxiety on executive functioning: inhibition, updating, and shifting

  • Peter J. CastagnaEmail author
  • Matthew Calamia
  • Scott Roye
  • Steven G. Greening
  • Thompson E. Davis
Original Article
  • 124 Downloads

Abstract

Although anxiety and attention-deficit/hyperactivity disorder (ADHD) symptoms are highly comorbid, research has generally examined the executive functioning (EF) deficits associated with each of these symptoms independently. The purpose of this study was to examine the unique and interactive effects of anxiety and ADHD symptoms (first respectively, then collectively) on multiple dimensions of EF (i.e., inhibition, updating, and shifting, respectively). A sample of 142 youth from the community (age range 8–17 years; Mage = 11.87 ± 2.94 years) completed the Delis–Kaplan Executive Function System and dimensional measures of anxiety, inattention, and hyperactivity/impulsivity. It was hypothesized that anxiety would moderate the effect of ADHD symptomatology on EF. Multiple regression models examined anxiety and ADHD symptom domains as predictors of EF. When examining ADHD symptom domains separately, anxiety moderated the relationship between inattention and both updating and shifting; the association between hyperactivity/impulsivity and updating was also moderated by anxiety. Within the full model including both ADHD symptom domains, results indicated that anxiety moderated the relationship between inattention and shifting. Analyses of ADHD symptoms in separate and combined models demonstrated a similar pattern: Increased inattention was associated with worse EF and when anxiety was a significant moderator, and increased ADHD symptoms were associated with worse EF only for those with high levels of anxiety. These results highlight the utility of including anxiety in studies examining the relationship between ADHD and EF. EF is related to multiple aspects of daily functioning (e.g., academic achievement), and EF deficits are often targeted in interventions for ADHD.

Keywords

Inattention Hyperactivity Executive functioning ADHD Anxiety 

Notes

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

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.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Achenbach TM, Rescorla LA (2001) Manual for the ASEBA schoolage forms and profiles. University of Vermont; Research Center for Children, Youth, and Families, BurlingtonGoogle Scholar
  2. Baldwin JS, Dadds MR (2007) Reliability and validity of parent and child versions of the multidimensional anxiety scale for children in community samples. J Am Acad Child Adolesc Psychiatry 46(2):252–260PubMedCrossRefGoogle Scholar
  3. Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121(1):65–94PubMedCrossRefGoogle Scholar
  4. Barkley RA, Grodzinsky G, DuPaul GJ (1992) Frontal lobe functions in attention deficit disorder with and without hyperactivity: A review and research report. J Abnorm Child Psychol 20(2):163–188PubMedCrossRefGoogle Scholar
  5. Bedard AC, Ickowicz A, Logan GD, Hogg-Johnson S, Schachar R, Tannock R (2003) Selective inhibition in children with attention-deficit hyperactivity disorder off and on stimulant medication. J Abnorm Child Psychol 31(3):315–327PubMedCrossRefGoogle Scholar
  6. Best JR, Miller PH, Jones LL (2009) Executive functions after age 5: changes and correlates. Dev Rev 29(3):180–200PubMedPubMedCentralCrossRefGoogle Scholar
  7. Brown TE (2006) Attention deficit disorder: the unfocused mind in children and adults. Yale University Press, New HavenGoogle Scholar
  8. Chhabildas NA, Pennington BF, Willcutt EG (2001) A comparison of the cognitive deficits in the DSM-IV subtypes of ADHD. J Abnorm Child Psychol 29(6):529–540PubMedCrossRefGoogle Scholar
  9. Conners CK (1997) Conners’ rating scales-revised: user’s manual. Multi-health systems, incorporatedGoogle Scholar
  10. 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(4):257–268PubMedCrossRefGoogle Scholar
  11. De Panfilis C, Meehan KB, Cain NM, Clarkin JF (2013) The relationship between effortful control, current psychopathology and interpersonal difficulties in adulthood. Compr Psychiatry 54(5):454–461PubMedCrossRefGoogle Scholar
  12. Emerson CS, Mollet GA, Harrison DW (2005) Anxious-depression in boys: an evaluation of executive functioning. Arch Clin Neuropsychol 20(4):539–546PubMedCrossRefGoogle Scholar
  13. Falkowski J, Atchison T, DeButte-Smith M, Weiner MF, O’Bryant S (2013) Executive functioning and the metabolic syndrome: a project FRONTIER study. Arch Clin Neuropsychol 29(1):47–53PubMedPubMedCentralCrossRefGoogle Scholar
  14. Fischer M, Barkley RA, Smallish L, Fletcher K (2005) Executive functioning in hyperactive children as young adults: attention, inhibition, response perseveration, and the impact of comorbidity. Dev Neuropsychol 27(1):107–133PubMedCrossRefGoogle Scholar
  15. Friedman NP, Miyake A (2016) Unity and diversity of executive functions: individual differences as a window on cognitive structure. Cortex 86:186–204PubMedPubMedCentralCrossRefGoogle Scholar
  16. Friedman NP, Haberstick BC, Willcutt EG, Miyake A, Young SE, Corley RP, Hewitt JK (2007) Greater attention problems during childhood predict poorer executive functioning in late adolescence. Psychol Sci 18(10):893–900PubMedCrossRefGoogle Scholar
  17. Friedman NP, Miyake A, Robinson JL, Hewitt JK (2011) Developmental trajectories in toddlers’ self-restraint predict individual differences in executive functions 14 years later: a behavioral genetic analysis. Dev Psychol 47(5):1410–1430PubMedPubMedCentralCrossRefGoogle Scholar
  18. Geurts HM, Verté S, Oosterlaan J, Roeyers H, Sergeant JA (2005) ADHD subtypes: do they differ in their executive functioning profile? Arch Clin Neuropsychol 20(4):457–477PubMedCrossRefGoogle Scholar
  19. Hall PA, Elias LJ, Crossley M (2006) Neurocognitive influences on health behavior in a community sample. Health Psychol 25(6):778–782PubMedCrossRefGoogle Scholar
  20. Halldorsdottir T, Ollendick TH (2014) Comorbid ADHD: implications for the treatment of anxiety disorders in children and adolescents. Cognit Behav Pract 21(3):310–322CrossRefGoogle Scholar
  21. Holmes AJ, Pizzagalli DA (2007) Task feedback effects on conflict monitoring and executive control: relationship to subclinical measures of depression. Emotion 7(1):68–76PubMedPubMedCentralCrossRefGoogle Scholar
  22. Houghton S, Douglas G, West J, Whiting K, Wall M, Langsford S et al (1999) Differential patterns of executive function in children with attention-deficit hyperactivity disorder according to gender and subtype. J Child Neurol 14:801–805PubMedCrossRefGoogle Scholar
  23. Jarrett MA, Ollendick TH (2008) A conceptual review of the comorbidity of attention-deficit/hyperactivity disorder and anxiety: implications for future research and practice. Clin Psychol Rev 28(7):1266–1280PubMedCrossRefGoogle Scholar
  24. Jarrett MA, Wolff JC, Davis TE, Cowart MJ, Ollendick TH (2012) Characteristics of children with ADHD and comorbid anxiety. J Atten Disorders 20:636–644CrossRefGoogle Scholar
  25. Larson K, Russ SA, Kahn RS, Halfon N (2011) Patterns of comorbidity, functioning, and service use for US children with ADHD, 2007. Pediatrics 127(3):462–470PubMedPubMedCentralCrossRefGoogle Scholar
  26. Latzman RD, Markon KE (2010) The factor structure and age-related factorial invariance of the Delis–Kaplan Executive Function System (D–KEFS). Assessment 17(2):172–184PubMedCrossRefGoogle Scholar
  27. Manassis K, Tannock R, Barbosa J (2000) Dichotic listening and response inhibition in children with comorbid anxiety disorders and ADHD. J Am Acad Child Adolesc Psychiatry 39:1152–1159PubMedCrossRefGoogle Scholar
  28. March JS (1998) Multi-dimensional anxiety scale for children. Multi Health Systems, North TonawandaGoogle Scholar
  29. March JS, Parker JD, Sullivan K, Stallings P, Conners CK (1997) The Multidimensional Anxiety Scale for Children (MASC): factor structure, reliability, and validity. J Am Acad Child Adolesc Psychiatry 36(4):554–565PubMedCrossRefGoogle Scholar
  30. Martel M, Nikolas M, Nigg JT (2007) Executive function in adolescents with ADHD. J Am Acad Child Adolesc Psychiatry 46(11):1437–1444PubMedCrossRefGoogle Scholar
  31. Miller M, Nevado-Montenegro AJ, Hinshaw SP (2012) Childhood executive function continues to predict outcomes in young adult females with and without childhood-diagnosed ADHD. J Abnorm Child Psychol 40(5):657–668PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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. Cognit Psychol 41(1):49–100PubMedCrossRefGoogle Scholar
  33. Muris P, Merckelbach H, Wessel I, Van de Ven M (1999) Psychopathological correlates of self-reported behavioural inhibition in normal children. Behav Res Ther 37(6):575–584PubMedCrossRefGoogle Scholar
  34. Muris P, Merckelbach H, Schmidt H, Gadet B, Bogie N (2001) Anxiety and depression as correlates of self-reported behavioural inhibition in normal adolescents. Behav Res Ther 39(9):1051–1061PubMedCrossRefGoogle Scholar
  35. Muris P, Meesters C, Spinder M (2003) Relationships between child-and parent-reported behavioural inhibition and symptoms of anxiety and depression in normal adolescents. Personal Individ Differ 34(5):759–771CrossRefGoogle Scholar
  36. Muris P, van Brakel AM, Arntz A, Schouten E (2011) Behavioral inhibition as a risk factor for the development of childhood anxiety disorders: a longitudinal study. J Child Fam Stud 20(2):157–170PubMedCrossRefGoogle Scholar
  37. Nakamura BJ, Ebesutani C, Bernstein A, Chorpita BF (2009) A psychometric analysis of the child behavior checklist DSM-oriented scales. J Psychopathol Behav Assess 31(3):178–189CrossRefGoogle Scholar
  38. Nigg JT (2001) Is ADHD a disinhibitory disorder? Psychol Bull 127(5):571–598PubMedCrossRefGoogle Scholar
  39. Nigg JT, Blaskey LG, Huang-Pollock CL, Rappley MD (2002) Neuropsychological executive functions and DSM-IV ADHD subtypes. J Am Acad Child Adolesc Psychiatry 41(1):59–66PubMedCrossRefGoogle Scholar
  40. Nigg JT, Stavro G, Ettenhofer M, Hambrick DZ, Miller T, Henderson JM (2005) Executive functions and ADHD in adults: evidence for selective effects on ADHD symptom domains. J Abnorm Psychol 114(4):706–717PubMedCrossRefGoogle Scholar
  41. Nigg JT, Wong MM, Martel MM, Jester JM, Puttler LI, Glass JM, Zucker RA (2006) Poor response inhibition as a predictor of problem drinking and illicit drug use in adolescents at risk for alcoholism and other substance use disorders. J Am Acad Child Adolesc Psychiatry 45(4):468–475PubMedCrossRefGoogle Scholar
  42. Nooner KB, Colcombe S, Tobe R, Mennes M, Benedict M, Moreno A, Sikka S (2012) The NKI-Rockland sample: a model for accelerating the pace of discovery science in psychiatry. Front Neurosci 6:152PubMedPubMedCentralCrossRefGoogle Scholar
  43. Oosterlaan J, Sergeant JA (1998) Effects of reward and response cost on response inhibition in AD/HD, disruptive, anxious, and normal children. J Abnorm Child Psychol 26(3):161–174PubMedCrossRefGoogle Scholar
  44. Ostrander R, Weinfurt KP, Yarnold PR, August GJ (1998) Diagnosing attention deficit disorders with the behavioral assessment system for children and the child behavior checklist: test and construct validity analyses using optimal discriminant classification trees. J Consult Clin Psychol 66(4):660–667PubMedCrossRefGoogle Scholar
  45. Pitcher TM, Piek JP, Barrett NC (2002) Timing and force control in boys with attention deficit hyperactivity disorder: subtype differences and the effect of comorbid developmental coordination disorder. Hum Mov Sci 21(5–6):919–945PubMedCrossRefGoogle Scholar
  46. Pliszka SR (1989) Effect of anxiety on cognition, behavior, and stimulant response in ADHD. J Am Acad Child Adolesc Psychiatry 28:882–887PubMedCrossRefGoogle Scholar
  47. Pliszka SR (1992) Comorbidity of attention-deficit hyperactivity disorder and overanxious disorder. J Am Acad Child Adolesc Psychiatry 31:197–203PubMedCrossRefGoogle Scholar
  48. Pliszka SR, Hatch JP, Borcherding SH, Rogeness GA (1993) Classical conditioning in children with attention deficit hyperactivity disorder (ADHD) and anxiety disorders: a test of Quay’s model. J Abnorm Child Psychol 21:411–423PubMedCrossRefGoogle Scholar
  49. Ruf BM, Bessette KL, Pearlson GD, Stevens MC (2016) Effect of trait anxiety on cognitive test performance in adolescents with and without attention-deficit/hyperactivity disorder. J Clin Exp Neuropsychol 39:434–448PubMedCrossRefGoogle Scholar
  50. Rynn MA, Barber JP, Khalid-Khan S, Siqueland L, Dembiski M, McCarthy KS, Gallop R (2006) The psychometric properties of the MASC in a pediatric psychiatric sample. J Anxiety Disord 20(2):139–157PubMedCrossRefGoogle Scholar
  51. Schatz DB, Rostain AL (2006) ADHD with comorbid anxiety a review of the current literature. J Atten Disorders 10(2):141–149CrossRefGoogle Scholar
  52. Schmitz M, Cadore L, Paczko M, Kipper L, Chaves M, Rohde LA, Knijnik M (2002) Neuropsychological performance in DSM-IV ADHD subtypes: an exploratory study with untreated adolescents. Can J Psychiatry 47(9):863–869PubMedCrossRefGoogle Scholar
  53. Skirbekk B, Hansen BH, Oerbeck B, Kristensen H (2011) The relationship between sluggish cognitive tempo, subtypes of attention-deficit/hyperactivity disorder, and anxiety disorders. J Abnorm Child Psychol 39:513–525PubMedCrossRefGoogle Scholar
  54. Sonuga-Barke EJ (2002) Psychological heterogeneity in AD/HD—a dual pathway model of behaviour and cognition. Behav Brain Res 130(1–2):29–36PubMedCrossRefGoogle Scholar
  55. Sprague J, Verona E, Kalkhoff W, Kilmer A (2011) Moderators and mediators of the stress-aggression relationship: executive function and state anger. Emotion 11(1):61–73PubMedCrossRefGoogle Scholar
  56. Tannock R (2009) ADHD with anxiety disorders. In: Brown TE (ed) ADHD comorbidities: handbook for ADHD complications in children and adults. American Psychiatric Publishing, Washington, DC, pp 131–155Google Scholar
  57. Tannock R, Ickowicz A, Schachar R (1995) Differential effects of methylphenidate on working memory in ADHD children with and without comorbid anxiety. J Am Acad Child Adolesc Psychiatry 34:886–896PubMedCrossRefGoogle Scholar
  58. Toren P, Sadeh M, Wolmer L, Eldar S, Koren S, Weizman R, Laor N (2000) Neurocognitive correlates of anxiety disorders in children: a preliminary report. J Anxiety Disord 14:239–247PubMedCrossRefGoogle Scholar
  59. Valiente C, Eisenberg N, Spinrad TL, Haugen RG, Thompson MS, Kupfer A (2013) Effortful control and impulsivity as concurrent and longitudinal predictors of academic achievement. J Early Adolesc 33(7):946–972CrossRefGoogle Scholar
  60. Visu-Petra L, Cheie L, Benga O, Alloway TP (2010) Effects of anxiety on memory storage and updating in young children. Int J Behav Dev 35(1):38–47CrossRefGoogle Scholar
  61. Visu-Petra L, Stanciu O, Benga O, Miclea M, Cheie L (2014) Longitudinal and concurrent links between memory span, anxiety symptoms, and subsequent executive functioning in young children. Front Psychol 5:443PubMedPubMedCentralCrossRefGoogle Scholar
  62. Vloet TD, Konrad K, Herpertz-Dahlmann B, Polier GG, Gunther T (2010) Impact of anxiety disorders on attentional functions in children with ADHD. J Affect Disord 124:283–290PubMedCrossRefGoogle Scholar
  63. Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005) Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiat 57(11):1336–1346PubMedCrossRefGoogle Scholar
  64. Wodka EL, Loftis C, Mostofsky SH, Prahme C, Larson JCG, Denckla MB, Mahone EM (2008) Prediction of ADHD in boys and girls using the D–KEFS. Arch Clin Neuropsychol 23(3):283–293PubMedPubMedCentralCrossRefGoogle Scholar
  65. Young SE, Friedman NP, Miyake A, Willcutt EG, Corley RP, Haberstick BC, Hewitt JK (2009) Behavioral disinhibition: liability for externalizing spectrum disorders and its genetic and environmental relation to response inhibition across adolescence. J Abnorm Psychol 118(1):117–130PubMedPubMedCentralCrossRefGoogle Scholar
  66. Yurtbaşı P, Aldemir S, Teksin Bakır MG, Aktaş Ş, Ayvaz FB, Piştav Satılmış Ş, Münir K (2018) Comparison of neurological and cognitive deficits in children with ADHD and anxiety disorders. J Attention Disord 22(5):472–485CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of PsychologyLouisiana State UniversityBaton RougeUSA
  2. 2.Pennington Biomedical Research CenterBaton RougeUSA

Personalised recommendations