Skip to main content
Log in

Variability of ecological executive function in children and adolescents genetically at high risk for schizophrenia: a latent class analysis

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

Abstract

Executive impairments have been observed both in patients with schizophrenia and in their unaffected first-degree relatives. Very few studies have investigated neurocognitive subgroups in unaffected first-degree relatives and in healthy participants using data-driven methods. The study included a high-risk group consisting of 100 unaffected young offspring and siblings of patients with schizophrenia and 198 healthy controls, all aged between 9 and 23 years. Executive function, victimization, and emotional and behavioral problems of participants were assessed by a series of self-report scales. Neurocognitive subgroups were investigated using latent class analysis of executive function measures. Four neurocognitive clusters were identified: a good performance cluster, a good self-control cluster, a low self-control cluster, and a severe impairment cluster. Participants in severe impaired executive function cluster reported a significantly higher level of victimization and had more prominent emotional and behavioral problems than the good performance cluster. Neurocognitive differences between high-risk young people and healthy controls were driven by individuals who have severe and global, rather than selective, executive deficits. Our results may provide clues to an explanation of the mechanisms behind executive impairments in young individuals at genetic risk and help to identify new targets for early interventions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

EF:

Executive function

HR:

High risk

HC:

Healthy control

LCA:

Latent class analysis

LC:

Latent class

SPSS:

Statistical Package for Social Sciences

References

  1. Owen MJ, Sawa A, Mortensen PB (2016) Schizophrenia. Lancet 388(10039):86–97. https://doi.org/10.1016/s0140-6736(15)01121-6

    Article  PubMed  PubMed Central  Google Scholar 

  2. Greenberg DA (1992) There is more than one way to collect data for linkage analysis: what a study of epilepsy can tell us about linkage strategy for psychiatric disease. Arch Gen Psychiatry 49(9):745–750. https://doi.org/10.1001/archpsyc.1992.01820090073012

    Article  CAS  PubMed  Google Scholar 

  3. Owens EM, Bachman P, Glahn DC, Bearden CE (2016) Electrophysiological endophenotypes for schizophrenia. Harv Rev Psychiatry 24(2):129–147

    Article  PubMed  PubMed Central  Google Scholar 

  4. Turetsky BI, Calkins ME, Light GA, Olincy A, Radant AD, Swerdlow NR (2007) Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophr Bull 33(1):69–94. https://doi.org/10.1093/schbul/sbl060

    Article  PubMed  Google Scholar 

  5. Pinkham AE, Penn DL, Perkins DO, Lieberman J (2003) Implications for the neural basis of social cognition for the study of schizophrenia. Am J Psychiatry 160(5):815–824

    Article  PubMed  Google Scholar 

  6. Bhojraj TS, Diwadkar VA, Sweeney JA, Prasad KM, Eack SM, Montrose DM, Keshavan MS (2010) Longitudinal alterations of executive function in non-psychotic adolescents at familial risk for schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 34(3):469–474

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lieberman JA, Perkins D, Belger A, Chakos M, Jarskog F, Boteva K, Gilmore J (2001) The early stages of schizophrenia: speculations on pathogenesis, pathophysiology, and therapeutic approaches. Biol Psychiatry 50(11):884–897

    Article  CAS  PubMed  Google Scholar 

  8. Seidman LJ, Giuliano AJ, Smith CW, Stone WS, Glatt SJ, Meyer E, Faraone SV, Tsuang MT, Cornblatt B (2006) Neuropsychological functioning in adolescents and young adults at genetic risk for schizophrenia and affective psychoses: results from the Harvard and hillside adolescent high risk studies. Schizophr Bull 32(3):507–524. https://doi.org/10.1093/schbul/sbj078

    Article  PubMed  PubMed Central  Google Scholar 

  9. Kremen WS, Hoff AL (2004) Neurocognitive deficits in the biological relatives of individuals with schizophrenia. Early clinical intervention and prevention in schizophrenia. Springer, Berlin, pp 133–158

    Book  Google Scholar 

  10. Snitz BE, MacDonald AW, Carter CS (2006) Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophr Bull 32(1):179–194

    Article  PubMed  PubMed Central  Google Scholar 

  11. Maziade M, Rouleau N, Gingras N, Boutin P, Paradis M-E, Jomphe V, Boutin J, Létourneau K, Gilbert E, Lefebvre A-A (2009) Shared neurocognitive dysfunctions in young offspring at extreme risk for schizophrenia or bipolar disorder in eastern quebec multigenerational families. Schizophr Bull 35(5):919–930

    Article  PubMed  Google Scholar 

  12. Li Y, Cao F, Shao D, Xue J (2014) Ecological assessment of executive functions in adolescents genetically at high risk for schizophrenia. Compr Psychiatry 55(6):1350–1357. https://doi.org/10.1016/j.comppsych.2014.04.009

    Article  PubMed  Google Scholar 

  13. Wagshal D, Knowlton BJ, Cohen JR, Poldrack RA, Bookheimer SY, Bilder RM, Asarnow RF (2014) Impaired automatization of a cognitive skill in first-degree relatives of patients with schizophrenia. Psychiatry Res 215(2):294–299

    Article  PubMed  Google Scholar 

  14. Keefe R (2006) Cognitive deficits in patients with schizophrenia: effects and treatment. J Clin Psychiatry 68:8–13

    Google Scholar 

  15. McAuley T, Chen S, Goos L, Schachar R, Crosbie J (2010) Is the behavior rating inventory of executive function more strongly associated with measures of impairment or executive function? J Int Neuropsychol Soc 16(03):495–505

    Article  PubMed  Google Scholar 

  16. Organization WH (1992) The ICD-10 classification of mental and behavioural disorders: clinical descriptions and diagnostic guidelines. World Health Organization, Geneva

    Google Scholar 

  17. Guy SC, Gioia GA, Isquith PK (2004) Behavior rating inventory of executive function: self-report version. Psychological Assessment Resources, Lutz

    Google Scholar 

  18. Gioia GA, Isquith PK, Guy SC, Kenworthy L (2000) Test review behavior rating inventory of executive function. Child Neuropsychol 6(3):235–238

    Article  Google Scholar 

  19. Finkelhor D, Hamby SL, Ormrod R, Turner H (2005) The Juvenile Victimization Questionnaire: reliability, validity, and national norms. Child Abuse Negl 29(4):383–412

    Article  PubMed  Google Scholar 

  20. Chan KL (2013) Victimization and poly-victimization among school-aged Chinese adolescents: prevalence and associations with health. Prev Med 56(3–4):207–210. https://doi.org/10.1016/j.ypmed.2012.12.018

    Article  PubMed  Google Scholar 

  21. Goodman R (2001) Psychometric properties of the strengths and difficulties questionnaire. J Am Acad Child Adolesc Psychiatry 40(11):1337–1345

    Article  CAS  PubMed  Google Scholar 

  22. Nunnally J, Bernstein I (1994) Psychometric theory, 3rd edn. McGraw-Hill, New York

    Google Scholar 

  23. Porcu M, Giambona F (2017) Introduction to latent class analysis with applications. J Early Adolesc 37(1):129–158

    Article  Google Scholar 

  24. Butera NM, Lanza ST, Coffman DL (2014) A framework for estimating causal effects in latent class analysis: is there a causal link between early sex and subsequent profiles of delinquency? Prev Sci 15(3):397–407

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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):49–100. https://doi.org/10.1006/cogp.1999.0734

    Article  CAS  PubMed  Google Scholar 

  26. Lanza ST, Rhoades BL (2013) Latent class analysis: an alternative perspective on subgroup analysis in prevention and treatment. Prev Sci 14(2):157–168

    Article  PubMed  PubMed Central  Google Scholar 

  27. Magidson J, Vermunt J (2002) Latent class models for clustering: a comparison with K-means. Can J Mark Res 20(1):36–43

    Google Scholar 

  28. Roth RM, Gioia GA (2005) Behavior rating inventory of executive function—adult version. Psychological Assessment Resources, Lutz

    Google Scholar 

  29. Seaton BE, Goldstein G, Allen DN (2001) Sources of heterogeneity in schizophrenia: the role of neuropsychological functioning. Neuropsychol Rev 11(1):45–67

    Article  CAS  PubMed  Google Scholar 

  30. Fatemi SH, Folsom TD (2009) The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull 35(3):528–548. https://doi.org/10.1093/schbul/sbn187

    Article  PubMed  PubMed Central  Google Scholar 

  31. Keshavan M, Gilbert A, Diwadkar V (2006) Neurodevelopmental theories. The American Psychiatric Publishing textbook of schizophrenia. American Psychiatric Publishing Inc, Washington, DC, pp 69–84

    Google Scholar 

  32. Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, Kenny LC, Mortensen PB (2008) Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65(2):146–152

    Article  PubMed  Google Scholar 

  33. Brown AS (2012) Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol 72(10):1272–1276

    Article  PubMed  PubMed Central  Google Scholar 

  34. Khandaker G, Zimbron J, Lewis G, Jones P (2013) Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies. Psychol Med 43(02):239–257

    Article  CAS  PubMed  Google Scholar 

  35. Brown AS (2006) Prenatal infection as a risk factor for schizophrenia. Schizophr Bull 32(2):200–202

    Article  PubMed  PubMed Central  Google Scholar 

  36. Zalla T, Joyce C, Szöke A, Schürhoff F, Pillon B, Komano O, Perez-Diaz F, Bellivier F, Alter C, Dubois B, Rouillon F, Houde O, Leboyer M (2004) Executive dysfunctions as potential markers of familial vulnerability to bipolar disorder and schizophrenia. Psychiatry Res 121(3):207–217. https://doi.org/10.1016/S0165-1781(03)00252-X

    Article  PubMed  Google Scholar 

  37. Bora E, Hıdıroğlu C, Özerdem A, Kaçar ÖF, Sarısoy G, Arslan FC, Aydemir Ö, Tas ZC, Vahip S, Atalay A (2016) Executive dysfunction and cognitive subgroups in a large sample of euthymic patients with bipolar disorder. Eur Neuropsychopharmacol 26(8):1338–1347

    Article  CAS  PubMed  Google Scholar 

  38. Vasile C (2013) Cognitive reserve and cortical plasticity. Procedia Soc Behav Sci 78:601–604. https://doi.org/10.1016/j.sbspro.2013.04.359

    Article  Google Scholar 

  39. Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8(03):448–460

    Article  PubMed  Google Scholar 

  40. Biederman J, Monuteaux MC, Doyle AE, Seidman LJ, Wilens TE, Ferrero F, Morgan CL, Faraone SV (2004) Impact of executive function deficits and attention-deficit/hyperactivity disorder (ADHD) on academic outcomes in children. J Consult Clin Psychol 72(5):757

    Article  PubMed  Google Scholar 

  41. Tolman AW, Kurtz MM (2012) Neurocognitive predictors of objective and subjective quality of life in individuals with schizophrenia: a meta-analytic investigation. Schizophr Bull 38(2):304–315. https://doi.org/10.1093/schbul/sbq077

    Article  PubMed  Google Scholar 

  42. Fett A-KJ, Viechtbauer W, Dominguez M-d-G, Penn DL, van Os J, Krabbendam L (2011) The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neurosci Biobehav Rev 35(3):573–588. https://doi.org/10.1016/j.neubiorev.2010.07.001

    Article  PubMed  Google Scholar 

  43. Lewis GJ, Asbury K, Plomin R (2017) Externalizing problems in childhood and adolescence predict subsequent educational achievement but for different genetic and environmental reasons. J Child Psychol Psychiatry Allied Discip 58(3):292–304. https://doi.org/10.1111/jcpp.12655

    Article  Google Scholar 

  44. Beratis S, Hoidas GJ S (1994) Age at onset in subtypes of schizophrenic disorders. Schizophr Bull 20(2):287–296

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors extend their gratitude to all the participants for their time and effort. This study was financially supported by the Natural Science Foundation of Shandong Province (No. ZR2013HM087). All authors had critically reviewed and contributed to manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fenglin Cao.

Ethics declarations

Conflict of interest

The authors have declared that they have no competing or potential conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 609 KB)

Supplementary material 2 (DOCX 19 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, M., Li, Y., Sun, J. et al. Variability of ecological executive function in children and adolescents genetically at high risk for schizophrenia: a latent class analysis. Eur Child Adolesc Psychiatry 28, 237–245 (2019). https://doi.org/10.1007/s00787-018-1168-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00787-018-1168-2

Keywords

Navigation