Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T06:21:22.521Z Has data issue: false hasContentIssue false
  • English
  • Français

The impact of parent socio-economic status on executive functioning and cortical morphology in individuals with schizophrenia and healthy controls

Published online by Cambridge University Press:  19 July 2013

R. A. Yeo ,
D. Martinez ,
J. Pommy ,
S. Ehrlich ,
S. C. Schulz ,
B.-C. Ho ,
J. R. Bustillo  and
V. D. Calhoun
R. A. Yeo*
Affiliation:
Department of Psychology, University of New Mexico, Albuquerque, NM, USA The Mind Research Network, Albuquerque, NM, USA
D. Martinez
Affiliation:
Department of Psychology, University of New Mexico, Albuquerque, NM, USA
J. Pommy
Affiliation:
Department of Psychology, University of New Mexico, Albuquerque, NM, USA
S. Ehrlich
Affiliation:
Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, USA Department of Child and Adolescent Psychiatry, University Hospital Carl Gustav Carus, Dresden University of Technology, Dresden, Germany
S. C. Schulz
Affiliation:
Department of Psychiatry, University of Minnesota, Minneapolis, MN, USA
B.-C. Ho
Affiliation:
Department of Psychiatry, Carver College of Medicine, University of Iowa, Iowa City, IA, USA
J. R. Bustillo
Affiliation:
The Mind Research Network, Albuquerque, NM, USA Department of Psychiatry, University of New Mexico, Albuquerque, NM, USA
V. D. Calhoun
Affiliation:
The Mind Research Network, Albuquerque, NM, USA Department of Electrical and Computer Engineering, University of New Mexico, Albuquerque, NM, USA
*
* Address for correspondence: R. A. Yeo, Ph.D., Department of Psychology, University of New Mexico, Albuquerque, NM, USA. (Email: ryeo@unm.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Relatively lower executive functioning is characteristic of individuals with schizophrenia. As low socio-economic status (SES) early in life (i.e. parent SES) has been linked with lower executive skills in healthy children, we hypothesized that parental SES (pSES) would be more strongly related to executive functioning in individuals with schizophrenia than in controls and have a greater impact on prefrontal cortical morphology.

Method

Healthy controls (n = 125) and individuals with schizophrenia (n = 102) completed tests assessing executive functioning and intelligence. The groups were matched on pSES, which was evaluated with the Hollingshead–Redlich scale. A principal components analysis (PCA) was conducted on 10 variables from six executive tests, yielding three specific components (fluency, planning and response inhibition). Voxel-based morphometry (VBM) was used to evaluate effects of pSES on gray matter (GM) concentration.

Results

Lower pSES was associated with lower scores across the three executive functioning components, and a significant group by pSES interaction was observed such that low pSES, in particular, affected individuals with schizophrenia. These effects remained significant when intellectual ability, education and self-SES (sSES) were added as covariates. VBM revealed that lower pSES was associated with reduced GM volume in several anterior brain regions, especially the superior frontal gyrus, in patients but not in controls.

Conclusions

These findings suggest that individuals with schizophrenia may be particularly vulnerable to the adverse impact of low pSES, in terms of both lower executive skills and reduced anterior GM volumes.

Keywords

Executive functionfrontal lobesschizophreniasocio-economic statusvoxel-based morphometry
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 6 , April 2014 , pp. 1257 - 1265
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andreasen, NC (1983). The Scale for the Assessment of Positive Symptoms. University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC, Flaum, M, Arndt, S (1992). The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. Archives of General Psychiatry 49, 615–623.Google Scholar
Ashburner, J, Friston, KJ (2005). Unified segmentation. NeuroImage 26, 839–851.Google Scholar
Bradley, RH, Corwyn, RF (2002). Socioeconomic status and child development. Annual Review of Psychology 53, 371–399.Google Scholar
Buda, M, Fornito, A, Bergstrom, ZM, Simons, JS (2011). A specific brain structural basis for individual differences in reality monitoring. Journal of Neuroscience 31, 14308–14313.Google Scholar
Chan, SK, Chan, KK, Lam, MM, Chiu, CP, Hui, CL, Wong, GH, Chang, WC, Chen, EY (2012). Clinical and cognitive correlates of insight in first-episode schizophrenia. Schizophrenia Research 135, 40–45.CrossRefGoogle ScholarPubMed
Cohen, RA, Grieve, S, Hoth, KF, Paul, RH, Sweet, L, Tate, D, Gunstad, J, Stroud, L, McCaffery, J, Hitsman, B, Niaura, R, Clark, CR, MacFarlane, A, Bryant, R, Gordon, E, Williams, LM (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry 59, 975–982.Google Scholar
Delis, D, Kaplan, E, Kramer, J (2001). The Delis-Kaplan Executive Function System. Psychological Corporation: San Antonio, TX.Google Scholar
Dickinson, D, Goldberg, TE, Gold, JM, Elvevag, B, Weinberger, DR (2011). Cognitive factor structure and invariance in people with schizophrenia, their unaffected siblings, and controls. Schizophrenia Bulletin 37, 1157–1167.Google Scholar
Eisenberg, DP, Berman, KF (2010). Executive function, neural circuitry, and genetic mechanisms in schizophrenia. Neuropsychopharmacology 35, 258–277.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patent Edition (SCID-I/P) and Non-patient Edition (SCID-N/P). Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Friedman, NP, Miyake, A, Young, SE, Defries, JC, Corley, RP, Hewitt, JK (2008). Individual differences in executive functions are almost entirely genetic in origin. Journal of Experimental Psychology. General 137, 201–225.Google Scholar
Goghari, VM, Sponheim, SR, MacDonald, AW 3rd (2010). The functional neuroanatomy of symptom dimensions in schizophrenia: a qualitative and quantitative review of a persistent question. Neuroscience and Biobehavioral Reviews 34, 468–486.Google Scholar
Gottesman, II, Gould, TD (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. American Journal of Psychiatry 160, 636–645.CrossRefGoogle ScholarPubMed
Habets, P, Marcelis, M, Gronenschild, E, Drukker, M, van Os, J; Genetic Risk and Outcome of Psychosis (G.R.O.U.P) (2011). Reduced cortical thickness as an outcome of differential sensitivity to environmental risks in schizophrenia. Biological Psychiatry 69, 487–494.Google Scholar
Hackman, DA, Farah, MJ, Meaney, MJ (2010). Socioeconomic status and the brain: mechanistic insights from human and animal research. Nature Reviews Neuroscience 11, 651–659.CrossRefGoogle ScholarPubMed
Hagmann, P, Cammoun, L, Gigandet, X, Meuli, R, Honey, CJ, Wedeen, V, Sporns, O (2008). Mapping the structural core of human cerebral cortex. Plos Biology 6, 1479–1493.Google Scholar
Hanscombe, KB, Trzaskowski, M, Haworth, CM, Davis, OS, Dale, PS, Plomin, R (2012). Socioeconomic status (SES) and children's intelligence (IQ): in a UK-representative sample SES moderates the environmental, not genetic, effect on IQ. Plos One 7, e30320.Google Scholar
Hanson, JL, Chandra, A, Wolfe, BL, Pollak, SD (2011). Association between income and the hippocampus. PLoS One 6, e18712.Google Scholar
Haworth, CM, Wright, MJ, Luciano, M, Martin, NG, de Geus, EJ, van Beijsterveldt, CE, Bartels, M, Posthuma, D, Boomsma, DI, Davis, OSP, Kovas, Y, Corley, RP, Defries, JC, Hewitt, JK, Olson, RK, Rhea, SA, Wadsworth, SJ, Iacono, WG, McGue, M, Thompson, LA, Hart, SA, Petrill, SA, Lubinski, D, Plomin, R (2010). The heritability of general cognitive ability increases linearly from childhood to young adulthood. Molecular Psychiatry 15, 1112–1120.Google Scholar
Hofer, A, Bodner, T, Kaufmann, A, Kemmler, G, Mattarei, U, Pfaffenberger, NM, Rettenbacher, MA, Trebo, E, Yalcin, N, Fleischhacker, WW (2011). Symptomatic remission and neurocognitive functioning in patients with schizophrenia. Psychological Medicine 41, 2131–2139.Google Scholar
Hollingshead, AB, Redlich, FC (1958). Social Class and Mental Illness: A Community Study. Wiley & Sons: New York.CrossRefGoogle Scholar
Hutton, SB, Puri, BK, Duncan, LJ, Robbins, TW, Barnes, TRE, Joyce, EM (1998). Executive function in first-episode schizophrenia. Psychological Medicine 28, 463–473.CrossRefGoogle ScholarPubMed
LaPointe, LL, Heald, GR, Stierwalt, JA, Kemker, BE, Maurice, T (2007). Effects of auditory distraction on cognitive processing of young adults. Journal of Attention Disorders 10, 398–409.Google Scholar
Lezak, MD, Howieson, DB, Bigler, ED, Tranel, D (2012). Neuropsychological Assessment, 5th edn. Oxford University Press: New York.Google Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 1233–1239.Google Scholar
McNeil, TF, Cantor-Graae, E, Weinberger, DR (2000). Relationship of obstetric complications and differences in size of brain structures in monozygotic twin pairs discordant for schizophrenia. American Journal of Psychiatry 157, 203–212.Google Scholar
Minzenberg, MJ, Laird, AR, Thelen, S, Carter, CS, Glahn, DC (2009). Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Archives of General Psychiatry 66, 811–822.Google Scholar
Nisbett, RE, Aronson, J, Blair, C, Dickens, W, Flynn, J, Halpern, DF, Turkheimer, E (2012). Intelligence new findings and theoretical developments. American Psychologist 67, 130–159.Google Scholar
Puig, O, Penades, R, Baeza, I, Sanchez-Gistau, V, De La Serna, E, Fonrodona, L, Andres-Perpina, S, Bernardo, M, Castro-Fornieles, J (2012). Processing speed and executive functions predict real-world everyday living skills in adolescents with early-onset schizophrenia. European Child and Adolescent Psychiatry 21, 315–326.Google Scholar
Segall, JM, Turner, JA, van Erp, TGM, White, T, Bockholt, HJ, Gollub, RL, Ho, BC, Magnotta, V, Jung, RE, McCarley, RW, Schulz, SC, Lauriello, J, Clark, VP, Voyvodic, JT, Diaz, MT, Calhoun, VD (2009). Voxel-based morphometric multisite collaborative study on schizophrenia. Schizophrenia Bulletin 35, 82–95.Google Scholar
Shallice, T (1982). Specific impairments of planning. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 298, 199–209.Google Scholar
Snitz, BE, MacDonald, AW 3rd, Carter, CS (2006). Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophrenia Bulletin 32, 179–194.Google Scholar
Sponheim, SR, Jung, RE, Seidman, LJ, Mesholam-Gately, RI, Manoach, DS, O'Leary, DS, Ho, BC, Andreasen, NC, Lauriello, J, Schulz, SC (2010). Cognitive deficits in recent-onset and chronic schizophrenia. Journal of Psychiatric Research 44, 421–428.Google Scholar
van den Heuvel, MP, Mandl, RC, Stam, CJ, Kahn, RS, Hulshoff Pol, HE (2010). Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. Journal of Neuroscience 30, 15915–15926.CrossRefGoogle ScholarPubMed
van den Heuvel, MP, Sporns, O (2011). Rich-club organization of the human connectome. Journal of Neuroscience 31, 15775–15786.Google Scholar
van Harmelen, AL, van Tol, MJ, van der Wee, NJA, Veltman, DJ, Aleman, A, Spinhoven, P, van Buchem, MA, Zitman, FG, Penninx, BWJH, Elzinga, BM (2010). Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biological Psychiatry 68, 832–838.Google Scholar
van Os, J, Kenis, G, Rutten, B (2010). The environment and schizophrenia. Nature Perspectives 468, 203–212.Google ScholarPubMed
Wechsler, D (1997). Wechsler Adult Intelligence Scale, Third Edition (WAIS-III). Psychological Corporation: San Antonio, TX.Google Scholar
Welch, KA, McIntosh, AM, Job, DE, Whalley, HC, Moorhead, TW, Hall, J, Owens, DGC, Lawrie, SM, Johnstone, EC (2011). The impact of substance use on brain structure in people at high risk of developing schizophrenia. Schizophrenia Bulletin 37, 1066–1076.Google Scholar
Whitwell, JL (2009). Voxel-based morphometry: an automated technique for assessing structural changes in the brain. Journal of Neuroscience 29, 9661–9664.Google Scholar
Winkler, AM, Kochunov, P, Blangero, J, Almasy, L, Zilles, K, Fox, PT, Duggirala, R, Glahn, DC (2010). Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. NeuroImage 53, 1135–1146.Google Scholar
Yeo, RA, Gangestad, SW, Edgar, C, Thoma, R (1999). The evolutionary genetic underpinnings of schizophrenia: the developmental instability model. Schizophrenia Research 39, 197–206.Google Scholar
Yeo, RA, Gangestad, SW, Thoma, RJ (2007). Developmental instability and individual variation in brain development: implications for the origin of neurodevelopmental disorders. Current Directions in Psychological Science 16, 245–249.Google Scholar
Zink, CF, Tong, YX, Chen, Q, Bassett, DS, Stein, JL, Meyer-Lindenberg, A (2008). Know your place: neural processing of social hierarchy in humans. Neuron 58, 273–283.Google Scholar