Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T01:00:52.266Z Has data issue: false hasContentIssue false
  • English
  • Français

Proxy measures of premortem cognitive aptitude in postmortem subjects with schizophrenia

Published online by Cambridge University Press:  14 March 2019

Jill R. Glausier ,
Mary Ann Kelly ,
Samantha Salem ,
Kehui Chen  and
David A. Lewis Open the ORCID record for David A. Lewis [Opens in a new window]
Jill R. Glausier
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Mary Ann Kelly
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Samantha Salem
Affiliation:
Department of Psychiatry, University of Buffalo, Buffalo, NY, USA
Kehui Chen
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA Department of Statistics, University of Pittsburgh, Pittsburgh, PA, USA
David A. Lewis*
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA
*
Author for correspondence: David A. Lewis, E-mail: lewisda@upmc.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Postmortem human brain studies provide the molecular, cellular, and circuitry levels of resolution essential for the development of mechanistically-novel interventions for cognitive deficits in schizophrenia. However, the absence of measures of premortem cognitive aptitude in postmortem subjects has presented a major challenge to interpreting the relationship between the severity of neural alterations and cognitive deficits within the same subjects.

Methods

To begin addressing this challenge, proxy measures of cognitive aptitude were evaluated in postmortem subjects (N = 507) meeting criteria for schizophrenia, major depressive or bipolar disorder, and unaffected comparison subjects. Specifically, highest levels of educational and occupational attainment of the decedent and their parents were obtained during postmortem psychological autopsies.

Results

Consistent with prior findings in living subjects, subjects with schizophrenia had the lowest educational and occupational attainment relative to all other subject groups, and they also failed to show the generational improvement in attainment observed in all other subject groups.

Conclusions

Educational and occupational attainment data obtained during postmortem psychological autopsies can be used as proxy measures of premortem cognitive function to interrogate the neural substrate of cognitive dysfunction in schizophrenia.

Keywords

Bipolar disordercognitioncognitive impairmenteducationfirst-degree relativemajor depressive disorderoccupationprobandpsychological autopsyschizoaffective disorder
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 3 , February 2020 , pp. 507 - 514
Copyright
Copyright © Cambridge University Press 2019

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

American Psychiatric Association (1994) DSM-IV. Diagnostic and Statistical Manual of Mental Disorders. 4th Edn.Washington, DC: American Psychiatric Association.Google Scholar
American Psychological Association (2019) Education and Socioeconomic Status. Resources and Publications [Online]. https://www.apa.org/pi/ses/resources/publications/education (Accessed 2019).Google Scholar
Aminoff, SR, Hellvin, T, Lagerberg, TV, Berg, AO, Andreassen, OA and Melle, I (2013) Neurocognitive features in subgroups of bipolar disorder. Bipolar Disorders 15, 272–283.CrossRefGoogle ScholarPubMed
Baldessarini, RJ, Tondo, L, Vazquez, GH, Undurraga, J, Bolzani, L, Yildiz, A, Khalsa, HM, Lai, M, Lepri, B, Lolich, M, Maffei, PM, Salvatore, P, Faedda, GL, Vieta, E and Tohen, M (2012) Age at onset versus family history and clinical outcomes in 1665 international bipolar-I disorder patients. World Psychiatry 11, 40–46.CrossRefGoogle ScholarPubMed
Beneyto, M, Sibille, E and Lewis, DA (2009) Human postmortem brain research in mental illness syndromes. In Charney, DS and Nestler, EJ (eds), Neurobiology of Mental Illness. New York: Oxford University Press, pp. 202–214.Google Scholar
Bianchi, D, Gordon, J and Koroshetz, W (2017) The NIH NeuroBioBank: addressing the urgent need for brain donation [Online]. Published July 5, 2017. https://www.ninds.nih.gov/News-Events/Directors-Messages/All-Directors-Messages/NIH-NeuroBioBank-Addressing-Urgent-Need-Brain.Google Scholar
Bureau, USC. Table A-2. Percent of people 25 years and over who have completed high school or college, by race, Hispanic origin and sex: selected years 1940 to 2016. https://www.census.gov/data/tables/2016/demo/education-attainment/cps-detailed-tables.htmlGoogle Scholar
Cella, M, Stahl, D, Morris, S, Keefe, RSE, Bell, MD and Wykes, T (2017) Effects of cognitive remediation on negative symptoms dimensions: exploring the role of working memory. Psychological Medicine 4, 1–9.Google Scholar
Couture, SM, Granholm, EL and Fish, SC (2011) A path model investigation of neurocognition, theory of mind, social competence, negative symptoms and real-world functioning in schizophrenia. Schizophrenia Research 125, 152–160.CrossRefGoogle Scholar
Deary, IJ, Strand, S, Smith, PD and Fernandes, C (2007) Intelligence and educational achievement. Intelligence 35, 13–21.CrossRefGoogle Scholar
Deep-Soboslay, A, Akil, M, Martin, CE, Bigelow, LB, Herman, MM, Hyde, TM and Kleinman, JE (2005) Reliability of psychiatric diagnosis in postmortem research. Biological Psychiatry 57, 96–101.CrossRefGoogle ScholarPubMed
Deep-Soboslay, A, Benes, FM, Haroutunian, V, Ellis, JK, Kleinman, JE and Hyde, TM (2011) Psychiatric brain banking: three perspectives on current trends and future directions. Biological Psychiatry 69, 104–112.CrossRefGoogle ScholarPubMed
Depp, CA, Davis, CE, Mittal, D, Patterson, TL and Jeste, DV (2006) Health-related quality of life and functioning of middle-aged and elderly adults with bipolar disorder. Journal of Clinical Psychiatry 67, 215–221.CrossRefGoogle ScholarPubMed
Duckworth, AL, Quinn, PD, Lynam, DR, Loeber, R and Stouthamer-Loeber, M (2011) Role of test motivation in intelligence testing. Proceedings of the National Academy of Sciences of the USA 108, 7716–7720.CrossRefGoogle ScholarPubMed
Fervaha, G, Foussias, G, Agid, O and Remington, G (2014) Motivational and neurocognitive deficits are central to the prediction of longitudinal functional outcome in schizophrenia. Acta Psychiatrica Scandinavica 130, 290–299.CrossRefGoogle Scholar
Green, MF (2016) Impact of cognitive and social cognitive impairment on functional outcomes in patients with schizophrenia. Journal of Clinical Psychiatry 77(suppl. 2), 8–11.CrossRefGoogle ScholarPubMed
Green, MF, Kern, RS and Heaton, RK (2004) Longitudinal studies of cognition and functional outcome in schizophrenia: implications for MATRICS. Schizophrenia Research 72, 41–51.CrossRefGoogle ScholarPubMed
Hackman, DA, Farah, MJ and Meaney, MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nature Reviews: Neuroscience 11, 651–659.CrossRefGoogle ScholarPubMed
Harvey, PD (2011) Mood symptoms, cognition, and everyday functioning: in major depression, bipolar disorder, and schizophrenia. Innovations in Clinical Neuroscience 8, 14–18.Google Scholar
Harvey, PD, Koren, D, Reichenberg, A and Bowie, CR (2006) Negative symptoms and cognitive deficits: what is the nature of their relationship? Schizophrenia Bulletin 32, 250–258.CrossRefGoogle ScholarPubMed
Hollingshead, AB (1975) Four Factor Index of Social Status (dissertation). Yale University.Google Scholar
Humphries, C, Mortimer, A, Hirsch, S and De Belleroche, J (1996) NMDA receptor mRNA correlation with antemortem cognitive impairment in schizophrenia. Neuroreport 7, 2051–2055.CrossRefGoogle Scholar
Immonen, J, Jaaskelainen, E, Korpela, H and Miettunen, J (2017) Age at onset and the outcomes of schizophrenia: a systematic review and meta-analysis. Early Intervention in Psychiatry 11, 453–460.CrossRefGoogle ScholarPubMed
Jackson, M (2006) Personality traits and occupational attainment. European Sociological Review 22, 187–199.CrossRefGoogle Scholar
Joslyn, C, Hawes, DJ, Hunt, C and Mitchell, PB (2016) Is age of onset associated with severity, prognosis, and clinical features in bipolar disorder? A meta-analytic review. Bipolar Disorders 18, 389–403.CrossRefGoogle ScholarPubMed
Karpov, B, Joffe, G, Aaltonen, K, Suvisaari, J, Baryshnikov, I, Naatanen, P, Koivisto, M, Melartin, T, Oksanen, J, Suominen, K, Heikkinen, M and Isometsa, E (2017) Level of functioning, perceived work ability, and work status among psychiatric patients with major mental disorders. European Psychiatry 44, 83–89.CrossRefGoogle ScholarPubMed
Keefe, RS and Fenton, WS (2007) How should DSM-V criteria for schizophrenia include cognitive impairment? Schizophrenia Bulletin 33, 912–920.CrossRefGoogle ScholarPubMed
Keefe, RS and Harvey, PD (2012) Cognitive impairment in schizophrenia. Handbook of Experimental Pharmacology 213, 11–37.CrossRefGoogle Scholar
Keefe, RS, Eesley, CE and Poe, MP (2005) Defining a cognitive function decrement in schizophrenia. Biological Psychiatry 57, 688–691.CrossRefGoogle Scholar
Kelly, TM and Mann, JJ (1996) Validity of DSM-III-R diagnosis by psychological autopsy: a comparison with clinician ante-mortem diagnosis. Acta Psychiatrica Scandinavica 94, 337–343.CrossRefGoogle ScholarPubMed
Kendler, KS, Ohlsson, H, Mezuk, B, Sundquist, JO and Sundquist, K (2016) Observed cognitive performance and deviation from familial cognitive aptitude at age 16 years and ages 18 to 20 years and risk for schizophrenia and bipolar illness in a Swedish National Sample. JAMA Psychiatry 73, 465–471.CrossRefGoogle Scholar
Komarraju, M and Karau, SJ (2005) The relationship between the big five personality traits and academic motivation. Personality and Individual Differences 39, 557–567.CrossRefGoogle Scholar
Krapohl, E, Rimfeld, K, Shakeshaft, NG, Trzaskowski, M, Mcmillan, A, Pingault, JB, Asbury, K, Harlaar, N, Kovas, Y, Dale, PS and Plomin, R (2014) The high heritability of educational achievement reflects many genetically influenced traits, not just intelligence. Proceedings of the National Academy of Sciences of the USA 111, 15273–8.CrossRefGoogle Scholar
Le Hellard, S, Wang, Y, Witoelar, A, Zuber, V, Bettella, F, Hugdahl, K, Espeseth, T, Steen, VM, Melle, I, Desikan, R, Schork, AJ, Thompson, WK, Dale, AM, Djurovic, S and Andreassen, OA (2017) Identification of gene loci that overlap between schizophrenia and educational attainment. Schizophrenia Bulletin 43, 654–664.Google ScholarPubMed
Leboyer, M, Henry, C, Paillere-Martinot, ML and Bellivier, F (2005) Age at onset in bipolar affective disorders: a review. Bipolar Disorders 7, 111–118.CrossRefGoogle ScholarPubMed
Lewis, DA (2002) The human brain revisited: opportunities and challenges in postmortem studies of psychiatric disorders. Neuropsychopharmacology 26, 143–154.CrossRefGoogle ScholarPubMed
Maccabe, JH, Lambe, MP, Cnattingius, S, Sham, PC, David, AS, Reichenberg, A, Murray, RM and Hultman, CM (2010) Excellent school performance at age 16 and risk of adult bipolar disorder: national cohort study. British Journal of Psychiatry 196, 109–115.CrossRefGoogle ScholarPubMed
Martin-Ruiz, CM, Haroutunian, VH, Long, P, Young, AH, Davis, KL, Perry, EK and Court, JA (2003) Dementia rating and nicotinic receptor expression in the prefrontal cortex in schizophrenia. Biological Psychiatry 54, 1222–1233.CrossRefGoogle Scholar
Martinez-Aran, A, Vieta, E, Torrent, C, Sanchez-Moreno, J, Goikolea, JM, Salamero, M, Malhi, GS, Gonzalez-Pinto, A, Daban, C, Alvarez-Grandi, S, Fountoulakis, K, Kaprinis, G, Tabares-Seisdedos, R and Ayuso-Mateos, JL (2007) Functional outcome in bipolar disorder: the role of clinical and cognitive factors. Bipolar Disorders 9, 103–113.CrossRefGoogle ScholarPubMed
Mcgurk, SR and Meltzer, HY (2000) The role of cognition in vocational functioning in schizophrenia. Schizophrenia Research 45, 175–184.CrossRefGoogle Scholar
Menezes, NM, Arenovich, T and Zipursky, RB (2006) A systematic review of longitudinal outcome studies of first-episode psychosis. Psychological Medicine 36, 1349–1362.CrossRefGoogle ScholarPubMed
Milev, P, Ho, BC, Arndt, S and Andreasen, NC (2005) Predictive values of neurocognition and negative symptoms on functional outcome in schizophrenia: a longitudinal first-episode study with 7-year follow-up. American Journal of Psychiatry 162, 495–506.CrossRefGoogle ScholarPubMed
Nuechterlein, KH, Ventura, J, Subotnik, KL, Hayata, JN, Medalia, A and Bell, MD (2014) Developing a cognitive training strategy for first-episode schizophrenia: integrating bottom-up and top-down approaches. American Journal of Psychiatric Rehabilitation 17, 225–253.CrossRefGoogle ScholarPubMed
Peters, A, Sylvia, LG, Magalhaes, PV, Miklowitz, DJ, Frank, E, Otto, MW, Hansen, NS, Dougherty, DD, Berk, M, Nierenberg, AA and Deckersbach, T (2014) Age at onset, course of illness and response to psychotherapy in bipolar disorder: results from the Systematic Treatment Enhancement Program for Bipolar Disorder (STEP-BD). Psychological Medicine 44, 3455–3467.CrossRefGoogle Scholar
Poropat, AE (2009) A meta-analysis of the five-factor model of personality and academic performance. Psychological Bulletin 135, 322–338.CrossRefGoogle Scholar
Purohit, DP, Perl, DP, Haroutunian, V, Powchik, P, Davidson, M and Davis, KL (1998) Alzheimer disease and related neurodegenerative diseases in elderly patients with schizophrenia: a postmortem neuropathologic study of 100 cases. Archives of General Psychiatry 55, 205–211.CrossRefGoogle ScholarPubMed
Rajji, TK, Miranda, D and Mulsant, BH (2014) Cognition, function, and disability in patients with schizophrenia: a review of longitudinal studies. Canadian Journal of Psychiatry Revue Canadienne de Psychiatrie 59, 13–17.CrossRefGoogle ScholarPubMed
Rapp, MA, Schnaider-Beeri, M, Purohit, DP, Reichenberg, A, Mcgurk, SR, Haroutunian, V and Harvey, PD (2010) Cortical neuritic plaques and hippocampal neurofibrillary tangles are related to dementia severity in elderly schizophrenia patients. Schizophrenia Research 116, 90–96.CrossRefGoogle ScholarPubMed
Rietveld, CA, Medland, SE, Derringer, J, Yang, J, Esko, T, Martin, NW, Westra, HJ, Shakhbazov, K, Abdellaoui, A, Agrawal, A, Albrecht, E, Alizadeh, BZ, Amin, N, Barnard, J, Baumeister, SE, Benke, KS, Bielak, LF, Boatman, JA, Boyle, PA, Davies, G, De Leeuw, C, Eklund, N, Evans, DS, Ferhmann, R, Fischer, K, Gieger, C, Gjessing, HK, Hagg, S, Harris, JR, Hayward, C, Holzapfel, C, Ibrahim-Verbaas, CA, Ingelsson, E, Jacobsson, B, Joshi, PK, Jugessur, A, Kaakinen, M, Kanoni, S, Karjalainen, J, Kolcic, I, Kristiansson, K, Kutalik, Z, Lahti, J, Lee, SH, Lin, P, Lind, PA, Liu, Y, Lohman, K, Loitfelder, M, Mcmahon, G, Vidal, PM, Meirelles, O, Milani, L, Myhre, R, Nuotio, ML, Oldmeadow, CJ, Petrovic, KE, Peyrot, WJ, Polasek, O, Quaye, L, Reinmaa, E, Rice, JP, Rizzi, TS, Schmidt, H, Schmidt, R, Smith, AV, Smith, JA, Tanaka, T, Terracciano, A, Van Der Loos, MJ, Vitart, V, Volzke, H, Wellmann, J, Yu, L, Zhao, W, Allik, J, Attia, JR, Bandinelli, S, Bastardot, F, Beauchamp, J, Bennett, DA, Berger, K, Bierut, LJ, Boomsma, DI, Bultmann, U, Campbell, H, Chabris, CF, Cherkas, L, Chung, MK, Cucca, F, De Andrade, M, De Jager, PL, De Neve, JE, Deary, IJ, Dedoussis, GV, Deloukas, P, Dimitriou, M, Eiriksdottir, G, Elderson, MF, Eriksson, JG, Evans, DM, Faul, JD, Ferrucci, L, Garcia, ME, Gronberg, H, Guethnason, V, Hall, P, Harris, JM, Harris, TB, Hastie, ND, Heath, AC, Hernandez, DG, Hoffmann, W, Hofman, A, Holle, R, Holliday, EG, Hottenga, JJ, Iacono, WG, Illig, T, Jarvelin, MR, Kahonen, M, Kaprio, J, Kirkpatrick, RM, Kowgier, M, Latvala, A, Launer, LJ, Lawlor, DA, Lehtimaki, T, Li, J, Lichtenstein, P, Lichtner, P, Liewald, DC, Madden, PA, Magnusson, PK, Makinen, TE, Masala, M, Mcgue, M, Metspalu, A, Mielck, A, Miller, MB, Montgomery, GW, Mukherjee, S, Nyholt, DR, Oostra, BA, Palmer, LJ, Palotie, A, Penninx, BW, Perola, M, Peyser, PA, Preisig, M, Raikkonen, K, Raitakari, OT, Realo, A, Ring, SM, Ripatti, S, Rivadeneira, F, Rudan, I, Rustichini, A, Salomaa, V, Sarin, AP, Schlessinger, D, Scott, RJ, Snieder, H, St Pourcain, B, Starr, JM, Sul, JH, Surakka, I, Svento, R, Teumer, A, Tiemeier, H, Van Rooij, FJ, Van Wagoner, DR, Vartiainen, E, Viikari, J, Vollenweider, P, Vonk, JM, Waeber, G, Weir, DR, Wichmann, HE, Widen, E, Willemsen, G, Wilson, JF, Wright, AF, Conley, D, Davey-Smith, G, Franke, L, Groenen, PJ, Hofman, A, Johannesson, M, Kardia, SL, Krueger, RF, Laibson, D, Martin, NG, Meyer, MN, Posthuma, D, Thurik, AR, Timpson, NJ, Uitterlinden, AG, Van Duijn, CM, Visscher, PM, Benjamin, DJ, Cesarini, D and Koellinger, PD (2013) GWAS of 126559 individuals identifies genetic variants associated with educational attainment. Science 340, 1467–1471.CrossRefGoogle ScholarPubMed
Ryan, CL and Bauman, K (2016) Educational attainment in the United States: 2015. In Commerce USDO (ed.). https://www.census.gov/content/dam/Census/library/publications/2016/demo/p20-578.pdfGoogle Scholar
Schaefer, J, Giangrande, E, Weinberger, DR and Dickinson, D (2013) The global cognitive impairment in schizophrenia: consistent over decades and around the world. Schizophrenia Research 150, 42–50.CrossRefGoogle ScholarPubMed
Semple, D and Smyth, R (2013) Oxford Handbook of Psychiatry. Oxford, England: Oxford University Press.CrossRefGoogle Scholar
Stentebjerg-Olesen, M, Pagsberg, AK, Fink-Jensen, A, Correll, CU and Jeppesen, P (2016) Clinical characteristics and predictors of outcome of schizophrenia-spectrum psychosis in children and adolescents: a systematic review. Journal of Child and Adolescent Psychopharmacology 26, 410–427.CrossRefGoogle ScholarPubMed
Strenze, T (2007) Intelligence and socioeconomic success: a meta-analytic review of longitudinal research. Intelligence 35, 401–426.CrossRefGoogle Scholar
Sundqvist, N, Garrick, T, Bishop, I and Harper, C (2008) Reliability of post-mortem psychiatric diagnosis for neuroscience research. Australian and New Zealand Journal of Psychiatry 42, 221–227.CrossRefGoogle ScholarPubMed
Tondo, L, Lepri, B, Cruz, N and Baldessarini, RJ (2010) Age at onset in 3014 Sardinian bipolar and major depressive disorder patients. Acta Psychiatrica Scandinavica 121, 446–452.CrossRefGoogle ScholarPubMed
Tsang, HW, Leung, AY, Chung, RC, Bell, M and Cheung, WM (2010) Review on vocational predictors: a systematic review of predictors of vocational outcomes among individuals with schizophrenia: an update since 1998. Australian and New Zealand Journal of Psychiatry 44, 495–504.Google ScholarPubMed
Ventura, J, Subotnik, KL, Gitlin, MJ, Gretchen-Doorly, D, Ered, A, Villa, KF, Hellemann, GS and Nuechterlein, KH (2015) Negative symptoms and functioning during the first year after a recent onset of schizophrenia and 8 years later. Schizophrenia Research 161, 407–413.CrossRefGoogle ScholarPubMed
Vreeker, A, Boks, MP, Abramovic, L, Verkooijen, S, Van Bergen, AH, Hillegers, MH, Spijker, AT, Hoencamp, E, Regeer, EJ, Riemersma-Van Der Lek, RF, Stevens, AW, Schulte, PF, Vonk, R, Hoekstra, R, Van Beveren, NJ, Kupka, RW, Brouwer, RM, Bearden, CE, Maccabe, JH and Ophoff, RA (2016) High educational performance is a distinctive feature of bipolar disorder: a study on cognition in bipolar disorder, schizophrenia patients, relatives and controls. Psychological Medicine 46, 807–818.CrossRefGoogle Scholar
Wilson, S, Hicks, BM, Foster, KT, Mcgue, M and Iacono, WG (2015) Age of onset and course of major depressive disorder: associations with psychosocial functioning outcomes in adulthood. Psychological Medicine 45, 505–514.CrossRefGoogle ScholarPubMed
Wyatt, ID and Hecker, DE (2006) Occupational changes during the 20th century. Monthly Labor Review, March 2006, pp. 35–57.Google Scholar
Supplementary material: File

Glausier et al. supplementary material

Glausier et al. supplementary material 1

Download Glausier et al. supplementary material(File)
File 19.8 KB