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A longitudinal study of cortical changes and their cognitive correlates in patients followed up after first-episode psychosis

Published online by Cambridge University Press:  03 July 2014

L. Gutiérrez-Galve*
Affiliation:
University College London, Queen Square, London, UK Imperial College Faculty of Medicine, St Mary's Campus, London, UK Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Instituto de Salud Carlos III, Ministerio de Ciencia e Innovación, Madrid, Spain
E. M. Chu
Affiliation:
University College London, Queen Square, London, UK
V. C. Leeson
Affiliation:
Imperial College Faculty of Medicine, Charing Cross Campus, London, UK
G. Price
Affiliation:
University College London, Queen Square, London, UK
T. R. E. Barnes
Affiliation:
Imperial College Faculty of Medicine, Charing Cross Campus, London, UK
E. M. Joyce
Affiliation:
University College London, Queen Square, London, UK
M. A. Ron
Affiliation:
University College London, Queen Square, London, UK
*
*Address for correspondence: Dr L. Gutiérrez-Galve, Academic Unit of Child and Adolescent Psychiatry, 3rd floor QEQM Building, Imperial College, St Mary's Campus, Norfolk Place, London W2 1PG, UK. (Email: [email protected])

Abstract

Background

Loss of cortical volume in frontotemporal regions occurs in patients with first-episode psychosis (FEP) and longitudinal studies have reported progressive brain volume changes at different stages of the disease, even if cognitive deficits remain stable over time. We investigated cortical changes in patients over the 2 years following their FEP and their associations with clinical and cognitive measures.

Method

Twenty-seven patients after their FEP (20 with schizophrenia, seven with schizo-affective disorder) and 25 healthy controls matched for age and gender participated in this study. Magnetic resonance imaging (MRI) was performed on a 1.5-T scanner both at baseline and after 2 years. Area and thickness of the cortex were measured using surface-based morphometry (SBM). Patients also underwent neuropsychological testing at these two time points.

Results

Progressive cortical thinning in the superior and inferior frontal and, to a lesser extent, superior temporal cortex was observed in patients. Cortical area remained constant. Cortical thinning was associated with duration of treatment at a trend level and was predicted by baseline measures of IQ and working memory. Cortical thinning occurred in the absence of clinical or cognitive deterioration.

Conclusions

The clinical implications of these cortical changes remain uncertain, but patients with less cognitive reserve may be more vulnerable to developing cortical abnormalities when exposed to medication or other disease-related biological factors.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2014 

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References

Andreasen, N (1983). The Scale for the Assessment of Negative Symptoms (SANS). The University of Iowa: Iowa City, IA.Google Scholar
Andreasen, N (1984). The Scale for the Assessment of Positive Symptoms (SAPS). The University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC, Nopoulos, P, Magnotta, V, Pierson, R, Ziebell, S, Ho, BC (2011). Progressive brain change in schizophrenia: a prospective longitudinal study of first-episode schizophrenia. Biological Psychiatry 70, 672679.CrossRefGoogle ScholarPubMed
Annett, M (1970). A classification of hand preference by association analysis. British Journal of Psychology 61, 303321.CrossRefGoogle ScholarPubMed
Arango, C, Moreno, C, Martinez, S, Parellada, M, Desco, M, Moreno, D, Fraguas, D, Gogtay, N, James, A, Rapoport, J (2008). Longitudinal brain changes in early-onset psychosis. Schizophrenia Bulletin 34, 341353.CrossRefGoogle ScholarPubMed
Arango, C, Rapado-Castro, M, Reig, S, Castro-Fornieles, J, Gonzalez-Pinto, A, Otero, S, Baeza, I, Moreno, C, Graell, M, Janssen, J, Parellada, M, Moreno, D, Bargallo, N, Desco, M (2012). Progressive brain changes in children and adolescents with first-episode psychosis. Archives of General Psychiatry 69, 1626.CrossRefGoogle ScholarPubMed
Asami, T, Bouix, S, Whitford, TJ, Shenton, ME, Salisbury, DF, McCarley, RW (2012). Longitudinal loss of gray matter volume in patients with first-episode schizophrenia: DARTEL automated analysis and ROI validation. NeuroImage 59, 986996.CrossRefGoogle ScholarPubMed
Boksa, P (2012). Abnormal synaptic pruning in schizophrenia: urban myth or reality? Journal of Psychiatry and Neuroscience 37, 7577.CrossRefGoogle ScholarPubMed
Brans, RG, van Haren, NE, van Baal, GC, Schnack, HG, Kahn, RS, Hulshoff Pol, HE (2008). Heritability of changes in brain volume over time in twin pairs discordant for schizophrenia. Archives of General Psychiatry 65, 12591268.CrossRefGoogle ScholarPubMed
Breslow, NE, Clayton, DG (1993). Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88, 925.Google Scholar
Buckner, RL, Head, D, Parker, J, Fotenos, AF, Marcus, D, Morris, JC, Snyder, AZ (2004). A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. NeuroImage 23, 724738.CrossRefGoogle ScholarPubMed
Cobia, DJ, Smith, MJ, Wang, L, Csernansky, JG (2012). Longitudinal progression of frontal and temporal lobe changes in schizophrenia. Schizophrenia Research 139, 16.CrossRefGoogle ScholarPubMed
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179194.CrossRefGoogle ScholarPubMed
Desikan, RS, Segonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, Buckner, RL, Dale, AM, Maguire, RP, Hyman, BT, Albert, MS, Killiany, RJ (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31, 968980.CrossRefGoogle ScholarPubMed
Drake, RE, Osher, FC, Noordsy, DL, Hurlbut, SC, Teague, GB, Beaudett, MS (1990). Diagnosis of alcohol use disorders in schizophrenia. Schizophrenia Bulletin 16, 5767.CrossRefGoogle ScholarPubMed
Du, AT, Schuff, N, Kramer, JH, Rosen, HJ, Gorno-Tempini, ML, Rankin, K, Miller, BL, Weiner, MW (2007). Different regional patterns of cortical thinning in Alzheimer's disease and frontotemporal dementia. Brain 130, 11591166.CrossRefGoogle ScholarPubMed
Ellison-Wright, I, Glahn, DC, Laird, AR, Thelen, SM, Bullmore, E (2008). The anatomy of first-episode and chronic schizophrenia: an anatomical likelihood estimation meta-analysis. American Journal of Psychiatry 165, 10151023.CrossRefGoogle ScholarPubMed
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences USA 97, 1105011055.CrossRefGoogle ScholarPubMed
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195207.CrossRefGoogle Scholar
Fusar-Poli, P, Smieskova, R, Kempton, MJ, Ho, BC, Andreasen, NC, Borgwardt, S (2013). Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neuroscience and Biobehavioral Reviews 37, 16801691.CrossRefGoogle ScholarPubMed
Genovese, CR, Lazar, NA, Nichols, T (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15, 870878.CrossRefGoogle ScholarPubMed
Giedd, JN, Schmitt, JE, Neale, MC (2007). Structural brain magnetic resonance imaging of pediatric twins. Human Brain Mapping 28, 474481.CrossRefGoogle ScholarPubMed
Goghari, VM, Smith, GN, Honer, WG, Kopala, LC, Thornton, AE, Su, W, Macewan, GW, Lang, DJ (2013). Effects of eight weeks of atypical antipsychotic treatment on middle frontal thickness in drug-naive first-episode psychosis patients. Schizophrenia Research 149, 149155.CrossRefGoogle ScholarPubMed
Gutiérrez-Galve, L, Flugel, D, Thompson, PJ, Koepp, MJ, Symms, MR, Ron, MA, Foong, J (2012). Cortical abnormalities and their cognitive correlates in patients with temporal lobe epilepsy and interictal psychosis. Epilepsia 53, 10771087.CrossRefGoogle ScholarPubMed
Gutiérrez-Galve, L, Wheeler-Kingshott, CA, Altmann, DR, Price, G, Chu, EM, Leeson, VC, Lobo, A, Barker, GJ, Barnes, TR, Joyce, EM, Ron, MA (2010). Changes in the frontotemporal cortex and cognitive correlates in first-episode psychosis. Biological Psychiatry 68, 5160.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Ho, BC, Andreasen, NC, Ziebell, S, Pierson, R, Magnotta, V (2011). Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Archives of General Psychiatry 68, 128137.CrossRefGoogle ScholarPubMed
Huddy, VC, Hodgson, TL, Kapasi, M, Mutsatsa, SH, Harrison, I, Barnes, TR, Joyce, EM (2007). Gaze strategies during planning in first-episode psychosis. Journal of Abnormal Psychology 116, 589598.CrossRefGoogle ScholarPubMed
Hulshoff Pol, HE, Kahn, RS (2008). What happens after the first episode? A review of progressive brain changes in chronically ill patients with schizophrenia. Schizophrenia Bulletin 34, 354366.CrossRefGoogle ScholarPubMed
Ivleva, EI, Bidesi, AS, Keshavan, MS, Pearlson, GD, Meda, SA, Dodig, D, Moates, AF, Lu, H, Francis, AN, Tandon, N, Schretlen, DJ, Sweeney, JA, Clementz, BA, Tamminga, CA (2013). Gray matter volume as an intermediate phenotype for psychosis: Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP). American Journal of Psychiatry 170, 12851296.CrossRefGoogle ScholarPubMed
Jablensky, A, McGrath, J, Herrman, H, Castle, D, Gureje, O, Evans, M, Carr, V, Morgan, V, Korten, A, Harvey, C (2000). Psychotic disorders in urban areas: an overview of the Study on Low Prevalence Disorders. Australian and New Zealand Journal of Psychiatry 34, 221236.CrossRefGoogle Scholar
Joyce, EM, Hutton, SB, Mutsatsa, SH, Barnes, TR (2005). Cognitive heterogeneity in first-episode schizophrenia. British Journal of Psychiatry 187, 516522.CrossRefGoogle ScholarPubMed
Khandaker, GM, Barnett, JH, White, IR, Jones, PB (2011). A quantitative meta-analysis of population-based studies of premorbid intelligence and schizophrenia. Schizophrenia Research 132, 220227.CrossRefGoogle ScholarPubMed
Konopaske, GT, Dorph-Petersen, KA, Pierri, JN, Wu, Q, Sampson, AR, Lewis, DA (2007). Effect of chronic exposure to antipsychotic medication on cell numbers in the parietal cortex of macaque monkeys. Neuropsychopharmacology 32, 12161223.CrossRefGoogle ScholarPubMed
Kuperberg, GR, Broome, MR, McGuire, PK, David, AS, Eddy, M, Ozawa, F, Goff, D, West, WC, Williams, SC, van der Kouwe, AJ, Salat, DH, Dale, AM, Fischl, B (2003). Regionally localized thinning of the cerebral cortex in schizophrenia. Archives General of Psychiatry 60, 878888.CrossRefGoogle ScholarPubMed
Leeson, VC, Sharma, P, Harrison, M, Ron, MA, Barnes, TR, Joyce, EM (2011). IQ trajectory, cognitive reserve, and clinical outcome following a first episode of psychosis: a 3-year longitudinal study. Schizophrenia Bulletin 37, 768777.CrossRefGoogle ScholarPubMed
Lezak, MD (1995). Neuropsychological Assessment. Oxford University Press: New York, NY.Google Scholar
Martin-Santos, R, Fagundo, AB, Crippa, JA, Atakan, Z, Bhattacharyya, S, Allen, P, Fusar-Poli, P, Borgwardt, S, Seal, M, Busatto, GF, McGuire, P (2010). Neuroimaging in cannabis use: a systematic review of the literature. Psychological Medicine 40, 383398.CrossRefGoogle ScholarPubMed
Minatogawa-Chang, TM, Schaufelberger, MS, Ayres, AM, Duran, FL, Gutt, EK, Murray, RM, Rushe, TM, McGuire, PK, Menezes, PR, Scazufca, M, Busatto, GF (2009). Cognitive performance is related to cortical grey matter volumes in early stages of schizophrenia: a population-based study of first-episode psychosis. Schizophrenia Research 113, 200209.CrossRefGoogle ScholarPubMed
Moncrieff, J, Leo, J (2010). A systematic review of the effects of antipsychotic drugs on brain volume. Psychological Medicine 40, 14091422.CrossRefGoogle ScholarPubMed
Murray, GK, Corlett, PR, Fletcher, PC (2010). The neural underpinnings of associative learning in health and psychosis: how can performance be preserved when brain responses are abnormal? Schizophrenia Bulletin 36, 465471.CrossRefGoogle ScholarPubMed
Murray, RM, Lewis, SW (1987). Is schizophrenia a neurodevelopmental disorder? British Medical Journal (Clinical Research Edition) 295, 681682.CrossRefGoogle ScholarPubMed
Narr, KL, Bilder, RM, Toga, AW, Woods, RP, Rex, DE, Szeszko, PR, Robinson, D, Sevy, S, Gunduz-Bruce, H, Wang, YP, DeLuca, H, Thompson, PM (2005). Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cerebral Cortex 15, 708719.CrossRefGoogle ScholarPubMed
Nelson, H, Willson, J (1991). The Revised National Adult Reading Test (NART): Test Manual. NFER-Nelson: Windsor.Google Scholar
Owens, SF, Picchioni, MM, Ettinger, U, McDonald, C, Walshe, M, Schmechtig, A, Murray, RM, Rijsdijk, F, Toulopoulou, T (2012). Prefrontal deviations in function but not volume are putative endophenotypes for schizophrenia. Brain 135, 22312244.CrossRefGoogle Scholar
Panizzon, MS, Fennema-Notestine, C, Eyler, LT, Jernigan, TL, Prom-Wormley, E, Neale, M, Jacobson, K, Lyons, MJ, Grant, MD, Franz, CE, Xian, H, Tsuang, M, Fischl, B, Seidman, L, Dale, A, Kremen, WS (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex 19, 27282735.CrossRefGoogle ScholarPubMed
Perkins, DO, Leserman, J, Jarskog, LF, Graham, K, Kazmer, J, Lieberman, JA (2000). Characterizing and dating the onset of symptoms in psychotic illness: the Symptom Onset in Schizophrenia (SOS) inventory. Schizophrenia Research 44, 110.CrossRefGoogle ScholarPubMed
Rais, M, Cahn, W, Van Haren, N, Schnack, H, Caspers, E, Hulshoff Pol, H, Kahn, R (2008). Excessive brain volume loss over time in cannabis-using first-episode schizophrenia patients. American Journal of Psychiatry 165, 490496.CrossRefGoogle ScholarPubMed
Reilly, JL, Sweeney, JA (2014). Generalized and specific neurocognitive deficits in psychotic disorders: utility for evaluating pharmacological treatment effects and as intermediate phenotypes for gene discovery. Schizophrenia Bulletin 40, 516522.CrossRefGoogle ScholarPubMed
Reuter, M, Fischl, B (2011). Avoiding asymmetry-induced bias in longitudinal image processing. NeuroImage 57, 1921.CrossRefGoogle ScholarPubMed
Reuter, M, Schmansky, NJ, Rosas, HD, Fischl, B (2012). Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 61, 14021418.CrossRefGoogle ScholarPubMed
Roiz-Santianez, R, Tordesillas-Gutierrez, D, Ortiz-Garcia de la Foz, V, Ayesa-Arriola, R, Gutierrez, A, Tabares-Seisdedos, R, Vazquez-Barquero, JL, Crespo-Facorro, B (2012). Effect of antipsychotic drugs on cortical thickness. A randomized controlled one-year follow-up study of haloperidol, risperidone and olanzapine. Schizophrenia Research 141, 2228.CrossRefGoogle ScholarPubMed
Sahakian, BJ, Owen, AM (1992). Computerized assessment in neuropsychiatry using CANTAB: discussion paper. Journal of the Royal Society of Medicine 85, 399402.Google ScholarPubMed
Schultz, CC, Koch, K, Wagner, G, Roebel, M, Schachtzabel, C, Gaser, C, Nenadic, I, Reichenbach, JR, Sauer, H, Schlosser, RG (2010). Reduced cortical thickness in first episode schizophrenia. Schizophrenia Research 116, 204209.CrossRefGoogle ScholarPubMed
Selemon, LD (2001). Regionally diverse cortical pathology in schizophrenia: clues to the etiology of the disease. Schizophrenia Bulletin 27, 349377.CrossRefGoogle Scholar
Sun, D, Stuart, GW, Jenkinson, M, Wood, SJ, McGorry, PD, Velakoulis, D, van Erp, TG, Thompson, PM, Toga, AW, Smith, DJ, Cannon, TD, Pantelis, C (2009). Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Molecular Psychiatry 14, 976986.CrossRefGoogle ScholarPubMed
Thompson, PM, Vidal, C, Giedd, JN, Gochman, P, Blumenthal, J, Nicolson, R, Toga, AW, Rapoport, JL (2001). Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proceedings of the National Academy of Sciences USA 98, 1165011655.CrossRefGoogle ScholarPubMed
Uranova, NA, Vostrikov, VM, Orlovskaya, DD, Rachmanova, VI (2004). Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophrenia Research 67, 269275.CrossRefGoogle ScholarPubMed
van Haren, NE, Cahn, W, Hulshoff Pol, HE, Kahn, RS (2012). The course of brain abnormalities in schizophrenia: can we slow the progression? Journal of Psychopharmacology 26, 814.CrossRefGoogle ScholarPubMed
van Haren, NE, Hulshoff Pol, HE, Schnack, HG, Cahn, W, Brans, R, Carati, I, Rais, M, Kahn, RS (2008). Progressive brain volume loss in schizophrenia over the course of the illness: evidence of maturational abnormalities in early adulthood. Biological Psychiatry 63, 106113.CrossRefGoogle ScholarPubMed
van Haren, NE, Schnack, HG, Cahn, W, van den Heuvel, MP, Lepage, C, Collins, L, Evans, AC, Hulshoff Pol, HE, Kahn, RS (2011). Changes in cortical thickness during the course of illness in schizophrenia. Archives of General Psychiatry 68, 871880.CrossRefGoogle ScholarPubMed
Vernon, AC, Natesan, S, Modo, M, Kapur, S (2011). Effect of chronic antipsychotic treatment on brain structure: a serial magnetic resonance imaging study with ex vivo and postmortem confirmation. Biological Psychiatry 69, 936944.CrossRefGoogle ScholarPubMed
Vidal, CN, Rapoport, JL, Hayashi, KM, Geaga, JA, Sui, Y, McLemore, LE, Alaghband, Y, Giedd, JN, Gochman, P, Blumenthal, J, Gogtay, N, Nicolson, R, Toga, AW, Thompson, PM (2006). Dynamically spreading frontal and cingulate deficits mapped in adolescents with schizophrenia. Archives of General Psychiatry 63, 2534.CrossRefGoogle ScholarPubMed
Voets, NL, Hough, MG, Douaud, G, Matthews, PM, James, A, Winmill, L, Webster, P, Smith, S (2008). Evidence for abnormalities of cortical development in adolescent-onset schizophrenia. NeuroImage 43, 665675.CrossRefGoogle ScholarPubMed
Wechsler, D (1997). Wechsler Adult Intelligence Scale – 3rd Edition (WAIS-III). The Psychological Corporation: San Antonio, TX.Google Scholar
Wisco, JJ, Kuperberg, G, Manoach, D, Quinn, BT, Busa, E, Fischl, B, Heckers, S, Sorensen, AG (2007). Abnormal cortical folding patterns within Broca's area in schizophrenia: evidence from structural MRI. Schizophrenia Research 94, 317327.CrossRefGoogle ScholarPubMed
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435.CrossRefGoogle ScholarPubMed
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