Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-19T03:21:23.119Z Has data issue: false hasContentIssue false
  • English
  • Français

Cortical thickness and surface area correlates with cognitive dysfunction among first-episode psychosis patients

Published online by Cambridge University Press:  07 June 2016

L. Haring ,
A. Müürsepp ,
R. Mõttus ,
P. Ilves ,
K. Koch ,
K. Uppin ,
J. Tarnovskaja ,
E. Maron ,
A. Zharkovsky  and
E. Vasar
...Show all authors
L. Haring*
Affiliation:
Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia
A. Müürsepp
Affiliation:
Radiology Clinic of Tartu University Hospital, Tartu, Estonia Department of Radiology, University of Tartu, Tartu, Estonia
R. Mõttus
Affiliation:
Department of Psychology, University of Edinburgh, Edinburgh, UK Department of Psychology, University of Tartu, Tartu, Estonia
P. Ilves
Affiliation:
Radiology Clinic of Tartu University Hospital, Tartu, Estonia Department of Radiology, University of Tartu, Tartu, Estonia
K. Koch
Affiliation:
Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia
K. Uppin
Affiliation:
Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia
J. Tarnovskaja
Affiliation:
Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia
E. Maron
Affiliation:
Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia Department of Psychiatry, North Estonia Medical Centre, Tallinn, Estonia Centre for Mental Health, Imperial College London, London, UK
A. Zharkovsky
Affiliation:
Department of Pharmacology and Translational Medicine, University of Tartu, Tartu, Estonia Centre of Excellence for Translational Medicine, University of Tartu, Tartu, Estonia
E. Vasar
Affiliation:
Centre of Excellence for Translational Medicine, University of Tartu, Tartu, Estonia Institute of Biomedicine and Translational Medicine, University of Tartu, Tartu, Estonia
V. Vasar
Affiliation:
Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia
*
*Address for correspondence: L. Haring, M.D., Psychiatry Clinic of Tartu University Hospital, Tartu, Estonia. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

In studies using magnetic resonance imaging (MRI), some have reported specific brain structure–function relationships among first-episode psychosis (FEP) patients, but findings are inconsistent. We aimed to localize the brain regions where cortical thickness (CTh) and surface area (cortical area; CA) relate to neurocognition, by performing an MRI on participants and measuring their neurocognitive performance using the Cambridge Neuropsychological Test Automated Battery (CANTAB), in order to investigate any significant differences between FEP patients and control subjects (CS).

Method

Exploration of potential correlations between specific cognitive functions and brain structure was performed using CANTAB computer-based neurocognitive testing and a vertex-by-vertex whole-brain MRI analysis of 63 FEP patients and 30 CS.

Results

Significant correlations were found between cortical parameters in the frontal, temporal, cingular and occipital brain regions and performance in set-shifting, working memory manipulation, strategy usage and sustained attention tests. These correlations were significantly dissimilar between FEP patients and CS.

Conclusions

Significant correlations between CTh and CA with neurocognitive performance were localized in brain areas known to be involved in cognition. The results also suggested a disrupted structure–function relationship in FEP patients compared with CS.

Keywords

Cambridge Neuropsychological Test Automated Batterycognitionfirst-episode psychosismagnetic resonance imaging
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 10 , July 2016 , pp. 2145 - 2155
Copyright
Copyright © Cambridge University Press 2016 

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

Ansell, BRE, Dwyer, DB, Wood, SJ, Bora, E, Brewer, WJ, Proffitt, TM, Velakoulis, D, McGorry, PD, Pantelis, C (2015). Divergent effects of first-generation and second-generation antipsychotics on cortical thickness in first-episode psychosis. Psychological Medicine 45, 515–527.Google Scholar
Antonova, E, Kumari, V, Morris, R, Halari, R, Anilkumar, A, Mehrotra, R, Sharma, T (2005). The relationship of structural alterations to cognitive deficits in schizophrenia: a voxel-based morphometry study. Biological Psychiatry 58, 457–467.Google Scholar
Barch, DM, Keefe, RSE (2010). Anticipating DSM-V: opportunities and challenges for cognition and psychosis. Schizophrenia Bulletin 36, 43–47.Google Scholar
Bassett, DS, Bullmore, E, Verchinski, BA, Mattay, VS, Weinberger, DR, Meyer-Lindenberg, A (2008). Hierarchical organization of human cortical networks in health and schizophrenia. Journal of Neuroscience 28, 9239–9248.Google Scholar
Bilder, RM, Goldman, RS, Robinson, D, Reiter, G, Bell, L, Bates, JA, Pappadopulos, E, Willson, DF, Alvir, JMJ, Woerner, MG, Geisler, S, Kane, JM, Lieberman, JA (2000). Neuropsychology of first-episode schizophrenia: initial characterization and clinical correlates. American Journal of Psychiatry 157, 549–559.Google Scholar
Burgaleta, M, Johnson, W, Waber, DP, Colom, R, Karama, S (2014). Cognitive ability changes and dynamics of cortical thickness development in healthy children and adolescents. NeuroImage 84, 810–819.Google Scholar
Casanova, MF, de Zeeuw, L, Switala, A, Kreczmanski, P, Korr, H, Ulfig, N, Heinsen, H, Steinbusch, HWM, Schmitz, C (2005). Mean cell spacing abnormalities in the neocortex of patients with schizophrenia. Psychiatry Research 133, 1–12.Google Scholar
Cocchi, L, Walterfang, M, Testa, R, Wood, SJ, Seal, ML, Suckling, J, Takahashi, T, Proffitt, T-M, Brewer, WJ, Adamson, C, Soulsby, B, Velakoulis, D, McGorry, PD, Pantelis, C (2009). Grey and white matter abnormalities are associated with impaired spatial working memory ability in first-episode schizophrenia. Schizophrenia Research 115, 163–172.Google Scholar
Cohen, J (1977). Statistical Power Analysis for the Behavioral Sciences, rev. edn. Lawrence Erlbaum Associates, Inc.: Hillsdale, NJ.Google Scholar
Colom, R, Burgaleta, M, Román, FJ, Karama, S, Álvarez-Linera, J, Abad, FJ, Martínez, K, Quiroga, MÁ, Haier, RJ (2013). Neuroanatomic overlap between intelligence and cognitive factors: morphometry methods provide support for the key role of the frontal lobes. NeuroImage 72, 143–152.Google Scholar
Crespo-Facorro, B, Roiz-Sántiañez, R, Pérez-Iglesias, R, Rodriguez-Sanchez, JM, Mata, I, Tordesillas-Gutierrez, D, Sanchez, E, Tabarés-Seisdedos, R, Andreasen, N, Magnotta, V, Vázquez-Barquero, JL (2011). Global and regional cortical thinning in first-episode psychosis patients: relationships with clinical and cognitive features. Psychological Medicine 41, 1449–1460.Google Scholar
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179–194.Google Scholar
DeLisi, LE, Hoff, AL, Schwartz, JE, Shields, GW, Halthore, SN, Gupta, SM, Henn, FA, Anand, AK (1991). Brain morphology in first-episode schizophrenic-like psychotic patients: a quantitative magnetic resonance imaging study. Biological Psychiatry 29, 159–175.Google Scholar
Dickinson, D, Goldberg, TE, Gold, JM, Elvevåg, 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
Doorduin, J, de Vries, EFJ, Willemsen, ATM, de Groot, JC, Dierckx, RA, Klein, HC (2009). Neuroinflammation in schizophrenia-related psychosis: a PET study. Journal of Nuclear Medicine 50, 1801–1807.Google Scholar
Ehrlich, S, Brauns, S, Yendiki, A, Ho, B-C, Calhoun, V, Schulz, SC, Gollub, RL, Sponheim, SR (2012). Associations of cortical thickness and cognition in patients with schizophrenia and healthy controls. Schizophrenia Bulletin 38, 1050–1062.Google Scholar
Falkai, P, Rossner, MJ, Schulze, TG, Hasan, A, Brzózka, MM, Malchow, B, Honer, WG, Schmitt, A (2015). Kraepelin revisited: schizophrenia from degeneration to failed regeneration. Molecular Psychiatry 20, 671–676.Google Scholar
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America 97, 11050–11055.Google Scholar
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, van der Kouwe, A, Killiany, R, Kennedy, D, Klaveness, S, Montillo, A, Makris, N, Rosen, B, Dale, AM (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.Google Scholar
Fischl, B, Sereno, MI, Tootell, RBH, Dale, AM (1999). High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping 8, 272–284.Google Scholar
Fischl, B, van der Kouwe, A, Destrieux, C, Halgren, E, Ségonne, F, Salat, DH, Busa, E, Seidman, LJ, Goldstein, J, Kennedy, D, Caviness, V, Makris, N, Rosen, B, Dale, AM (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex 14, 11–22.Google Scholar
Fornito, A, Bullmore, ET (2015). Reconciling abnormalities of brain network structure and function in schizophrenia. Current Opinion in Neurobiology 30, 44–50.Google Scholar
Fornito, A, Yücel, M, Wood, SJ, Adamson, C, Velakoulis, D, Saling, MM, McGorry, PD, Pantelis, C (2008). Surface-based morphometry of the anterior cingulate cortex in first episode schizophrenia. Human Brain Mapping 29, 478–489.Google Scholar
Friston, KJ (1998). The disconnection hypothesis. Schizophrenia Research 30, 115–125.Google Scholar
Gardner, DM, Murphy, AL, O'Donnell, H, Centorrino, F, Baldessarini, RJ (2010). International consensus study of antipsychotic dosing. American Journal of Psychiatry 167, 686–693.Google Scholar
Genovese, CR, Lazar, NA, Nichols, T (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15, 870–878.Google Scholar
Goldman-Rakic, PS, Selemon, LD (1997). Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophrenia Bulletin 23, 437–458.Google Scholar
Green, RL, Gazzaniga, MS (2001). Linking neuroimaging and cognitive neuropsychiatry. Cognitive Neuropsychiatry 6, 229–234.Google Scholar
Gutiérrez-Galve, L, Wheeler-Kingshott, CAM, Altmann, DR, Price, G, Chu, EM, Leeson, VC, Lobo, A, Barker, GJ, Barnes, TRE, Joyce, EM, Ron, MA (2010). Changes in the frontotemporal cortex and cognitive correlates in first-episode psychosis. Biological Psychiatry 68, 51–60.Google Scholar
Haring, L, Koido, K, Vasar, V, Leping, V, Zilmer, K, Zilmer, M, Vasar, E (2015 a). Antipsychotic treatment reduces psychotic symptoms and markers of low-grade inflammation in first episode psychosis patients, but increases their body mass index. Schizophrenia Research 169, 22–29.Google Scholar
Haring, L, Mõttus, R, Koch, K, Trei, M, Maron, E (2015 b). Factorial validity, measurement equivalence and cognitive performance of the Cambridge Neuropsychological Test Automated Battery (CANTAB) between patients with first-episode psychosis and healthy volunteers. Psychological Medicine 45, 1919–1929.Google Scholar
Hartberg, CB, Lawyer, G, Nyman, H, Jönsson, EG, Haukvik, UK, Saetre, P, Bjerkan, PS, Andreassen, OA, Hall, H, Agartz, I (2010). Investigating relationships between cortical thickness and cognitive performance in patients with schizophrenia and healthy adults. Psychiatry Research: Neuroimaging 182, 123–133.Google Scholar
Hatton, SN, Lagopoulos, J, Hermens, DF, Naismith, SL, Bennett, MR, Hickie, IB (2012). Correlating anterior insula gray matter volume changes in young people with clinical and neurocognitive outcomes: an MRI study. BMC Psychiatry 12, 45.Google Scholar
Hatton, SN, Lagopoulos, J, Hermens, DF, Scott, E, Hickie, IB, Bennett, MR (2013). Cortical thinning in young psychosis and bipolar patients correlate with common neurocognitive deficits. International Journal of Bipolar Disorders 1, 3.Google Scholar
Kasai, K, Shenton, ME, Salisbury, DF, Hirayasu, Y, Lee, C-U, Ciszewski, AA, Yurgelun-Todd, D, Kinikis, R, Jolesz, FA, McCarley, RW (2003). Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. American Journal of Psychiatry 160, 156–164.Google Scholar
Keshavan, MS, Berger, G, Zipursky, RB, Wood, SJ, Pantelis, C (2005). Neurobiology of early psychosis. British Journal of Psychiatry 187, s8–s18.Google Scholar
Keshavan, MS, Haas, GL, Kahn, CE, Aguilar, E, Dick, EL, Schooler, NR, Sweeney, JA, Pettegrew, JW (1998). Superior temporal gyrus and the course of early schizophrenia: progressive, static, or reversible? Journal of Psychiatric Research 32, 161–167.Google Scholar
Kuroki, N, Shenton, ME, Salisbury, DF, Hirayasu, Y, Onitsuka, T, Ersner-Hershfield, H, Yurgelun-Todd, D, Kikinis, R, Jolesz, FA, McCarley, RW (2006). Middle and inferior temporal gyrus gray matter volume abnormalities in first-episode schizophrenia: an MRI study. American Journal of Psychiatry 163, 2103–2110.Google Scholar
Leeson, VC, Robbins, TW, Franklin, C, Harrison, M, Harrison, I, Ron, MA, Barnes, TRE, Joyce, EM (2009). Dissociation of long-term verbal memory and fronto-executive impairment in first-episode psychosis. Psychological Medicine 39, 1799–1808.Google Scholar
Liberto, CM, Albrecht, PJ, Herx, LM, Yong, VW, Levison, SW (2004). Pro-regenerative properties of cytokine-activated astrocytes. Journal of Neurochemistry 89, 1092–1100.Google Scholar
Makris, N, Kaiser, J, Haselgrove, C, Seidman, LJ, Biederman, J, Boriel, D, Valera, EM, Papadimitriou, GM, Fischl, B, Caviness, VS Jr., Kennedy, DN (2006). Human cerebral cortex: a system for the integration of volume- and surface-based representations. NeuroImage 33, 139–153.Google Scholar
Minatogawa-Chang, TM, Schaufelberger, MS, Ayres, AM, Duran, FLS, 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, 200–209.Google Scholar
Molina, V, Sanz, J, Sarramea, F, Benito, C, Palomo, T (2004). Lower prefrontal gray matter volume in schizophrenia in chronic but not in first episode schizophrenia patients. Psychiatry Research 131, 45–56.Google Scholar
Murray, RM, Lewis, SW (1988). Is schizophrenia a neurodevelopmental disorder? British Medical Journal 296, 63–63.Google Scholar
Narr, KL, Bilder, RM, Toga, AW, Woods, RP, Rex, DE, Szeszko, PR, Robinson, D, Sevy, S, Gunduz-Bruce, H, Wang, Y-P, DeLuca, H, Thompson, PM (2005). Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cerebral Cortex 15, 708–719.Google Scholar
Nenadic, I, Dietzek, M, Schönfeld, N, Lorenz, C, Gussew, A, Reichenbach, JR, Sauer, H, Gaser, C, Smesny, S (2015). Brain structure in people at ultra-high risk of psychosis, patients with first-episode schizophrenia, and healthy controls: a VBM study. Schizophrenia Research 161, 169–176.Google Scholar
Neubauer, AC, Fink, A (2009). Intelligence and neural efficiency. Neuroscience and Biobehavioral Reviews 33, 1004–1023.Google Scholar
Overall, JE, Gorham, DR (1962). The Brief Psychiatric Rating Scale. Psychological Reports 10, 799–812.Google Scholar
Palaniyappan, L, Mallikarjun, P, Joseph, V, White, TP, Liddle, PF (2011). Regional contraction of brain surface area involves three large-scale networks in schizophrenia. Schizophrenia Research 129, 163–168.Google Scholar
Penke, L, Maniega, SM, Bastin, ME, Hernández, MCV, Murray, C, Royle, NA, Starr, JM, Wardlaw, JM, Deary, IJ (2012). Brain-wide white matter tract integrity is associated with information processing speed and general intelligence. Molecular Psychiatry 17, 955–955.Google Scholar
Premkumar, P, Kumari, V, Corr, PJJ, Fannon, D, Sharma, T (2008). Neuropsychological function–brain structure relationships and stage of illness: an investigation into chronic and first-episode schizophrenia. Psychiatry Research: Neuroimaging 162, 195–204.Google Scholar
R Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.Google Scholar
Rimol, LM, Nesvåg, R, Hagler, DJJ, Bergmann, Ø, Fennema-Notestine, C, Hartberg, CB, Haukvik, UK, Lange, E, Pung, CJ, Server, A, Melle, I, Andreassen, OA, Agartz, I, Dale, AM (2012). Cortical volume, surface area, and thickness in schizophrenia and bipolar disorder. Biological Psychiatry 71, 552–560.Google Scholar
Robbins, TW, Sahakian, BJ (1994 ). Computer methods of assessment of cognitive function. In Principles and Practice of Geriatric Psychiatry, vol. 2013 (ed. Copeland, J.R.M., Abou-Saleh, M.T. and Blazer, D.G.), pp. 205–209. John Wiley & Sons, Ltd: Chichester, UK.Google Scholar
Roiz-Santiáñez, R, Pérez-Iglesias, R, Quintero, C, Tordesillas-Gutiérrez, D, Mata, I, Gutiérrez, A, Sánchez, E, Pazos, A, Tabarés-Seisdedos, R, Vázquez-Barquero, JL, Crespo-Facorro, B (2010). Temporal pole morphology in first-episode schizophrenia patients. Psychiatry Research: Neuroimaging 184, 189–191.Google Scholar
Salgado-Pineda, P, Baeza, I, Pérez-Gómez, M, Vendrell, P, Junqué, C, Bargalló, N, Bernardo, M (2003). Sustained attention impairment correlates to gray matter decreases in first episode neuroleptic-naive schizophrenic patients. NeuroImage 19, 365–375.Google Scholar
Sanabria-Diaz, G, Melie-García, L, Iturria-Medina, Y, Alemán-Gómez, Y, Hernández-González, G, Valdés-Urrutia, L, Galán, L, Valdés-Sosa, P (2010). Surface area and cortical thickness descriptors reveal different attributes of the structural human brain networks. NeuroImage 50, 1497–1510.Google Scholar
Ségonne, F, Pacheco, J, Fischl, B (2007). Geometrically accurate topology – correction of cortical surfaces using nonseparating loops. IEEE Transactions on Medical Imaging 26, 518–529.Google Scholar
Selemon, LD, Goldman-Rakic, PS (1999). The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biological Psychiatry 45, 17–25.Google Scholar
Selemon, LD, Rajkowska, G, Goldman-Rakic, PS (1998). Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. Journal of Comparative Neurology 392, 402–412.Google Scholar
Shaw, P, Greenstein, D, Lerch, J, Clasen, L, Lenroot, R, Gogtay, N, Evans, A, Rapoport, J, Giedd, J (2006). Intellectual ability and cortical development in children and adolescents. Nature 440, 676–679.Google Scholar
Shenton, ME, Dickey, CC, Frumin, M, McCarley, RW (2001). A review of MRI findings in schizophrenia. Schizophrenia Research 49, 1–52.Google Scholar
Sled, JG, Zijdenbos, AP, Evans, AC (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging 17, 87–97.Google Scholar
Takayanagi, Y, Takahashi, T, Orikabe, L, Mozue, Y, Kawasaki, Y, Nakamura, K, Sato, Y, Itokawa, M, Yamasue, H, Kasai, K, Kurachi, M, Okazaki, Y, Suzuki, M (2011). Classification of first-episode schizophrenia patients and healthy subjects by automated MRI measures of regional brain volume and cortical thickness. PLoS ONE 6, e21047.Google Scholar
Tamminga, CA (1997). Gender and schizophrenia. Journal of Clinical Psychiatry 58, 33–37.Google Scholar
Tan, H-Y, Callicott, JH, Weinberger, DR (2007). Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cerebral Cortex 17, 171–181.Google Scholar
Toulopoulou, T, Grech, A, Morris, RG, Schulze, K, McDonald, C, Chapple, B, Rabe-Hesketh, S, Murray, RM (2004). The relationship between volumetric brain changes and cognitive function: a family study on schizophrenia. Biological Psychiatry 56, 447–453.Google Scholar
Vakhtin, AA, Ryman, SG, Flores, RA, Jung, RE (2014). Functional brain networks contributing to the parieto-frontal integration theory of intelligence. NeuroImage 103, 349–354.Google Scholar
van Berckel, BN, Bossong, MG, Boellaard, R, Kloet, R, Schuitemaker, A, Caspers, E, Luurtsema, G, Windhorst, AD, Cahn, W, Lammertsma, AA, Kahn, RS (2008). Microglia activation in recent-onset schizophrenia: a quantitative (R)-[11C]PK11195 positron emission tomography study. Biological Psychiatry 64, 820–822.Google Scholar
van den Heuvel, MP, Stam, CJ, Kahn, RS, Hulshoff Pol, HE (2009). Efficiency of functional brain networks and intellectual performance. Journal of Neuroscience 29, 7619–7624.Google Scholar
Vita, A, De Peri, L, Silenzi, C, Dieci, M (2006). Brain morphology in first-episode schizophrenia: a meta-analysis of quantitative magnetic resonance imaging studies. Schizophrenia Research 82, 75–88.Google Scholar
Weinberger, DR (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 44, 660–669.Google Scholar
World Health Organization (1992). The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines. WHO: Geneva, Switzerland.Google Scholar
Supplementary material: PDF

Haring supplementary material

Figures S1-S3

Download Haring supplementary material(PDF)
PDF 1.8 MB
Supplementary material: File

Haring supplementary material

Tables S1-S3

Download Haring supplementary material(File)
File 573.4 KB