Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-18T15:40:12.040Z Has data issue: false hasContentIssue false

Global and regional cortical thinning in first-episode psychosis patients: relationships with clinical and cognitive features

Published online by Cambridge University Press:  14 October 2010

B. Crespo-Facorro*
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
R. Roiz-Santiáñez
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
R. Pérez-Iglesias
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
J. M. Rodriguez-Sanchez
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
I. Mata
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
D. Tordesillas-Gutierrez
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
E. Sanchez
Affiliation:
University Hospital Marqués de Valdecilla, Department of Neuroradiology, Santander, Spain
R. Tabarés-Seisdedos
Affiliation:
Teaching Unit of Psychiatry and Psychological Medicine, CIBERSAM, Department of Medicine, University of Valencia, Valencia, Spain
N. Andreasen
Affiliation:
Department of Psychiatry, Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, USA
V. Magnotta
Affiliation:
Department of Psychiatry, Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, USA Department of Radiology, Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, USA Department of Biomedical Engineering, College of Engineering, University of Iowa, Iowa City, USA
J. L. Vázquez-Barquero
Affiliation:
University Hospital Marqués de Valdecilla, CIBERSAM, IFIMAV, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
*
*Address for correspondence: Professor B. Crespo-Facorro, Hospital Universitario Marqués de Valdecilla, Department of Psychiatry, Planta 2a, Edificio 2 de Noviembre. Avda. Valdecilla s/n, 39008, Santander, Spain. (Email: bcfacorro@humv.es)

Abstract

Background

The thickness of the cortical mantle is a sensitive measure for identifying alterations in cortical structure. We aimed to explore whether first episode schizophrenia patients already show a significant cortical thinning and whether cortical thickness anomalies may significantly influence clinical and cognitive features.

Method

We investigated regional changes in cortical thickness in a large and heterogeneous sample of schizophrenia spectrum patients (n=142) at their first break of the illness and healthy controls (n=83). Magnetic resonance imaging brain scans (1.5 T) were obtained and images were analyzed by using brains2. The contribution of sociodemographic, cognitive and clinical characterictics was investigated.

Results

Patients showed a significant total cortical thinning (F=17.55, d=−0.62, p<0.001) and there was a diffuse pattern of reduced thickness (encompassing frontal, temporal and parietal cortices) (all p's<0.001, d's>0.53). No significant group×gender interactions were observed (all p's>0.15). There were no significant associations between the clinical and pre-morbid variables and cortical thickness measurements (all r's<0.12). A weak significant negative correlation between attention and total (r=−0.24, p=0.021) and parietal cortical thickness (r=−0.27, p=0.009) was found in patients (thicker cortex was associated with lower attention). Our data revealed a similar pattern of cortical thickness changes related to age in patients and controls.

Conclusions

Cortical thinning is independent of gender, age, age of onset and duration of the illness and does not seem to significantly influence clinical and functional symptomatology. These findings support a primary neurodevelopment disorder affecting the normal cerebral cortex development in schizophrenia.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2010

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 Negative Symptoms (SANS). University of Iowa: Iowa City.Google Scholar
Andreasen, NC (1984). The Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa: Iowa City.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, 615623.CrossRefGoogle ScholarPubMed
Andreasen, NC, Rajarethinam, R, Cizadlo, T, Arndt, S, Swayze, VW 2nd, Flashman, LA, O'Leary, DS, Ehrhardt, JC, Yuh, WT (1996). Automatic atlas-based volume estimation of human brain regions from MR images. Journal of Computer Assisted Tomography 20, 98–106.CrossRefGoogle ScholarPubMed
Bystron, I, Blakemore, C, Rakic, P (2008). Development of the human cerebral cortex: Boulder Committee revisited. Nature Reviews Neuroscience 9, 110122.CrossRefGoogle ScholarPubMed
Coffey, CE, Lucke, JF, Saxton, JA, Ratcliff, G, Unitas, LJ, Billig, B, Bryan, RN (1998). Sex differences in brain aging: a quantitative magnetic resonance imaging study. Archives of Neurology 55, 169179.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Barbadillo, L, Pelayo-Teran, JM, Rodriguez-Sanchez, JM (2007). Neuropsychological functioning and brain structure in schizophrenia. International Review of Psychiatry 19, 325336.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Kim, J, Andreasen, NC, O'Leary, DS, Bockholt, HJ, Magnotta, V (2000 a). Insular cortex abnormalities in schizophrenia: a structural magnetic resonance imaging study of first-episode patients. Schizophrenia Research 46, 3543.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Kim, J, Andreasen, NC, O'Leary, DS, Magnotta, V (2000 b). Regional frontal abnormalities in schizophrenia: a quantitative gray matter volume and cortical surface size study. Biological Psychiatry 48, 110119.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Roiz-Santiáñez, R, Pelayo-Terán, JM, Rodríguez-Sánchez, JM, Pérez-Iglesias, R, González-Blanch, C, Tordesillas-Gutiérrez, D, González-Mandly, A, Díez, C, Magnotta, VA, Andreasen, NC, Vázquez-Barquero, JL (2007). Reduced thalamic volume in first-episode non-affective psychosis: correlations with clinical variables, symptomatology and cognitive functioning. Neuroimage 35, 16131623.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Roiz-Santiáñez, R, Pérez-Iglesias, R, Mata, I, Rodriguez-Sanchez, JM, Tordesillas-Gutierrez, D, Tabarés-Seisdedos, R, Sanchez, E, Andreasen, N, Magnotta, V, Vázquez-Barquero, JL (in press). Sex differences in cortical morphometry. Brain and Cognition.Google Scholar
Csernansky, JG, Gillespie, SK, Dierker, DL, Anticevic, A, Wang, L, Barch, DM, van Essen, DC (2008). Symmetric abnormalities in sulcal patterning in schizophrenia. Neuroimage 43, 440446.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, J (2001). Structured Clinical Interview for DSM-IV-TR Axis I Disorders – Non Patient Edition. New York State Psychiatric Institute: New York.Google Scholar
Flagstad, P, Glenthoj, BY, Didriksen, M (2005). Cognitive deficits caused by late gestational disruption of neurogenesis in rats: a preclinical model of schizophrenia. Neuropsychopharmacology 30, 250260.CrossRefGoogle ScholarPubMed
Goghari, VM, Rehm, K, Carter, CS, MacDonald, AW (2007). Sulcal thickness as a vulnerability indicator for schizophrenia. The British Journal of Psychiatry 191, 229233.CrossRefGoogle ScholarPubMed
Gogtay, N, Giedd, JN, Lusk, L, Hayashi, KM, Greenstein, D, Vaituzis, AC, Nugent, TF, Herman, DH, Clasen, LS, Toga, AW, Rapoport, JL, Thompson, PM (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences USA 101, 13421348.CrossRefGoogle ScholarPubMed
Goldman, AL, Pezawas, L, Mattay, VS, Fischl, B, Verchinski, BA, Chen, Q, Weinberger, DR, Meyer-Lindenberg, A (2009). Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Archives of General Psychiatry 66, 467477.CrossRefGoogle ScholarPubMed
Gong, QY, Sluming, V, Mayes, A, Keller, S, Barrick, T, Cezayirli, E, Roberts, N (2005). Voxel-based morphometry and stereology provide convergent evidence of the importance of medial prefrontal cortex for fluid intelligence in healthy adults. Neuroimage 25, 11751186.CrossRefGoogle ScholarPubMed
Gonzalez-Blanch, C, Crespo-Facorro, B, Alvarez-Jimenez, M, Rodriguez-Sanchez, JM, Pelayo-Teran, JM, Perez-Iglesias, R, Vazquez-Barquero, JL (2007). Cognitive dimensions in first-episode schizophrenia spectrum disorders. Journal of Psychiatric Research 41, 968977.CrossRefGoogle ScholarPubMed
Good, CD, Johnsrude, IS, Ashburner, J, Henson, RN, Friston, KJ, Frackowiak, RS (2001). A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14, 2136.CrossRefGoogle ScholarPubMed
Haller, S, Borgwardt, SJ, Schindler, C, Aston, J, Radue, EW, Riecher-Rossler, A (2009). Can cortical thickness asymmetry analysis contribute to detection of at-risk mental state and first-episode psychosis? A pilot study. Radiology 250, 212221.CrossRefGoogle ScholarPubMed
Hamilton, LS, Narr, KL, Luders, E, Szeszko, PR, Thompson, PM, Bilder, RM, Toga, AW (2007). Asymmetries of cortical thickness: effects of handedness, sex, and schizophrenia. Neuroreport 18, 14271431.CrossRefGoogle ScholarPubMed
Harris, G, Andreasen, NC, Cizadlo, T, Bailey, JM, Bockholt, HJ, Magnotta, VA, Arndt, S (1999). Improving tissue classification in MRI: a three-dimensional multispectral discriminant analysis method with automated training class selection. Journal of Computer Assisted Tomography 23, 144154.CrossRefGoogle ScholarPubMed
Hilgetag, CC, Barbas, H (2006). Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Computational Biology 2, e22.CrossRefGoogle ScholarPubMed
Karama, S, Ad-Dab'bagha, Y, Haierb, RJ, Dearyc, IJ, Lytteltona, OC, Lepagea, C, Evansa, AC (2009). Positive association between cognitive ability and cortical thickness in a representative US sample of healthy 6 to 18 year-olds. Intelligence 37, 145155.CrossRefGoogle Scholar
Kruggel, F, Bruckner, MK, Arendt, T, Wiggins, CJ, von Cramon, DY (2003). Analyzing the neocortical fine-structure. Medical Image Analysis 7, 251264.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 of General Psychiatry 60, 878888.CrossRefGoogle ScholarPubMed
Magnotta, VA, Andreasen, NC, Schultz, SK, Harris, G, Cizadlo, T, Heckel, D, Nopoulos, P, Flaum, M (1999). Quantitative in vivo measurement of gyrification in the human brain: changes associated with aging. Cerebral Cortex 9, 151160.CrossRefGoogle ScholarPubMed
Magnotta, VA, Harris, G, Andreasen, NC, O'Leary, DS, Yuh, WT, Heckel, D (2002). Structural MR image processing using the BRAINS2 toolbox. Computerized Medical Imaging and Graphics 26, 251264.CrossRefGoogle ScholarPubMed
Morrison, JH, Hof, PR (1997). Life and death of neurons in the aging brain. Science 278, 412419.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 a). Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cerebral Cortex 15, 708719.CrossRefGoogle ScholarPubMed
Narr, KL, Sharma, T, Woods, RP, Thompson, PM, Sowell, ER, Rex, D, Kim, S, Asuncion, D, Jang, S, Mazziotta, J, Toga, AW (2003). Increases in regional subarachnoid CSF without apparent cortical gray matter deficits in schizophrenia: modulating effects of sex and age. American Journal of Psychiatry 160, 21692180.CrossRefGoogle ScholarPubMed
Narr, KL, Toga, AW, Szeszko, P, Thompson, PM, Woods, RP, Robinson, D, Sevy, S, Wang, Y, Schrock, K, Bilder, RM (2005 b). Cortical thinning in cingulate and occipital cortices in first episode schizophrenia. Biological Psychiatry 58, 3240.CrossRefGoogle ScholarPubMed
Nesvag, R, Lawyer, G, Varnas, K, Fjell, AM, Walhovd, KB, Frigessi, A, Jonsson, EG, Agartz, I (2008). Regional thinning of the cerebral cortex in schizophrenia: effects of diagnosis, age and antipsychotic medication. Schizophrenia Research 98, 1628.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Overall, JE, Gorman, DR (1962). The Brief Psychiatric Rating Scale. Psychology Report 10, 799821.CrossRefGoogle Scholar
Pelayo-Terán, JM, Pérez-Iglesias, R, Ramírez-Bonilla, M, González-Blanch, C, Martínez-García, O, Pardo-García, G, Rodríguez-Sánchez, JM, Roiz-Santiáñez, R, Tordesillas-Gutiérrez, D, Mata, I, Vázquez-Barquero, JL, Crespo-Facorro, B (2008). Epidemiological factors associated with treated incidence of first-episode non-affective psychosis in Cantabria: insights from the Clinical Programme on Early Phases of Psychosis. Early Intervention in Psychiatry 2, 178187.CrossRefGoogle ScholarPubMed
Rajkowska, G (1997). Morphometric methods for studying the prefrontal cortex in suicide victims and psychiatric patients. Annals of the New York Academy of Sciences 836, 353–268.CrossRefGoogle ScholarPubMed
Rockel, AJ, Hiorns, RW, Powell, TP (1980). The basic uniformity in structure of the neocortex. Brain 103, 221244.CrossRefGoogle ScholarPubMed
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, 365375.CrossRefGoogle ScholarPubMed
Salgado-Pineda, P, Junqué, C, Vendrell, P, Baeza, I, Bargalló, N, Falcón, C, Bernardo, M (2004). Decreased cerebral activation during CPT performance: structural and functional deficits in schizophrenic patients. Neuroimage 21, 840847.CrossRefGoogle ScholarPubMed
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, 402412.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
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, 676679.CrossRefGoogle ScholarPubMed
Sowell, ER, Thompson, PM, Welcome, SE, Henkenius, AL, Toga, AW, Peterson, BS (2003). Cortical abnormalities in children and adolescents with attention-deficit hyperactivity disorder. Lancet 362, 1699–707.CrossRefGoogle ScholarPubMed
Venkatasubramanian, G, Jayakumar, PN, Gangadhar, BN, Keshavan, MS (2008). Automated MRI parcellation study of regional volume and thickness of prefrontal cortex (PFC) in antipsychotic-naive schizophrenia. Acta Psychiatrica Scandinavica 117, 420431.CrossRefGoogle ScholarPubMed
Weinberger, DR, McClure, RK (2002). Neurotoxicity, neuroplasticity, and magnetic resonance imaging morphometry: what is happening in the schizophrenic brain? Archives of General Psychiatry 59, 553558.CrossRefGoogle ScholarPubMed
Weiss, EM, Siedentopf, C, Golaszewski, S, Mottaghy, FM, Hofer, A, Kremser, C, Felber, S, Fleischhacker, WW (2007). Brain activation patterns during a selective attention test – a functional MRI study in healthy volunteers and unmedicated patients during an acute episode of schizophrenia. Psychiatry Research 15, 154, 3140.CrossRefGoogle Scholar
White, T, Andreasen, NC, Nopoulos, P, Magnotta, V (2003). Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biological Psychiatry 54, 418426.CrossRefGoogle ScholarPubMed
Wiegand, LC, Warfield, SK, Levitt, JJ, Hirayasu, Y, Salisbury, DF, Heckers, S, Dickey, CC, Kikinis, R, Jolesz, FA, McCarley, RW, Shenton, ME (2004). Prefrontal cortical thickness in first-episode psychosis: a magnetic resonance imaging study. Biological Psychiatry 55, 131140.CrossRefGoogle ScholarPubMed
Supplementary material: File

Crespo-Facorro Supplementary Material

Table.doc

Download Crespo-Facorro Supplementary Material(File)
File 77.3 KB