Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T18:31:41.114Z Has data issue: false hasContentIssue false
  • English
  • Français

Cortical folding in Broca's area relates to obstetric complications in schizophrenia patients and healthy controls

Published online by Cambridge University Press:  26 October 2011

U. K. Haukvik ,
M. Schaer ,
R. Nesvåg ,
T. McNeil ,
C. B. Hartberg ,
E. G. Jönsson ,
S. Eliez  and
I. Agartz
U. K. Haukvik*
Affiliation:
Department of Clinical Medicine, section Vinderen, University of Oslo, Norway Department of Psychiatry, Diakonhjemmet Hospital, Oslo, Norway
M. Schaer
Affiliation:
Office Médico-Pédagogique, Department of Psychiatry, Geneva University School of Medicine, Geneva, Switzerland
R. Nesvåg
Affiliation:
Department of Clinical Medicine, section Vinderen, University of Oslo, Norway Department of Psychiatry, Diakonhjemmet Hospital, Oslo, Norway
T. McNeil
Affiliation:
Department of Psychiatric Epidemiology, Lund University Hospital USiL, Lund, Sweden School of Psychiatry and Clinical Neurosciences, University of Western Australia, Perth, Australia
C. B. Hartberg
Affiliation:
Department of Clinical Medicine, section Vinderen, University of Oslo, Norway Department of Psychiatry, Diakonhjemmet Hospital, Oslo, Norway
E. G. Jönsson
Affiliation:
Department of Clinical Neuroscience, HUBIN project, Karolinska Institutet and Hospital, Stockholm, Sweden
S. Eliez
Affiliation:
Office Médico-Pédagogique, Department of Psychiatry, Geneva University School of Medicine, Geneva, Switzerland
I. Agartz
Affiliation:
Department of Clinical Medicine, section Vinderen, University of Oslo, Norway Department of Clinical Neuroscience, HUBIN project, Karolinska Institutet and Hospital, Stockholm, Sweden Department of Psychiatric Research, Diakonhjemmet Hospital, Oslo, Norway
*
*Address for correspondence: U. K. Haukvik MD, PhD, Department of Clinical Medicine, University of Oslo, P.O. Box 85 Vinderen, N-0319 Oslo, Norway. (Email: unn.haukvik@medisin.uio.no)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

The increased occurrence of obstetric complications (OCs) in patients with schizophrenia suggests that alterations in neurodevelopment may be of importance to the aetiology of the illness. Abnormal cortical folding may reflect subtle deviation from normal neurodevelopment during the foetal or neonatal period. In the present study, we hypothesized that OCs would be related to cortical folding abnormalities in schizophrenia patients corresponding to areas where patients with schizophrenia display altered cortical folding when compared with healthy controls.

Method

In total, 54 schizophrenia patients and 54 healthy control subjects underwent clinical examination and magnetic resonance image scanning on a 1.5 T scanner. Information on OCs was collected from original birth records. An automated algorithm was used to calculate a three-dimensional local gyrification index (lGI) at numerous points across the cortical mantle.

Results

In both schizophrenia patients and healthy controls, an increasing number of OCs was significantly related to lower lGI in the left pars triangularis (p<0.0005) in Broca's area. For five other anatomical cortical parcellations in the left hemisphere, a similar trend was demonstrated. No significant relationships between OCs and lGI were found in the right hemisphere and there were no significant case–control differences in lGI.

Conclusions

The reduced cortical folding in the left pars triangularis, associated with OCs in both patients and control subjects suggests that the cortical effect of OCs is caused by factors shared by schizophrenia patients and healthy controls rather than factors related to schizophrenia alone.

Keywords

Broca's areagyrificationMRIneurodevelopmentobstetric complicationsschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 6 , June 2012 , pp. 1329 - 1337
Copyright
Copyright © Cambridge University Press 2011

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

Amunts, K, Zilles, K (2006). A multimodal analysis of structure and function in broca's region. In Broca's Region (ed. Grodzinsky, Y. and Amunts, K.), pp. 17–30. Oxford University Press: New York.CrossRefGoogle Scholar
Armstrong, E, Schleicher, A, Omran, H, Curtis, M, Zilles, K (1995). The ontogeny of human gyrification. Cerebral Cortex 5, 56–63.CrossRefGoogle ScholarPubMed
Arnoudse-Moens, CS, Weisglas-Kuperus, N, van Goudoever, JB, Oosterlaan, J (2009). Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics 124, 717–728.CrossRefGoogle Scholar
Badre, D, Wagner, AD (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia 45, 2883–2901.CrossRefGoogle ScholarPubMed
Bartley, AJ, Jones, DW, Weinberger, DR (1997). Genetic variability of human brain size and cortical gyral patterns. Brain 120 (Pt 2), 257–269.CrossRefGoogle ScholarPubMed
Bhojraj, TS, Francis, AN, Rajarethinam, R, Eack, S, Kulkarni, S, Prasad, KM, Montrose, DM, Dworakowski, D, Diwadkar, V, Keshavan, MS (2009). Verbal fluency deficits and altered lateralization of language brain areas in individuals genetically predisposed to schizophrenia. Schizophrenia Research 115, 202–208.CrossRefGoogle ScholarPubMed
Boksa, P (2004). Animal models of obstetric complications in relation to schizophrenia. Brain Research Brain Research Reviews 45, 1–17.CrossRefGoogle ScholarPubMed
Bonnici, HM, William, T, Moorhead, J, Stanfield, AC, Harris, JM, Owens, DG, Johnstone, EC, Lawrie, SM (2007). Pre-frontal lobe gyrification index in schizophrenia, mental retardation and comorbid groups: an automated study. Neuroimage 35, 648–654.CrossRefGoogle ScholarPubMed
Cachia, A, Paillere-Martinot, ML, Galinowski, A, Januel, D, de, BR, Bellivier, F, Artiges, E, Andoh, J, Bartres-Faz, D, Duchesnay, E, Riviere, D, Plaze, M, Mangin, JF, Martinot, JL (2008). Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations. Neuroimage 39, 927–935.CrossRefGoogle ScholarPubMed
Cannon, TD, van Erp, TG, Rosso, IM, Huttunen, M, Lonnqvist, J, Pirkola, T, Salonen, O, Valanne, L, Poutanen, VP, Standertskjold-Nordenstam, CG (2002). Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Archives of General Psychiatry 59, 35–41.CrossRefGoogle ScholarPubMed
Demb, JB, Desmond, JE, Wagner, AD, Vaidya, CJ, Glover, GH, Gabrieli, JD (1995). Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity. Journal of Neuroscience 15, 5870–5878.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, 968–980.CrossRefGoogle ScholarPubMed
Dubois, J, Benders, M, Borradori-Tolsa, C, Cachia, A, Lazeyras, F, Ha-Vinh, LR, Sizonenko, SV, Warfield, SK, Mangin, JF, Huppi, PS (2008). Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131, 2028–2041.CrossRefGoogle ScholarPubMed
Ebner, F, Tepest, R, Dani, I, Pfeiffer, U, Schulze, TG, Rietschel, M, Maier, W, Traber, F, Block, W, Schild, HH, Wagner, M, Steinmetz, H, Gaebel, W, Honer, WG, Schneider-Axmann, T, Falkai, P (2008). The hippocampus in families with schizophrenia in relation to obstetric complications. Schizophrenia Research 104, 71–78.CrossRefGoogle ScholarPubMed
Ekholm, B, Ekholm, A, Adolfsson, R, Vares, M, Osby, U, Sedvall, GC, Jonsson, EG (2005). Evaluation of diagnostic procedures in Swedish patients with schizophrenia and related psychoses. Nordic Journal of Psychiatry 59, 457–464.CrossRefGoogle ScholarPubMed
Falkai, P, Honer, WG, Kamer, T, Dustert, S, Vogeley, K, Schneider-Axmann, T, Dani, I, Wagner, M, Rietschel, M, Muller, DJ, Schulze, TG, Gaebel, W, Cordes, J, Schonell, H, Schild, HH, Block, W, Traber, F, Steinmetz, H, Maier, W, Tepest, R (2007). Disturbed frontal gyrification within families affected with schizophrenia. Journal of Psychiatric Research 41, 805–813.CrossRefGoogle ScholarPubMed
Falkai, P, Schneider-Axmann, T, Honer, WG, Vogeley, K, Schonell, H, Pfeiffer, U, Scherk, H, Block, W, Traber, F, Schild, HH, Maier, W, Tepest, R (2003). Influence of genetic loading, obstetric complications and premorbid adjustment on brain morphology in schizophrenia: a MRI study. European Archives of Psychiatry and Clinical Neuroscience 253, 92–99.CrossRefGoogle ScholarPubMed
Fatemi, SH, Folsom, TD (2009). The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophrenia Bulletin 35, 528–548.CrossRefGoogle ScholarPubMed
Fiebach, CJ, Schlesewsky, M, Lohmann, G, von Cramon, DY, Friederici, AD (2005). Revisiting the role of Broca's area in sentence processing: syntactic integration versus syntactic working memory. Human Brain Mapping 24, 79–91.CrossRefGoogle ScholarPubMed
Friederici, AD, Ruschemeyer, SA, Hahne, A, Fiebach, CJ (2003). The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. Cerebral Cortex 13, 170–177.CrossRefGoogle ScholarPubMed
Genovese, CR, Lazar, NA, Nichols, T (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870–878.CrossRefGoogle ScholarPubMed
Glahn, DC, Laird, AR, Ellison-Wright, I, Thelen, SM, Robinson, JL, Lancaster, JL, Bullmore, E, Fox, PT (2008). Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biological Psychiatry 64, 774–781.CrossRefGoogle ScholarPubMed
Harris, JM, Moorhead, TW, Miller, P, McIntosh, AM, Bonnici, HM, Owens, DG, Johnstone, EC, Lawrie, SM (2007). Increased prefrontal gyrification in a large high-risk cohort characterizes those who develop schizophrenia and reflects abnormal prefrontal development. Biological Psychiatry 62, 722–729.CrossRefGoogle Scholar
Harris, JM, Whalley, H, Yates, S, Miller, P, Johnstone, EC, Lawrie, SM (2004 a). Abnormal cortical folding in high-risk individuals: a predictor of the development of schizophrenia? Biological Psychiatry 56, 182–189.CrossRefGoogle ScholarPubMed
Harris, JM, Yates, S, Miller, P, Best, JJ, Johnstone, EC, Lawrie, SM (2004 b). Gyrification in first-episode schizophrenia: a morphometric study. Biological Psychiatry 55, 141–147.CrossRefGoogle ScholarPubMed
Haukvik, UK, Lawyer, G, Bjerkan, PS, Hartberg, CB, Jonsson, EG, McNeil, T, Agartz, I (2009). Cerebral cortical thickness and a history of obstetric complications in schizophrenia. Journal of Psychiatric Research 43, 1287–1293.CrossRefGoogle Scholar
Haukvik, UK, McNeil, T, Nesvag, R, Soderman, E, Jonsson, E, Agartz, I (2010). No effect of obstetric complications on basal ganglia volumes in schizophrenia. Progress in Neuropsychopharmacology and Biological Psychiatry 34, 619–623.CrossRefGoogle ScholarPubMed
Highley, JR, DeLisi, LE, Roberts, N, Webb, JA, Relja, M, Razi, K, Crow, TJ (2003). Sex-dependent effects of schizophrenia: an MRI study of gyral folding, and cortical and white matter volume. Psychiatry Research. 124, 11–23.CrossRefGoogle ScholarPubMed
Honea, R, Crow, TJ, Passingham, D, Mackay, CE (2005). Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. American Journal of Psychiatry 162, 2233–2245.CrossRefGoogle ScholarPubMed
Janssen, J, Reig, S, Aleman, Y, Schnack, H, Udias, JM, Parellada, M, Graell, M, Moreno, D, Zabala, A, Balaban, E, Desco, M, Arango, C (2009). Gyral and sulcal cortical thinning in adolescents with first episode early-onset psychosis. Biological Psychiatry 66, 1047–1054.CrossRefGoogle ScholarPubMed
Jonsson, EG, Edman-Ahlbom, B, Sillen, A, Gunnar, A, Kulle, B, Frigessi, A, Vares, M, Ekholm, B, Wode-Helgodt, B, Schumacher, J, Cichon, S, Agartz, I, Sedvall, GC, Hall, H, Terenius, L (2006). Brain-derived neurotrophic factor gene (BDNF) variants and schizophrenia: an association study. Progress in Neuropsychopharmacology and Biological Psychiatry 30, 924–933.CrossRefGoogle ScholarPubMed
Kesler, SR, Vohr, B, Schneider, KC, Katz, KH, Makuch, RW, Reiss, AL, Ment, LR (2006). Increased temporal lobe gyrification in preterm children. Neuropsychologia 44, 445–453.CrossRefGoogle ScholarPubMed
Lewis, SW, Murray, RM (1987). Obstetric complications, neurodevelopmental deviance, and risk of schizophrenia. Journal of Psychiatric Research 21, 413–421.CrossRefGoogle ScholarPubMed
McNeil, T, Sjostrom, K (1995). The McNeil-Sjöström Scale for Obstetric Complications. University Hospital, Department of Psychiatry: Malmö.Google Scholar
McNeil, TF, Cantor-Graae, E, Sjostrom, K (1994). Obstetric complications as antecedents of schizophrenia: empirical effects of using different obstetric complication scales. Journal of Psychiatric Research 28, 519–530.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Marenco, S, Weinberger, DR (2000). The neurodevelopmental hypothesis of schizophrenia: following a trail of evidence from cradle to grave. Developmental Psychopathology 12, 501–527.CrossRefGoogle ScholarPubMed
Mesholam-Gately, RI, Giuliano, AJ, Goff, KP, Faraone, SV, Seidman, LJ (2009). Neurocognition in first-episode schizophrenia: a meta-analytic review. Neuropsychology 23, 315–336.CrossRefGoogle ScholarPubMed
Piao, X, Hill, RS, Bodell, A, Chang, BS, Basel-Vanagaite, L, Straussberg, R, Dobyns, WB, Qasrawi, B, Winter, RM, Innes, AM, Voit, T, Ross, ME, Michaud, JL, Descarie, JC, Barkovich, AJ, Walsh, CA (2004). G protein-coupled receptor-dependent development of human frontal cortex. Science 303, 2033–2036.CrossRefGoogle ScholarPubMed
Sallet, PC, Elkis, H, Alves, TM, Oliveira, JR, Sassi, E, Campi, de CC, Busatto, GF, Gattaz, WF (2003). Reduced cortical folding in schizophrenia: an MRI morphometric study. American Journal of Psychiatry 160, 1606–1613.CrossRefGoogle ScholarPubMed
Schaer, M, Cuadra, MB, Tamarit, L, Lazeyras, F, Eliez, S, Thiran, JP (2008). A surface-based approach to quantify local cortical gyrification. IEEE Transactions on Medical Imaging 27, 161–170.CrossRefGoogle ScholarPubMed
Schaer, M, Glaser, B, Cuadra, MB, Debbane, M, Thiran, JP, Eliez, S (2009). Congenital heart disease affects local gyrification in 22q11.2 deletion syndrome. Developmental Medicine and Child Neurology 51, 746–753.CrossRefGoogle ScholarPubMed
Schulze, K, McDonald, C, Frangou, S, Sham, P, Grech, A, Toulopoulou, T, Walshe, M, Sharma, T, Sigmundsson, T, Taylor, M, Murray, RM (2003). Hippocampal volume in familial and nonfamilial schizophrenic probands and their unaffected relatives. Biological Psychiatry 53, 562–570.CrossRefGoogle ScholarPubMed
Selemon, LD, Mrzljak, J, Kleinman, JE, Herman, MM, Goldman-Rakic, PS (2003). Regional specificity in the neuropathologic substrates of schizophrenia: a morphometric analysis of Broca's area 44 and area 9. Archives of General Psychiatry 60, 69–77.CrossRefGoogle ScholarPubMed
Smieskova, R, Fusar-Poli, P, Allen, P, Bendfeldt, K, Stieglitz, RD, Drewe, J, Radue, EW, McGuire, PK, Riecher-Rossler, A, Borgwardt, SJ (2009). The effects of antipsychotics on the brain: what have we learnt from structural imaging of schizophrenia? A systematic review. Current Pharmaceutical Design 15, 2535–2549.CrossRefGoogle ScholarPubMed
Spitzer, RL (1988). Structured Clinical Interview for DSM-III-R- Patient Version. Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Steen, RG, Mull, C, McClure, R, Hamer, RM, Lieberman, JA (2006). Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. British Journal of Psychiatry 188, 510–518.CrossRefGoogle ScholarPubMed
Stevens, CP, Raz, S, Sander, CJ (1999). Peripartum hypoxic risk and cognitive outcome: a study of term and preterm birth children at early school age. Neuropsychology 13, 598–608.CrossRefGoogle ScholarPubMed
Tanskanen, P, Ridler, K, Murray, GK, Haapea, M, Veijola, JM, Jaaskelainen, E, Miettunen, J, Jones, PB, Bullmore, ET, Isohanni, MK (2008). Morphometric brain abnormalities in schizophrenia in a population-based sample: relationship to duration of illness. Schizophrenia Bulletin 36, 766–777.CrossRefGoogle Scholar
Taylor, HG, Minich, NM, Klein, N, Hack, M (2004). Longitudinal outcomes of very low birth weight: neuropsychological findings. Journal of the International Neuropsychological Society 10, 149–163.CrossRefGoogle ScholarPubMed
van Erp, TG, Saleh, PA, Rosso, IM, Huttunen, M, Lonnqvist, J, Pirkola, T, Salonen, O, Valanne, L, Poutanen, VP, Standertskjold-Nordenstam, CG, Cannon, TD (2002). Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. American Journal of Psychiatry 159, 1514–1520.CrossRefGoogle ScholarPubMed
van Haren, NE, Bakker, SC, Kahn, RS (2008). Genes and structural brain imaging in schizophrenia. Current Opinion in Psychiatry 21, 161–167.CrossRefGoogle ScholarPubMed
van Haren, NE, Hulshoff Pol, HE, Schnack, HG, Cahn, W, Mandl, RC, Collins, DL, Evans, AC, Kahn, RS (2007). Focal gray matter changes in schizophrenia across the course of the illness: a 5-year follow-up study. Neuropsychopharmacology 32, 2057–2066.CrossRefGoogle ScholarPubMed
van Essen, DC (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318.CrossRefGoogle ScholarPubMed
Vares, M, Ekholm, A, Sedvall, GC, Hall, H, Jonsson, EG (2006). Characterization of patients with schizophrenia and related psychoses: evaluation of different diagnostic procedures. Psychopathology 39, 286–295.CrossRefGoogle ScholarPubMed
Vogeley, K, Schneider-Axmann, T, Pfeiffer, U, Tepest, R, Bayer, TA, Bogerts, B, Honer, WG, Falkai, P (2000). Disturbed gyrification of the prefrontal region in male schizophrenic patients: a morphometric postmortem study. American Journal of Psychiatry 157, 34–39.CrossRefGoogle ScholarPubMed
Vogeley, K, Tepest, R, Pfeiffer, U, Schneider-Axmann, T, Maier, W, Honer, WG, Falkai, P (2001). Right frontal hypergyria differentiation in affected and unaffected siblings from families multiply affected with schizophrenia: a morphometric MRI study. American Journal of Psychiatry 158, 494–496.CrossRefGoogle ScholarPubMed
Weinberger, DR (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 44, 660–669.CrossRefGoogle ScholarPubMed
White, T, Andreasen, NC, Nopoulos, P, Magnotta, V (2003). Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biological Psychiatry 54, 418–426.CrossRefGoogle ScholarPubMed
White, T, Su, S, Schmidt, M, Kao, CY, Sapiro, G (2010). The development of gyrification in childhood and adolescence. Brain and Cognition 72, 36–45.CrossRefGoogle ScholarPubMed
Wing, JK, Babor, T, Brugha, T, Burke, J, Cooper, JE, Giel, R, Jablenski, A, Regier, D, Sartorius, N (1990). SCAN. Schedules for clinical assessment in neuropsychiatry. Archives of General Psychiatry 47, 589–593.CrossRefGoogle ScholarPubMed
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, 317–327.CrossRefGoogle ScholarPubMed
Zilles, K, Armstrong, E, Schleicher, A, Kretschmann, HJ (1988). The human pattern of gyrification in the cerebral cortex. Anatomy and Embryology (Berlin) 179, 173–179.CrossRefGoogle ScholarPubMed
Supplementary material: File

Haukvik Supplementary Material

Haukvik Supplementary Material

Download Haukvik Supplementary Material(File)
File 136.2 KB
Supplementary material: PDF

Haukvik Supplementary Figure 1

Supplementary Fig. 1 (Fig. S1) Differences in local gyrification between patients and control subjects at p< 0.01 co-varied for age and gender, without FDR correction. Within the coloured areas, patients demonstrate lower cortical folding than healthy control subjects. None of the findings are significant after adjustment for multiple comparisons.

Download Haukvik Supplementary Figure 1(PDF)
PDF 1.7 MB
Supplementary material: PDF

Haukvik Supplementary Figure 2

Supplementary Fig. 2 (Fig. S2) The effect of increasing number of obstetric complications on local gyrification in schizophrenia patients, healthy controls, and the combined sample, co-varied for age and gender at two different p-levels without FDR correction. None of the findings are significant after adjustment for multiple comparisons.

Download Haukvik Supplementary Figure 2(PDF)
PDF 6.6 MB