Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-04T19:51:18.553Z Has data issue: false hasContentIssue false
  • English
  • Français

Common variation in NCAN, a risk factor for bipolar disorder and schizophrenia, influences local cortical folding in schizophrenia

Published online by Cambridge University Press:  24 June 2013

C. C. Schultz ,
T. W. Mühleisen ,
I. Nenadic ,
K. Koch ,
G. Wagner ,
C. Schachtzabel ,
F. Siedek ,
M. M. Nöthen ,
M. Rietschel  and
T. Deufel
...Show all authors
C. C. Schultz*
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany
T. W. Mühleisen
Affiliation:
Institute of Human Genetics, University of Bonn, Germany Department of Genomics, Life and Brain Centre, University of Bonn, Germany Institute of Neuroscience and Medicine (INM-1), Research Centre Juelich, Germany
I. Nenadic
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany
K. Koch
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany Department of Neuroradiology, Klinikum rechts der Isar, Technische Universität München, Germany
G. Wagner
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany
C. Schachtzabel
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany
F. Siedek
Affiliation:
Institute of Human Genetics, University of Bonn, Germany Department of Genomics, Life and Brain Centre, University of Bonn, Germany
M. M. Nöthen
Affiliation:
Institute of Human Genetics, University of Bonn, Germany Department of Genomics, Life and Brain Centre, University of Bonn, Germany German Centre for Neurodegenerative Diseases (DZNE), Bonn, Germany
M. Rietschel
Affiliation:
Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Germany
T. Deufel
Affiliation:
Department of Clinical Chemistry and Laboratory Diagnostics, Jena University Hospital, Germany
M. Kiehntopf
Affiliation:
Department of Clinical Chemistry and Laboratory Diagnostics, Jena University Hospital, Germany
S. Cichon
Affiliation:
Institute of Human Genetics, University of Bonn, Germany Department of Genomics, Life and Brain Centre, University of Bonn, Germany Institute of Neuroscience and Medicine (INM-1), Research Centre Juelich, Germany Division of Medical Genetics, University of Basel, Switzerland
J. R. Reichenbach
Affiliation:
Medical Physics Group, Institute for Diagnostic and Interventional Radiology I, Jena University Hospital, Germany
H. Sauer
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany
R. G. M. Schlösser
Affiliation:
Department of Psychiatry and Psychotherapy, Jena University Hospital, Germany
*
* Address for correspondence: C. C. Schultz, M.D., Department of Psychiatry and Psychotherapy, Jena University Hospital, Philosophenweg 3, 07740 Jena, Germany. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Recent studies have provided strong evidence that variation in the gene neurocan (NCAN, rs1064395) is a common risk factor for bipolar disorder (BD) and schizophrenia. However, the possible relevance of NCAN variation to disease mechanisms in the human brain has not yet been explored. Thus, to identify a putative pathomechanism, we tested whether the risk allele has an influence on cortical thickness and folding in a well-characterized sample of patients with schizophrenia and healthy controls.

Method

Sixty-three patients and 65 controls underwent T1-weighted magnetic resonance imaging (MRI) and were genotyped for the single nucleotide polymorphism (SNP) rs1064395. Folding and thickness were analysed on a node-by-node basis using a surface-based approach (FreeSurfer).

Results

In patients, NCAN risk status (defined by AA and AG carriers) was found to be associated with higher folding in the right lateral occipital region and at a trend level for the left dorsolateral prefrontal cortex. Controls did not show any association (p > 0.05). For cortical thickness, there was no significant effect in either patients or controls.

Conclusions

This study is the first to describe an effect of the NCAN risk variant on brain structure. Our data show that the NCAN risk allele influences cortical folding in the occipital and prefrontal cortex, which may establish disease susceptibility during neurodevelopment. The findings suggest that NCAN is involved in visual processing and top-down cognitive functioning. Both major cognitive processes are known to be disturbed in schizophrenia. Moreover, our study reveals new evidence for a specific genetic influence on local cortical folding in schizophrenia.

Keywords

Cerebral cortexhypergyrificationSNPV1V2visual system
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 4 , March 2014 , pp. 811 - 820
Copyright
Copyright © Cambridge University Press 2013 

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

Adcock, RA, Dale, C, Fisher, M, Aldebot, S, Genevsky, A, Simpson, GV, Nagarajan, S, Vinogradov, S (2009). When top-down meets bottom-up: auditory training enhances verbal memory in schizophrenia. Schizophrenia Bulletin 35, 1132–1141.CrossRefGoogle ScholarPubMed
Annett, M (1967). The binomial distribution of right, mixed and left handedness. Quarterly Journal of Experimental Psychology 19, 327–333.Google Scholar
Armstrong, E, Schleicher, A, Omran, H, Curtis, M, Zilles, K (1991). The ontogeny of human gyrification. Cerebral Cortex 5, 56–63.CrossRefGoogle Scholar
Butler, PD, Javitt, DC (2005). Early-stage visual processing deficits in schizophrenia. Current Opinion in Psychiatry 18, 151–157.Google Scholar
Cichon, S, Mühleisen, TW, Degenhardt, FA, Mattheisen, M, Miró, X, Strohmaier, J, Steffens, M, Meesters, C, Herms, S, Weingarten, M, Priebe, L, Haenisch, B, Alexander, M, Vollmer, J, Breuer, R, Schmäl, C, Tessmann, P, Moebus, S, Wichmann, HE, Schreiber, S, Müller-Myhsok, B, Lucae, S, Jamain, S, Leboyer, M, Bellivier, F, Etain, B, Henry, C, Kahn, JP, Heath, S; Bipolar Disorder Genome Study (BiGS) Consortium, Hamshere, M, O'Donovan, MC, Owen, MJ, Craddock, N, Schwarz, M, Vedder, H, Kammerer-Ciernioch, J, Reif, A, Sasse, J, Bauer, M, Hautzinger, M, Wright, A, Mitchell, PB, Schofield, PR, Montgomery, GW, Medland, SE, Gordon, SD, Martin, NG, Gustafsson, O, Andreassen, O, Djurovic, S, Sigurdsson, E, Steinberg, S, Stefansson, H, Stefansson, K, Kapur-Pojskic, L, Oruc, L, Rivas, F, Mayoral, F, Chuchalin, A, Babadjanova, G, Tiganov, AS, Pantelejeva, G, Abramova, LI, Grigoroiu-Serbanescu, M, Diaconu, CC, Czerski, PM, Hauser, J, Zimmer, A, Lathrop, M, Schulze, TG, Wienker, TF, Schumacher, J, Maier, W, Propping, P, Rietschel, M, Nöthen, MM (2011). Genome-wide association study identifies genetic variation in neurocan as a susceptibility factor for bipolar disorder. American Journal of Human Genetics 88, 372–381.CrossRefGoogle ScholarPubMed
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179–194.Google Scholar
Dauvermann, MR, Mukherjee, P, Moorhead, WT, Stanfield, AC, Fusar-Poli, P, Lawrie, SM, Whalley, HC (2012). Relationship between gyrification and functional connectivity of the prefrontal cortex in subjects at high genetic risk of schizophrenia. Current Pharmaceutical Design 18, 434–442.Google Scholar
Erk, S, Meyer-Lindenberg, A, Schnell, K, Opitz von Boberfeld, C, Esslinger, C, Kirsch, P, Grimm, O, Arnold, C, Haddad, L, Witt, SH, Cichon, S, Nöthen, MM, Rietschel, M, Walter, H (2010). Brain function in carriers of a genome-wide supported bipolar disorder variant. Archives of General Psychiatry 67, 803–811.Google Scholar
Esslinger, C, Walter, H, Kirsch, P, Erk, S, Schnell, K, Arnold, C, Haddad, L, Mier, D, Opitz von Boberfeld, C, Raab, K, Witt, SH, Rietschel, M, Cichon, S, Meyer-Lindenberg, A (2009). Neural mechanisms of a genome-wide supported psychosis variant. Science 324, 605.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 USA 97, 11050–11055.CrossRefGoogle ScholarPubMed
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195–207.CrossRefGoogle Scholar
Forbes, NF, Carrick, LA, McIntosh, AM, Lawrie, SM (2009). Working memory in schizophrenia: a meta-analysis. Psychological Medicine 39, 889–905.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
Frischknecht, R, Seidenbecher, CI (2008). The crosstalk of hyaluronan-based extracellular matrix and synapses. Neuron Glia Biology 4, 249–257.CrossRefGoogle ScholarPubMed
Gaser, C, Luders, E, Thompson, PM, Lee, AD, Dutton, RA, Geaga, JA, Hayashi, KM, Bellugi, U, Galaburda, AM, Korenberg, JR, Mills, DL, Toga, AW, Reiss, A (2006). Increased local gyrification mapped in Williams syndrome. NeuroImage 33, 46–54.Google Scholar
Goldman-Rakic, PS (1980). Morphological consequences of prenatal injury to the primate brain. Progress in Brain Research 53, 1–19.Google Scholar
Green, MF, Nuechterlein, KH, Mintz, J (1994). Backward masking in schizophrenia and mania. II. Specifying the visual channels. Archives of General Psychiatry 51, 945–951.Google Scholar
Hahn, B, Robinson, BM, Kaiser, ST, Harvey, AN, Beck, VM, Leonard, CJ, Kappenman, ES, Luck, SJ, Gold, JM (2010). Failure of schizophrenia patients to overcome salient distractors during working memory encoding. Biological Psychiatry 68, 603–609.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
Hill, SK, Harris, MSH, Herbener, ES, Pavuluri, M, Sweeney, JA (2008). Neurocognitive allied phenotypes for schizophrenia and bipolar disorder. Schizophrenia Bulletin 34, 743–759.Google Scholar
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.Google Scholar
Hugdahl, K (2009). ‘Hearing voices’: auditory hallucinations as failure of top-down control of bottom-up perceptual processes. Scandinavian Journal of Psychology 50, 553–560.Google Scholar
Javitt, DC (2009). When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. Annual Review of Clinical Psychology 5, 249–275.Google Scholar
Johnson, MB, Kawasawa, YI, Mason, CE, Krsnik, Z, Coppola, G, Bogdanović, D, Geschwind, DH, Mane, SM, State, MW, Sestan, N (2009). Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62, 494–509.Google Scholar
Kang, HJ, Kawasawa, YI, Cheng, F, Zhu, Y, Xu, X, Li, M, Sousa, AM, Pletikos, M, Meyer, KA, Sedmak, G, Guennel, T, Shin, Y, Johnson, MB, Krsnik, Z, Mayer, S, Fertuzinhos, S, Umlauf, S, Lisgo, SN, Vortmeyer, A, Weinberger, DR, Mane, S, Hyde, TM, Huttner, A, Reimers, M, Kleinman, JE, Sestan, N (2011). Spatio-temporal transcriptome of the human brain. Nature 478, 483–489.Google Scholar
Karetko, M, Skangiel-Kramska, J (2009). Diverse functions of perineuronal nets. Acta Neurobiologiae Experimentalis 69, 564–577.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Koenigs, M, Barbey, AK, Postle, BR, Grafman, J (2009). Superior parietal cortex is critical for the manipulation of information in working memory. Journal of Neuroscience 29, 14980–14986.Google Scholar
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, 878–888.CrossRefGoogle ScholarPubMed
Luders, E, Thompson, PM, Narr, KL, Toga, AW, Jancke, L, Gaser, C (2006). A curvature-based approach to estimate local gyrification on the cortical surface. NeuroImage 29, 1224–1230.Google Scholar
Mangin, JF, Jouvent, E, Cachia, A (2010). In-vivo measurement of cortical morphology: means and meanings. Current Opinion in Neurology 23, 359–367.Google Scholar
McIntosh, AM, Moorhead, TWJ, McKirdy, J, Hall, J, Sussmann, JED, Stanfield, AC, Harris, JM, Johnstone, EC, Lawrie, SM (2009). Prefrontal gyral folding and its cognitive correlates in bipolar disorder and schizophrenia. Acta Psychiatrica Scandinavica 119, 192–198.Google Scholar
Miller, EK (2000). The prefrontal cortex and cognitive control. Nature Reviews Neuroscience 1, 59–65.Google Scholar
Minzenberg, MJ, Laird, AR, Thelen, S, Carter, CS, Glahn, DC (2009). Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Archives of General Psychiatry 66, 811–822.Google Scholar
Miró, X, Meier, S, Dreisow, ML, Frank, J, Strohmaier, J, Breuer, R, Schmäl, C, Albayram, Ö, Pardo-Olmedilla, MT, Mühleisen, TW, Degenhardt, FA, Mattheisen, M, Reinhard, I, Bilkei-Gorzo, A, Cichon, S, Seidenbecher, C, Rietschel, M, Nöthen, MM, Zimmer, A (2012). Studies in humans and mice implicate neurocan in the etiology of mania. American Journal of Psychiatry 169, 982–990.CrossRefGoogle ScholarPubMed
Mühleisen, TW, Mattheisen, M, Strohmaier, J, Degenhardt, F, Priebe, L, Schultz, CC, Breuer, R, Meier, S, Hoffmann, P; GROUP Investigators, Rivandeneira, F, Hofman, A, Uitterlinden, AG, Moebus, S, Gieger, C, Emeny, R, Ladwig, KH, Wichmann, HE, Schwarz, M, Kammerer-Ciernioch, J, Schlösser, RG, Nenadic, I, Sauer, H, Mössner, R, Maier, W, Rujescu, D, Lange, C, Ophoff, RA, Schulze, TG, Rietschel, M, Nöthen, MM, Cichon, S (2012). Association between schizophrenia and common variation in neurocan (NCAN), a genetic risk factor for bipolar disorder. Schizophrenia Research 138, 69–73.Google Scholar
Narr, KL, Bilder, RM, Kim, S, Thompson, PM, Szeszko, P, Robinson, D, Luders, E, Toga, AW (2004). Abnormal gyral complexity in first-episode schizophrenia. Biological Psychiatry 55, 859–867.Google Scholar
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, 708–719.Google Scholar
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, 32–40.Google Scholar
Nesvåg, R, Lawyer, G, Varnäs, K, Fjell, AM, Walhovd, KB, Frigessi, A, Jönsson, EG, Agartz, I (2008). Regional thinning of the cerebral cortex in schizophrenia: effects of diagnosis, age and antipsychotic medication. Schizophrenia Research 98, 16–28.Google Scholar
Neuhaus, AH, Karl, C, Hahn, E, Trempler, NR, Opgen-Rhein, C, Urbanek, C, Hahn, C, Ta, TM, Dettling, M (2011). Dissection of early bottom-up and top-down deficits during visual attention in schizophrenia. Clinical Neurophysiology 122, 90–98.Google Scholar
Nöthen, MM, Nieratschker, V, Cichon, S, Rietschel, M (2010). New findings in the genetics of major psychoses. Dialogues in Clinical Neuroscience 12, 85–93.Google Scholar
Palaniyappan, L, Mallikarjun, P, Joseph, V, White, TP, Liddle, PF (2011). Folding of the prefrontal cortex in schizophrenia: regional differences in gyrification. Biological Psychiatry 69, 974–979.Google Scholar
Panizzon, MS, Fennema-Notestine, C, Eyler, LT, Jernigan, TL, Prom-Wormley, E, Neale, M, 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, 2728–2735.Google Scholar
Prange, CK, Pennacchio, LA, Lieuallen, K, Fan, W, Lennon, GG (1998). Characterization of the human neurocan gene, CSPG3. Gene 221, 199–205.Google Scholar
Prata, DP, Mechelli, A, Picchioni, MM, Fu, CH, Toulopoulou, T, Bramon, E, Walshe, M, Murray, RM, Collier, DA, McGuire, P (2009). Altered effect of dopamine transporter 3'UTR VNTR genotype on prefrontal and striatal function in schizophrenia. Archives of General Psychiatry 66, 1162–72.Google Scholar
Rauch, U, Feng, K, Zhou, XH (2001). Neurocan: a brain chondroitin sulfate proteoglycan. Cellular and Molecular Life Sciences 58, 1842–1856.Google Scholar
Reichenberg, A, Harvey, PD, Bowie, CR, Mojtabai, R, Rabinowitz, J, Heaton, RK, Bromet, E (2009). Neuropsychological function and dysfunction in schizophrenia and psychotic affective disorders. Schizophrenia Bulletin 35, 1022–1029.Google Scholar
Rietschel, M, Mattheisen, M, Degenhardt, F; Genetic Risk and Outcome in Psychosis (GROUP Investigators), Mühleisen, TW, Kirsch, P, Esslinger, C, Herms, S, Demontis, D, Steffens, M, Strohmaier, J, Haenisch, B, Breuer, R, Czerski, PM, Giegling, I, Strengman, E, Schmael, C, Mors, O, Mortensen, PB, Hougaard, DM, Ørntoft, T, Kapelski, P, Priebe, L, Basmanav, FF, Forstner, AJ, Hoffman, P, Meier, S, Nikitopoulos, J, Moebus, S, Alexander, M, Mössner, R, Wichmann, H-E, Schreiber, S, Rivandeneira, F, Hofman, A, Uitterlinden, AG, Wienker, TF, Schumacher, J, Hauser, J, Maier, W, Cantor, RM, Erk, S, Schulze, TG; SGENE-plus Consortium, Craddock, N, Owen, MJ, O'Donovan, MC, Børglum, AD, Rujescu, D, Walter, H, Meyer-Lindenberg, A, Nöthen, NM, Ophoff, RA, Cichon, S (2011). Association between genetic variation in a region on chromosome 11 and schizophrenia in large samples from Europe. Molecular Psychiatry 17, 906–917.Google Scholar
Rogers, J, Kochunov, P, Zilles, K, Shelledy, W, Lancaster, J, Thompson, P, Duggirala, R, Blangero, J, Fox, PT, Glahn, DC (2010). On the genetic architecture of cortical folding and brain volume in primates. NeuroImage 53, 1103–1108.Google Scholar
Schultz, CC, Koch, K, Wagner, G, Roebel, M, Nenadic, I, Gaser, C, Schachtzabel, C, Reichenbach, JR, Sauer, H, Schlösser, RG (2010 a). Increased parahippocampal and lingual gyrification in first-episode schizophrenia. Schizophrenia Research 123, 137–144.Google Scholar
Schultz, CC, Koch, K, Wagner, G, Roebel, M, Nenadic, I, Schachtzabel, C, Reichenbach, JR, Sauer, H, Schlösser, RG (2010 b). Complex pattern of cortical thinning in schizophrenia: results from an automated surface based analysis of cortical thickness. Psychiatry Research 182, 134–140.Google Scholar
Schultz, CC, Koch, K, Wagner, G, Roebel, M, Schachtzabel, C, Gaser, C, Nenadic, I, Reichenbach, JR, Sauer, H, Schlösser, RG (2010 c). Reduced cortical thickness in first episode schizophrenia. Schizophrenia Research 116, 204–209.Google Scholar
Schultz, CC, Nenadic, I, Koch, K, Wagner, G, Roebel, M, Schachtzabel, C, Mühleisen, TW, Nöthen, MM, Cichon, S, Deufel, T, Kiehntopf, M, Rietschel, M, Reichenbach, JR, Sauer, H, Schlösser, RG (2011). Reduced cortical thickness is associated with the glutamatergic regulatory gene risk variant DAOA Arg30Lys in schizophrenia. Neuropsychopharmacology 36, 1747–1753.Google Scholar
Schultz, CC, Wagner, G, Koch, K, Gaser, C, Roebel, M, Schachtzabel, C, Nenadic, I, Reichenbach, JR, Sauer, H, Schlösser, RG (2013). The visual cortex in schizophrenia: alterations of gyrification rather than cortical thickness – a combined cortical shape analysis. Brain Structure and Function 218, 51–58.Google Scholar
Silbersweig, D, Stern, E (1996). Functional neuroimaging of hallucinations in schizophrenia: toward an integration of bottom-up and top-down approaches. Molecular Psychiatry 1, 367–375.Google Scholar
Stein, JL, Medland, SE, Vasquez, AA, Hibar, DP, Senstad, RE, Winkler, AM, Toro, R, Appel, K, Bartecek, R, Bergmann, Ø, Bernard, M, Brown, AA, Cannon, DM, Chakravarty, MM, Christoforou, A, Domin, M, Grimm, O, Hollinshead, M, Holmes, AJ, Homuth, G, Hottenga, JJ, Langan, C, Lopez, LM, Hansell, NK, Hwang, KS, Kim, S, Laje, G, Lee, PH, Liu, X, Loth, E, Lourdusamy, A, Mattingsdal, M, Mohnke, S, Maniega, SM, Nho, K, Nugent, AC, O'Brien, C, Papmeyer, M, Pütz, B, Ramasamy, A, Rasmussen, J, Rijpkema, M, Risacher, SL, Roddey, JC, Rose, EJ, Ryten, M, Shen, L, Sprooten, E, Strengman, E, Teumer, A, Trabzuni, D, Turner, J, van Eijk, K, van Erp, TG, van Tol, MJ, Wittfeld, K, Wolf, C, Woudstra, S, Aleman, A, Alhusaini, S, Almasy, L, Binder, EB, Brohawn, DG, Cantor, RM, Carless, MA, Corvin, A, Czisch, M, Curran, JE, Davies, G, de Almeida, MA, Delanty, N, Depondt, C, Duggirala, R, Dyer, TD, Erk, S, Fagerness, J, Fox, PT, Freimer, NB, Gill, M, Göring, HH, Hagler, DJ, Hoehn, D, Holsboer, F, Hoogman, M, Hosten, N, Jahanshad, N, Johnson, MP, Kasperaviciute, D, Kent, JW Jr., Kochunov, P, Lancaster, JL, Lawrie, SM, Liewald, DC, Mandl, R, Matarin, M, Mattheisen, M, Meisenzahl, E, Melle, I, Moses, EK, Mühleisen, TW, Nauck, M, Nöthen, MM, Olvera, RL, Pandolfo, M, Pike, GB, Puls, R, Reinvang, I, Rentería, ME, Rietschel, M, Roffman, JL, Royle, NA, Rujescu, D, Savitz, J, Schnack, HG, Schnell, K, Seiferth, N, Smith, C, Steen, VM, Valdés Hernández, MC, Van den Heuvel, M, van der Wee, NJ, Van Haren, NE, Veltman, JA, Völzke, H, Walker, R, Westlye, LT, Whelan, CD, Agartz, I, Boomsma, DI, Cavalleri, GL, Dale, AM, Djurovic, S, Drevets, WC, Hagoort, P, Hall, J, Heinz, A, Jack, CR Jr., Foroud, TM, Le Hellard, S, Macciardi, F, Montgomery, GW, Poline, JB, Porteous, DJ, Sisodiya, SM, Starr, JM, Sussmann, J, Toga, AW, Veltman, DJ, Walter, H, Weiner, MW; Alzheimer's Disease Neuroimaging Initiative; EPIGEN Consortium; IMAGEN Consortium; Saguenay Youth Study Group, Bis, JC, Ikram, MA, Smith, AV, Gudnason, V, Tzourio, C, Vernooij, MW, Launer, LJ, DeCarli, C, Seshadri, S; Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium, Andreassen, OA, Apostolova, LG, Bastin, ME, Blangero, J, Brunner, HG, Buckner, RL, Cichon, S, Coppola, G, de Zubicaray, GI, Deary, IJ, Donohoe, G, de Geus, EJ, Espeseth, T, Fernández, G, Glahn, DC, Grabe, HJ, Hardy, J, Hulshoff Pol, HE, Jenkinson, M, Kahn, RS, McDonald, C, McIntosh, AM, McMahon, FJ, McMahon, KL, Meyer-Lindenberg, A, Morris, DW, Müller-Myhsok, B, Nichols, TE, Ophoff, RA, Paus, T, Pausova, Z, Penninx, BW, Potkin, SG, Sämann, PG, Saykin, AJ, Schumann, G, Smoller, JW, Wardlaw, JM, Weale, ME, Martin, NG, Franke, B, Wright, MJ, Thompson, PM; Enhancing Neuro Imaging Genetics through Meta-Analysis Consortium (2012). Identification of common variants associated with human hippocampal and intracranial volumes. Nature Genetics 44, 552–561.Google Scholar
Thaker, GK (2008). Neurophysiological endophenotypes across bipolar and schizophrenia psychosis. Schizophrenia Bulletin 34, 760–773.Google Scholar
Ward, BD (2000). Simultaneous inference for fMRI data. Biophysics Research Institute, Medical College of Wisconsin. (http://afni.nimh.nih.gov/pub/dist/doc/manual/AlphaSim.pdf).Google Scholar
Waters, F, Allen, P, Aleman, A, Fernyhough, C, Woodward, TS, Badcock, JC, Barkus, E, Johns, L, Varese, F, Menon, M, Vercammen, A, Larøi, F (2012). Auditory hallucinations in schizophrenia and nonschizophrenia populations: a review and integrated model of cognitive mechanisms. Schizophrenia Bulletin 38, 683–793.Google Scholar
White, T, Andreasen, NC, Nopoulos, P, Magnotta, V (2003). Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biological Psychiatry 54, 418–426.Google Scholar
White, T, Hilgetag, CC (2011). Gyrification and neural connectivity in schizophrenia. Development and Psychopathology 23, 339–352.Google Scholar
Winkler, AM, Kochunov, P, Blangero, J, Almasy, L, Zilles, K, Fox, PT, Duggirala, R, Glahn, DC (2010). Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. NeuroImage 53, 1135–1146.Google Scholar
Yamaguchi, Y (2000). Lecticans: organizers of the brain extracellular matrix. Cellular and Molecular Life Sciences 57, 276–289.Google Scholar
Yeap, S, Kelly, SP, Reilly, RB, Thakore, JH, Foxe, JJ (2009). Visual sensory processing deficits in patients with bipolar disorder revealed through high-density electrical mapping. Journal of Psychiatry and Neuroscience 34, 459–464.Google Scholar
Zilles, K, Palomero-Gallagher, N, Amunts, K (2013). Development of cortical folding during evolution and ontogeny. Trends in Neuroscience 36, 275–284.Google Scholar