Skip to main content Accessibility help
×
Home

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

  • C. C. Schultz (a1), T. W. Mühleisen (a2) (a3) (a4), I. Nenadic (a1), K. Koch (a1) (a5), G. Wagner (a1), C. Schachtzabel (a1), F. Siedek (a2) (a3), M. M. Nöthen (a2) (a3) (a6), M. Rietschel (a7), T. Deufel (a8), M. Kiehntopf (a8), S. Cichon (a2) (a3) (a4) (a9), J. R. Reichenbach (a10), H. Sauer (a1) and R. G. M. Schlösser (a1)...

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.

Copyright

Corresponding author

* Address for correspondence: C. C. Schultz, M.D., Department of Psychiatry and Psychotherapy, Jena University Hospital, Philosophenweg 3, 07740 Jena, Germany. (Email: christoph.schultz@med.uni-jena.de)

References

Hide All
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, 11321141.
Annett, M (1967). The binomial distribution of right, mixed and left handedness. Quarterly Journal of Experimental Psychology 19, 327333.
Armstrong, E, Schleicher, A, Omran, H, Curtis, M, Zilles, K (1991). The ontogeny of human gyrification. Cerebral Cortex 5, 5663.
Butler, PD, Javitt, DC (2005). Early-stage visual processing deficits in schizophrenia. Current Opinion in Psychiatry 18, 151157.
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, 372381.
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179194.
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, 434442.
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, 803811.
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.
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.
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195207.
Forbes, NF, Carrick, LA, McIntosh, AM, Lawrie, SM (2009). Working memory in schizophrenia: a meta-analysis. Psychological Medicine 39, 889905.
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, 478489.
Frischknecht, R, Seidenbecher, CI (2008). The crosstalk of hyaluronan-based extracellular matrix and synapses. Neuron Glia Biology 4, 249257.
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, 4654.
Goldman-Rakic, PS (1980). Morphological consequences of prenatal injury to the primate brain. Progress in Brain Research 53, 119.
Green, MF, Nuechterlein, KH, Mintz, J (1994). Backward masking in schizophrenia and mania. II. Specifying the visual channels. Archives of General Psychiatry 51, 945951.
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, 603609.
Hilgetag, CC, Barbas, H (2006). Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Computational Biology 2, e22.
Hill, SK, Harris, MSH, Herbener, ES, Pavuluri, M, Sweeney, JA (2008). Neurocognitive allied phenotypes for schizophrenia and bipolar disorder. Schizophrenia Bulletin 34, 743759.
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, 22332245.
Hugdahl, K (2009). ‘Hearing voices’: auditory hallucinations as failure of top-down control of bottom-up perceptual processes. Scandinavian Journal of Psychology 50, 553560.
Javitt, DC (2009). When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. Annual Review of Clinical Psychology 5, 249275.
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, 494509.
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, 483489.
Karetko, M, Skangiel-Kramska, J (2009). Diverse functions of perineuronal nets. Acta Neurobiologiae Experimentalis 69, 564577.
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261276.
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, 1498014986.
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.
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, 12241230.
Mangin, JF, Jouvent, E, Cachia, A (2010). In-vivo measurement of cortical morphology: means and meanings. Current Opinion in Neurology 23, 359367.
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, 192198.
Miller, EK (2000). The prefrontal cortex and cognitive control. Nature Reviews Neuroscience 1, 5965.
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, 811822.
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, 982990.
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, 6973.
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, 859867.
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.
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.
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, 1628.
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, 9098.
Nöthen, MM, Nieratschker, V, Cichon, S, Rietschel, M (2010). New findings in the genetics of major psychoses. Dialogues in Clinical Neuroscience 12, 8593.
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, 974979.
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, 27282735.
Prange, CK, Pennacchio, LA, Lieuallen, K, Fan, W, Lennon, GG (1998). Characterization of the human neurocan gene, CSPG3. Gene 221, 199205.
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.
Rauch, U, Feng, K, Zhou, XH (2001). Neurocan: a brain chondroitin sulfate proteoglycan. Cellular and Molecular Life Sciences 58, 18421856.
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, 10221029.
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, 906917.
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, 11031108.
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, 137144.
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, 134140.
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, 204209.
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, 17471753.
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, 5158.
Silbersweig, D, Stern, E (1996). Functional neuroimaging of hallucinations in schizophrenia: toward an integration of bottom-up and top-down approaches. Molecular Psychiatry 1, 367375.
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, 552561.
Thaker, GK (2008). Neurophysiological endophenotypes across bipolar and schizophrenia psychosis. Schizophrenia Bulletin 34, 760773.
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).
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, 683793.
White, T, Andreasen, NC, Nopoulos, P, Magnotta, V (2003). Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biological Psychiatry 54, 418426.
White, T, Hilgetag, CC (2011). Gyrification and neural connectivity in schizophrenia. Development and Psychopathology 23, 339352.
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, 11351146.
Yamaguchi, Y (2000). Lecticans: organizers of the brain extracellular matrix. Cellular and Molecular Life Sciences 57, 276289.
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, 459464.
Zilles, K, Palomero-Gallagher, N, Amunts, K (2013). Development of cortical folding during evolution and ontogeny. Trends in Neuroscience 36, 275284.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed