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Genetic and environmental influences on cortical surface area and cortical thickness in bipolar disorder

Published online by Cambridge University Press:  28 May 2014

F. Bootsman ,
R. M. Brouwer ,
H. G. Schnack ,
G. C. M. van Baal ,
A. C. van der Schot ,
R. Vonk ,
H. E. Hulshoff Pol ,
W. A. Nolen ,
R. S. Kahn  and
N. E. M. van Haren
F. Bootsman*
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
R. M. Brouwer
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
H. G. Schnack
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
G. C. M. van Baal
Affiliation:
Julius Center, University Medical Center Utrecht, Utrecht, The Netherlands
A. C. van der Schot
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
R. Vonk
Affiliation:
Reinier van Arkel Group, 's-Hertogenbosch, The Netherlands
H. E. Hulshoff Pol
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
W. A. Nolen
Affiliation:
Department of Psychiatry, University Medical Center Groningen, Groningen, The Netherlands
R. S. Kahn
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
N. E. M. van Haren
Affiliation:
Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
*
*Address for correspondence: Dr F. Bootsman, University Medical Center Utrecht, Brain Center Rudolf Magnus, Internal address: A.01.126, PO Box: 85500, 3508 GA Utrecht, The Netherlands. (Email: f.bootsman@umcutrecht.nl)
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Abstract

Background

The risk of developing bipolar disorder (BD) has been linked to structural brain abnormalities. The degree to which genes and environment influence the association of BD with cortical surface area remains to be elucidated. In this twin study, genetic and environmental contributions to the association between liability to develop BD and surface area, thickness and volume of the cortex were examined.

Method

The study cohort included 44 affected monozygotic (nine concordant, 12 discordant) and dizygotic (four concordant, 19 discordant) twin pairs, and seven twins from incomplete discordant monozygotic and dizygotic discordant twin pairs. In addition, 37 monozygotic and 24 dizygotic healthy control twin pairs, and six twins from incomplete monozygotic and dizygotic control pairs were included.

Results

Genetic liability to develop BD was associated with a larger cortical surface in limbic and parietal regions, and a thicker cortex in central and parietal regions. Environmental factors related to BD were associated with larger medial frontal, parietal and limbic, and smaller orbitofrontal surfaces. Furthermore, thinner frontal, limbic and occipital cortex, and larger frontal and parietal, and smaller orbitofrontal volumes were also associated with environmental factors related to BD.

Conclusions

Our results suggest that unique environmental factors play a prominent role in driving the associations between liability to develop BD and cortical measures, particularly those involving cortical thickness. Further evaluation of their influence on the surface and thickness of the cortical mantle is recommended. In addition, cortical volume appeared to be primarily dependent on surface and not thickness.

Keywords

Bipolar disordercortical surface areacortical thicknessheritabilitymagnetic resonance imagingtwin studiesunique environmental factors
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 1 , January 2015 , pp. 193 - 204
Copyright
Copyright © Cambridge University Press 2014 

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References

Adler, CM, Delbello, MP, Jarvis, K, Levine, A, Adams, J, Strakowski, SM (2007). Voxel-based study of structural changes in first-episode patients with bipolar disorder. Biological Psychiatry 61, 776–781.CrossRefGoogle ScholarPubMed
Aldhafeeri, FM, Mackenzie, I, Kay, T, Alghamdi, J, Sluming, V (2012). Regional brain responses to pleasant and unpleasant IAPS pictures: different networks. Neuroscience Letters 512, 94–98.Google Scholar
Baare, WF, Hulshoff Pol, HE, Boomsma, DI, Posthuma, D, de Geus, EJ, Schnack, HG, van Haren, NE, van Oel, CJ, Kahn, RS (2001). Quantitative genetic modeling of variation in human brain morphology. Cerebral Cortex 11, 816–824.Google Scholar
Bearden, CE, Thompson, PM, Dalwani, M, Hayashi, KM, Lee, AD, Nicoletti, M, Trakhtenbroit, M, Glahn, DC, Brambilla, P, Sassi, RB, Mallinger, AG, Frank, E, Kupfer, DJ, Soares, JC (2007). Greater cortical gray matter density in lithium-treated patients with bipolar disorder. Biological Psychiatry 62, 7–16.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.Google Scholar
Bender, RE, Alloy, LB, Sylvia, LG, Urosevic, S, Abramson, LY (2010). Generation of life events in bipolar spectrum disorders: a re-examination and extension of the stress generation theory. Journal of Clinical Psychology 66, 907–926.CrossRefGoogle ScholarPubMed
Boomsma, D, Busjahn, A, Peltonen, L (2002). Classical twin studies and beyond. Nature Reviews Genetic 3, 872–882.Google Scholar
Delvecchio, G, Sugranyes, G, Frangou, S (2013). Evidence of diagnostic specificity in the neural correlates of facial affect processing in bipolar disorder and schizophrenia: a meta-analysis of functional imaging studies. Psychological Medicine 43, 553–569.Google Scholar
Emsell, L, McDonald, C (2009). The structural neuroimaging of bipolar disorder. International Review of Psychiatry 21, 297–313.Google Scholar
Eyler, LT, Prom-Wormley, E, Panizzon, MS, Kaup, AR, Fennema-Notestine, C, Neale, MC, Jernigan, TL, Fischl, B, Franz, CE, Lyons, MJ, Grant, M, Stevens, A, Pacheco, J, Perry, ME, Schmitt, JE, Seidman, LJ, Thermenos, HW, Tsuang, MT, Chen, CH, Thompson, WK, Jak, A, Dale, AM, Kremen, WS (2011). Genetic and environmental contributions to regional cortical surface area in humans: a magnetic resonance imaging twin study. Cerebral Cortex 21, 2313–2321.Google Scholar
First, M, Spitzer, R, Gibbon, M, Williams, J (1997). User's Guide for the Structured Clinical Interview for DSM-IV Axis I Disorders – Clinical Version (SCID-CV). American Psychiatric Press: Washington, DC.Google Scholar
Foland-Ross, LC, Thompson, PM, Sugar, CA, Madsen, SK, Shen, JK, Penfold, C, Ahlf, K, Rasser, PE, Fischer, J, Yang, Y, Townsend, J, Bookheimer, SY, Altshuler, LL (2011). Investigation of cortical thickness abnormalities in lithium-free adults with bipolar I disorder using cortical pattern matching. American Journal of Psychiatry 168, 530–539.Google Scholar
Fornito, A, Yucel, 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
Fornito, A, Yucel, M, Wood, SJ, Bechdolf, A, Carter, S, Adamson, C, Velakoulis, D, Saling, MM, McGorry, PD, Pantelis, C (2009). Anterior cingulate cortex abnormalities associated with a first psychotic episode in bipolar disorder. British Journal of Psychiatry 194, 426–433.Google Scholar
Hajek, T, Kopecek, M, Hoschl, C, Alda, M (2012). Smaller hippocampal volumes in patients with bipolar disorder are masked by exposure to lithium: a meta-analysis. Journal of Psychiatry and Neuroscience 37, 333–343.Google Scholar
Hammen, C (1991). Generation of stress in the course of unipolar depression. Journal of Abnormal Psychology 100, 555–561.Google Scholar
Hogstrom, LJ, Westlye, LT, Walhovd, KB, Fjell, AM (2013). The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness and gyrification. Cerebral Cortex 23, 2521–2530.Google Scholar
Hulshoff Pol, HE, van Baal, GC, Schnack, HG, Brans, RG, van der Schot, AC, Brouwer, RM, van Haren, NE, Lepage, C, Collins, DL, Evans, AC, Boomsma, DI, Nolen, W, Kahn, RS (2012). Overlapping and segregating structural brain abnormalities in twins with schizophrenia or bipolar disorder. Archives of General Psychiatry 69, 349–359.Google Scholar
Im, K, Lee, JM, Lyttelton, O, Kim, SH, Evans, AC, Kim, SI (2008). Brain size and cortical structure in the adult human brain. Cerebral Cortex 18, 2181–2191.Google Scholar
Jansen, A, Andermann, E (2005). Genetics of the polymicrogyria syndromes. Journal of Medical Genetics 42, 369–378.Google Scholar
Kabani, N, Le, GG, MacDonald, D, Evans, AC (2001). Measurement of cortical thickness using an automated 3-D algorithm: a validation study. NeuroImage 13, 375–380.CrossRefGoogle ScholarPubMed
Kenny, S, Andric, M, Boker, SM, Neale, MC, Wilde, M, Small, SL (2009). Parallel workflows for data-driven structural equation modeling in functional neuroimaging. Frontiers in Neuroinformatics 3, 34.Google Scholar
Kieseppa, T, van Erp, TG, Haukka, J, Partonen, T, Cannon, TD, Poutanen, VP, Kaprio, J, Lonnqvist, J (2003). Reduced left hemispheric white matter volume in twins with bipolar I disorder. Biological Psychiatry 54, 896–905.Google Scholar
Kim, JS, Singh, V, Lee, JK, Lerch, J, Ad-Dab'bagh, Y, MacDonald, D, Lee, JM, Kim, SI, Evans, AC (2005). Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. NeuroImage 27, 210–221.CrossRefGoogle ScholarPubMed
Kochunov, P, Mangin, JF, Coyle, T, Lancaster, J, Thompson, P, Rivière, D, Cointepas, Y, Regis, J, Schlosser, A, Royall, DR, Zilles, K, Mazziotta, J, Toga, A, Fox, PT (2005). Age-related morphology trends of cortical sulci. Human Brain Mapping 26, 210–220.Google Scholar
Lyoo, IK, Sung, YH, Dager, SR, Friedman, SD, Lee, JY, Kim, SJ, Kim, N, Dunner, DL, Renshaw, PF (2006). Regional cerebral cortical thinning in bipolar disorder. Bipolar Disorders 8, 65–74.Google Scholar
Lyttelton, O, Boucher, M, Robbins, S, Evans, A (2007). An unbiased iterative group registration template for cortical surface analysis. NeuroImage 34, 1535–1544.Google Scholar
MacDonald, D, Kabani, N, Avis, D, Evans, AC (2000). Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. NeuroImage 12, 340–356.Google Scholar
McDonald, C, Bullmore, ET, Sham, PC, Chitnis, X, Wickham, H, Bramon, E, Murray, RM (2004). Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes. Archives of General Psychiatry 61, 974–984.Google Scholar
McGuffin, P, Rijsdijk, F, Andrew, M, Sham, P, Katz, R, Cardno, A (2003). The heritability of bipolar affective disorder and the genetic relationship to unipolar depression. Archives of General Psychiatry 60, 497–502.Google Scholar
Mountcastle, VB (1997). The columnar organization of the neocortex. Brain 120, 701–722.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). Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cerebral Cortex 15, 708–719.Google Scholar
Neale, MC, Miller, MB (1997). The use of likelihood-based confidence intervals in genetic models. Behavior Genetics 27, 113–120.Google Scholar
Noga, JT, Vladar, K, Torrey, EF (2001). A volumetric magnetic resonance imaging study of monozygotic twins discordant for bipolar disorder. Psychiatry Research 106, 25–34.Google Scholar
Nurnberger, JI Jr, Blehar, MC, Kaufmann, CA, York-Cooler, C, Simpson, SG, Harkavy-Friedman, J, Severe, JB, Malaspina, D, Reich, T (1994). Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Archives of General Psychiatry 51, 849–859.CrossRefGoogle ScholarPubMed
Pakkenberg, B, Gundersen, HJ (1997). Neocortical neuron number in humans: effect of sex and age. Journal of Comparative Neurology 384, 312–320.Google Scholar
Panizzon, MS, Fennema-Notestine, C, Eyler, LT, Jernigan, TL, Prom-Wormley, E, 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
Peper, JS, Brouwer, RM, Boomsma, DI, Kahn, RS, Hulshoff Pol, HE (2007). Genetic influences on human brain structure: a review of brain imaging studies in twins. Human Brain Mapping 28, 464–473.Google Scholar
Pfohl, B, Blum, N, Zimmerman, M (1997). Structured Interview for DSM-IV Personality (SIDP-IV). American Psychiatric Press: Washington, DC.Google Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.Google Scholar
Pontious, A, Kowalczyk, T, Englund, C, Hevner, RF (2008). Role of intermediate progenitor cells in cerebral cortex development. Developmental Neuroscience 30, 24–32.Google Scholar
Posthuma, D, Boomsma, DI (2000). A note on the statistical power in extended twin designs. Behavior Genetics 30, 147–158.Google Scholar
Rakic, P (1988). Specification of cerebral cortical areas. Science 241, 170–176.Google Scholar
Rakic, P (1995). A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends in Neurosciences 18, 383–388.Google Scholar
Rakic, P (2009). Evolution of the neocortex: a perspective from developmental biology. Nature Reviews Neuroscience 10, 724–735.Google Scholar
Rakic, P, Ayoub, AE, Breunig, JJ, Dominguez, MH (2009). Decision by division: making cortical maps. Trends in Neurosciences 32, 291–301.Google Scholar
Regeer, EJ, ten Have, M, Rosso, ML, Hakkaart-van, RL, Vollebergh, W, Nolen, WA (2004). Prevalence of bipolar disorder in the general population: a Reappraisal Study of the Netherlands Mental Health Survey and Incidence Study. Acta Psychiatrica Scandinavica 110, 374–382.Google Scholar
Rimol, LM, Hartberg, CB, Nesvag, R, Fennema-Notestine, C, Hagler, DJ Jr, Pung, CJ, Jennings, RG, Haukvik, UK, Lange, E, Nakstad, PH, Melle, I, Andreassen, OA, Dale, AM, Agartz, I (2010). Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry 68, 41–50.Google Scholar
Rimol, LM, Nesvag, R, Hagler, DJ Jr, Bergmann, O, 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.CrossRefGoogle ScholarPubMed
Safford, SM, Alloy, LB, Abramson, LY, Crossfield, AG (2007). Negative cognitive style as a predictor of negative life events in depression-prone individuals: a test of the stress generation hypothesis. Journal of Affective Disorders 99, 147–154.Google Scholar
Samamé, C, Martino, DJ, Strejilevich, SA (2012). Social cognition in euthymic bipolar disorder: systematic review and meta-analytic approach. Acta Psychiatrica Scandinavica 125, 266–280.Google Scholar
Savitz, J, Drevets, WC (2009). Bipolar and major depressive disorder: neuroimaging the developmental–degenerative divide. Neuroscience and Biobehavioral Reviews 33, 699–771.Google Scholar
Seldon, HL (2005). Does brain white matter growth expand the cortex like a balloon? Hypothesis and consequences. Laterality 10, 81–95.CrossRefGoogle Scholar
Selvaraj, S, Arnone, D, Job, D, Stanfield, A, Farrow, TF, Nugent, AC, Scherk, H, Gruber, O, Chen, X, Sachdev, PS, Dickstein, DP, Malhi, GS, Ha, TH, Ha, K, Phillips, ML, McIntosh, AM (2012). Grey matter differences in bipolar disorder: a meta-analysis of voxel-based morphometry studies. Bipolar Disorders 14, 135–145.Google Scholar
Thompson, PM, Cannon, TD, Narr, KL, van Eep, T, Poutanen, VP, Huttunen, M, Lonnqvist, J, Standertskjold-Nordenstam, CG, Kaprio, J, Khaledy, M, Dail, R, Zoumalan, CI, Toga, AW (2001). Genetic influences on brain structure. Nature Neuroscience 4, 1253–1258.Google Scholar
Toulopoulou, T, Picchioni, M, Rijsdijk, F, Hua-Hall, M, Ettinger, U, Sham, P, Murray, R (2007). Substantial genetic overlap between neurocognition and schizophrenia: genetic modeling in twin samples. Archives of General Psychiatry 64, 1348–1355.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.Google Scholar
van der Schot, AC, Vonk, R, Brans, RG, van Haren, NE, Koolschijn, PC, Nuboer, V, Schnack, HG, van Baal, GC, Boomsma, DI, Nolen, WA, Hulshoff Pol, HE, Kahn, RS (2009). Influence of genes and environment on brain volumes in twin pairs concordant and discordant for bipolar disorder. Archives of General Psychiatry 66, 142–151.Google Scholar
van der Schot, AC, Vonk, R, Brouwer, RM, van Baal, GC, Brans, RG, van Haren, NE, Schnack, HG, Boomsma, DI, Nolen, WA, Hulshoff Pol, HE, Kahn, RS (2010). Genetic and environmental influences on focal brain density in bipolar disorder. Brain 133, 3080–3092.Google Scholar
Visscher, PM (2004). Power of the classical twin design revisited. Twin Research 7, 505–512.Google Scholar
Wang, AY, Lohmann, KM, Yang, CK, Zimmerman, EI, Pantazopoulos, H, Herring, N, Berretta, S, Heckers, S, Konradi, C (2011). Bipolar disorder type 1 and schizophrenia are accompanied by decreased density of parvalbumin- and somatostatin-positive interneurons in the parahippocampal region. Acta Neuropathologica 122, 615–626.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
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.CrossRefGoogle ScholarPubMed
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