Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T13:53:40.109Z Has data issue: false hasContentIssue false
  • English
  • Français

Shared white-matter dysconnectivity in schizophrenia and bipolar disorder with psychosis

Published online by Cambridge University Press:  04 August 2014

J. Kumar ,
S. Iwabuchi ,
S. Oowise ,
V. Balain ,
L. Palaniyappan  and
P. F. Liddle
J. Kumar
Affiliation:
Translational Neuroimaging, Division of Psychiatry, Institute of Mental Health, University of Nottingham, Nottingham, UK
S. Iwabuchi
Affiliation:
Translational Neuroimaging, Division of Psychiatry, Institute of Mental Health, University of Nottingham, Nottingham, UK
S. Oowise
Affiliation:
The Forensic Hospital, Justice and Forensic Mental Health Network, Sydney, Australia
V. Balain
Affiliation:
Nottinghamshire Healthcare NHS Trust, Nottingham, UK
L. Palaniyappan*
Affiliation:
Translational Neuroimaging, Division of Psychiatry, Institute of Mental Health, University of Nottingham, Nottingham, UK Nottinghamshire Healthcare NHS Trust, Nottingham, UK
P. F. Liddle
Affiliation:
Translational Neuroimaging, Division of Psychiatry, Institute of Mental Health, University of Nottingham, Nottingham, UK
*
*Address for correspondence: Dr L. Palaniyappan, Room-09, C Floor, Institute of Mental Health Building, Triumph Road, Nottingham NG7 2TU, England, UK. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

There is an appreciable overlap in the clinical presentation, epidemiology and treatment response of the two major psychotic disorders – schizophrenia and bipolar disorder. Nevertheless, the shared neurobiological correlates of these two disorders are still elusive. Using diffusion tensor imaging (DTI), we sought to identify brain regions which share altered white-matter connectivity across a clinical spectrum of psychotic disorders.

Method

A sample of 41 healthy controls, 62 patients in a clinically stable state of an established psychotic disorder (40 with schizophrenia, 22 with bipolar disorder) were studied using DTI. Tract-based spatial statistics (TBSS) was used in order to study group differences between patients with psychosis and healthy controls using fractional anisotropy (FA). Probabilistic tractography was used in order to visualize the clusters that showed significant differences between these two groups.

Results

The TBSS analysis revealed five clusters (callosal, posterior thalamic/optic, paralimbic, fronto-occipital) with reduced FA in psychosis. This reduction in FA was associated with an increase in radial diffusivity and a decrease in mode of anisotropy. Factor analysis revealed a single white-matter integrity factor that predicted social and occupational functioning scores in patients irrespective of the diagnostic categorization.

Conclusions

Our results show that a shared white-matter dysconnectivity links the two major psychotic disorders. These microstructural abnormalities predict functional outcome better than symptom-based diagnostic boundaries during a clinically stable phase of illness, highlighting the importance of seeking shared neurobiological factors that underlie the clinical spectrum of psychosis.

Keywords

Bipolar disorderdiffusion tensor imagingdysconnectivityKraepelinpsychosisschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 4 , March 2015 , pp. 759 - 770
Copyright
Copyright © Cambridge University Press 2014 

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

Alexander, AL, Lee, JE, Lazar, M, Field, AS (2007). Diffusion tensor imaging of the brain. Neurotherapeutics 4, 316–329.Google Scholar
Ammons, RB, Ammons, CH (1962). The Quick Test (QT): provisional manual. Psychological Reports 11, 111–161.Google Scholar
Andersson, JLR, Jenkinson, M, Smith, S (2007 a). Non-linear optimisation. FMRIB technical report TR07JA1 (www.fmrib.ox.ac.uk/analysis/techrep). Accessed 10 April 2013.Google Scholar
Andersson, JLR, Jenkinson, M, Smith, S (2007 b). Non-linear registration, aka Spatial normalization. FMRIB technical report TR07JA2 (www.fmrib.ox.ac.uk/analysis/techrep). Accessed 10 April 2013.Google Scholar
Annett, M (1970). A classification of hand preference by association analysis. British Journal of Psychology 61, 303–321.Google Scholar
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association: Washington, DC, Axis V, pp. 760–761.Google Scholar
Argyelan, M, Ikuta, T, DeRosse, P, Braga, RJ, Burdick, KE, John, M, Kingsley, PB, Malhotra, AK, Szeszko, PR (2014). Resting-state FMRI connectivity impairment in schizophrenia and bipolar disorder. Schizophrenia Bulletin 40, 100–110.10.1093/schbul/sbt092Google Scholar
Aylward, E, Walker, E, Bettes, B (1984). Intelligence in schizophrenia: meta-analysis of the research. Schizophrenia Bulletin 10, 430–459.Google Scholar
Behrens, TE, Berg, HJ, Jbabdi, S, Rushworth, MF, Woolrich, MW (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34, 144–155.10.1016/j.neuroimage.2006.09.018Google Scholar
Behrens, TEJ, Woolrich, MW, Jenkinson, M, Johansen-Berg, H, Nunes, RG, Clare, S, Matthews, PM, Brady, JM, Smith, SM (2003). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine 50, 1077–1088.Google Scholar
Benedetti, F, Absinta, M, Rocca, MA, Radaelli, D, Poletti, S, Bernasconi, A, Dallaspezia, S, Pagani, E, Falini, A, Copetti, M, Colombo, C, Comi, G, Smeraldi, E, Filippi, M (2011 a). Tract-specific white matter structural disruption in patients with bipolar disorder. Bipolar Disorders 13, 414–424.10.1111/j.1399-5618.2011.00938.xGoogle Scholar
Benedetti, F, Yeh, P, Bellani, M, Radaelli, D, Nicoletti, MA, Poletti, S, Falini, A, Dallaspezia, S, Colombo, C, Giuseppe, S, Smeraldi, E, Soares, JC, Brambilla, P (2011 b). Disruption of white matter integrity in bipolar depression as a possible structural marker of illness. Biological Psychiatry 69, 309–317.10.1016/j.biopsych.2010.07.028Google Scholar
Berrettini, WH (2011). Are schizophrenic and bipolar disorders related? A review of family and molecular studies. Biological Psychiatry 48, 531–538.Google Scholar
Brambilla, P, Bellani, M, Yeh, PH, Soares, JC (2009). Myelination in bipolar patients and the effects of mood stabilizers on brain anatomy. Current Pharmaceutical Design 15, 2632–2636.10.2174/138161209788957519Google Scholar
Brandt, CL, Eichele, T, Melle, I, Sundet, K, Server, A, Agartz, I, Hugdahl, K, Jensen, J, Andreassen, OA (2014). Working memory networks and activation patterns in schizophrenia and bipolar disorder: comparison with healthy controls. British Journal of Psychiatry 204, 290–298.Google Scholar
Chan, WY, Yang, GL, Chia, MY, Lau, IY, Sitoh, YY, Nowinski, WL, Sim, K (2010 a). White matter abnormalities in first-episode schizophrenia: a combined structural MRI and DTI study. Schizophrenia Research 119, 52–60.Google Scholar
Chan, WY, Yang, GL, Chia, MY, Woon, PS, Lee, J, Keefe, R, Sitoh, YY, Nowinski, WL, Sim, K (2010 b). Cortical and subcortical white matter abnormalities in adults with remitted first-episode mania revealed by Tract-Based Spatial Statistics. Bipolar Disorders 12, 383–389.10.1111/j.1399-5618.2010.00829.xGoogle Scholar
Costafreda, SG, Fu, CH, Picchioni, M, Kane, F, McDonald, C, Prata, DP, Kalidindi, S, Walshe, M, Curtis, V, Bramon, E, Kravariti, E, Marshall, N, Toulopoulou, T, Barker, GJ, Davis, AS, Brammer, MJ, Murray, RM, McGuire, PK (2009). Increased inferior frontal activation during word generation: a marker of genetic risk for schizophrenia but not bipolar disorder? Human Brain Mapping 30, 3287–3298.10.1002/hbm.20749Google Scholar
Craddock, N, O'Donovan, MC, Owen, MJ (2005). The genetics of schizophrenia and bipolar disorder: dissecting psychosis. Journal of Medical Genetics 42, 193–204.Google Scholar
Cui, L, Chen, Z, Deng, W, Huang, X, Li, M, Ma, X, Huang, C, Jiang, L, Wang, Y, Wang, Q, Collier, DA, Gong, Q, Li, T (2011). Assessment of white matter abnormalities in paranoid schizophrenia and bipolar mania patients. Psychiatry Research: Neuroimaging 194, 347–353.Google Scholar
Curtis, VA, Dixon, TA, Morris, RG, Bullmore, ET, Brammer, MJ, Williams, SC, Sharma, T, Murray, RM, McGuire, PK (2001). Differential frontal activation in schizophrenia and bipolar illness during verbal fluency. Journal of Affective Disorders 66, 111–121.10.1016/S0165-0327(00)00240-8Google Scholar
Douaud, G, Jbabdi, S, Behrens, TE, Menke, RA, Gass, A, Monsch, AU, Rao, A, Whitcher, B, Kindlmann, G, Matthews, PM, Smith, S (2011). DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. Neuroimage 55, 880–890.Google Scholar
Ennis, DB, Kindmann, G (2006). Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images. Magnetic Resonance in Medicine 55, 136–146.Google Scholar
Farah, MJ, Shera, DM, Savage, JH, Betancourt, L, Giannetta, JM, Brodsky, NL, Malmud, EK, Hurt, H (2006). Childhood poverty: specific associations with neurocognitive development. Brain Research 1110, 166–174.10.1016/j.brainres.2006.06.072Google Scholar
Hafeman, DM, Chang, KD, Garrett, AS, Sanders, EM, Phillips, ML (2012). Effects of medication on neuroimaging findings in bipolar disorder: an updated review. Bipolar Disorders 14, 375–410.Google Scholar
Hall, J, Whalley, HC, Marwick, K, McKirdy, J, Sussmann, J, Romaniuk, L, Johnstone, EC, Wan, HI, McIntosh, AM, Lawrie, SM (2010). Hippocampal function in schizophrenia and bipolar disorder. Psychological Medicine 40, 761–770.Google Scholar
Heckers, S (2008). Making progress in schizophrenia research. Schizophrenia Bulletin 34, 591–594.10.1093/schbul/sbn046Google Scholar
Heng, S, Song, AW, Sim, K (2010). White matter abnormalities in bipolar disorder: insights from diffusion tensor imaging studies. Journal of Neural Transmission 117, 639–654.Google Scholar
Hill, SK, Reilly, JL, Margret, SH, Harris, MS, Rosen, C, Marvin, RW, DeLeon, O, Sweeney, JA (2009). A comparison of neuropsychological dysfunction in first-episode psychosis patients with unipolar depression, bipolar disorder and schizophrenia. Schizophrenia Research 113, 167–175.Google Scholar
Johnstone, EC, Frith, CD, Crow, TJ, Owens, DG, Done, DJ, Baldwin, EJ, Charlette, A (1992). The Northwick Park ‘Functional’ Psychosis Study: diagnosis and outcome. Psychological Medicine 22, 331–346.Google Scholar
Jolapara, M, Kesavadas, C, Radhakrishnan, VV, Saini, J, Patro, SN, Gupta, AK, Kapilamoorthy, TR, Bodhey, N (2009). Diffusion tensor mode in imaging of intracranial epidermoid cysts: one step ahead of fractional anisotropy. Neuroradiology 51, 123–129.Google Scholar
Kaur, M, Battisti, RA, Lagopoulos, J, Ward, PB, Hickie, IB, Franz, CP, Hermens, DF (2012). Neurophysiological biomarkers support bipolar-spectrum disorders within psychosis cluster. Journal of Psychiatry & Neuroscience 37, 313–321.Google Scholar
Keshavan, MS, Morris, DW, Sweeney, JA, Pearlson, G, Thaker, G, Seidman, LJ, Eack, SM, Tamminga, C (2011). A dimensional approach to the psychosis spectrum between bipolar disorder and schizophrenia: the Schizo-Bipolar Scale. Schizophrenia Research 133, 250–254.10.1016/j.schres.2011.09.005Google Scholar
Kraepelin, E (1919). Dementia Praecox and Paraphrenia (trans.), 8th edn. Livingstone: Edinburgh, UK.Google Scholar
Kunimatsu, N, Aoki, S, Kunimatsu, A, Abe, O, Yamada, H, Masutani, Y, Kasai, K, Yamasue, H, Ohtomo, K (2012). Tract-specific analysis of white matter integrity disruption in schizophrenia. Psychiatry Research: Neuroimaging 201, 136–143.10.1016/j.pscychresns.2011.07.010Google Scholar
Leckman, JF, Sholomskas, D, Thompson, WD, Belanger, A, Weissman, MM (1982). Best estimate of lifetime psychiatric diagnosis: a methodological study. Archives of General Psychiatry 39, 879–883.10.1001/archpsyc.1982.04290080001001Google Scholar
Levitt, JL, Alvarado, JL, Nestor, PG, Rosow, L, Pelavin, PE, McCarley, RW, Kubicki, M, Shenton, ME (2012). Fractional anisotropy and radial diffusivity: diffusion measures of white matter abnormalities in the anterior limb of the internal capsule in schizophrenia. Schizophrenia Research 136, 55–62.Google Scholar
Liddle, EB, Bates, AT, Das, D, White, TP, Groom, MJ, Jansen, M, Jackson, GM, Hollis, C, Liddle, PF (2012). Inefficient cerebral recruitment as a vulnerability marker for schizophrenia. Psychological Medicine 14, 1–14.Google Scholar
Liddle, PF, Ngan, ETC, Duffield, G, Kho, K, Warren, AJ (2002). Signs and Symptoms of Psychotic Illness (SSPI): a rating scale. British Journal of Psychiatry 180, 45–50.Google Scholar
Lu, LH, Zhou, XJ, Keedy, SK, Reilly, JL, Sweeney, JA (2011). White matter microstructure in untreated first episode bipolar disorder with psychosis: comparison with schizophrenia. Bipolar Disorders 13, 604–613.10.1111/j.1399-5618.2011.00958.xGoogle Scholar
Mandl, RCW, Rais, M, van Baal, GCM, van Haren, NEM, Cahn, W, Kahn, RS, Hulshoff Pol, HE (2013). Altered white matter connectivity in never-medicated patients with schizophrenia. Human Brain Mapping 34, 2353–2365.Google Scholar
McIntosh, AM, Maniega, SM, Lymer, GKS, McKirdy, J, Hall, J, Sussmann, JED, Bastin, ME, Clayden, JD, Johnstone, EC, Lawrie, SM (2008). White matter tractography in bipolar disorder and schizophrenia. Biological Psychiatry 64, 1088–1092.Google Scholar
Mori, S, Wakana, S, Nagae-Petscher, LM, van Zijl, PCM (2005). MRI Atlas of Human White Matter. Elsevier: Amsterdam, 284 pp.Google Scholar
Murray, RM, Sham, P, van OS, J, Zanelli, J, Cannon, M, McDonald, C (2004). A developmental model for similarities and dissimilarities between schizophrenia and bipolar disorder. Schizophrenia Research 71, 405–416.10.1016/j.schres.2004.03.002Google Scholar
Noble, KG, Norman, MF, Farah, MJ (2005). Neurocognitive correlates of socioeconomic status in kindergarten children. Developmental Science 8, 74–87.10.1111/j.1467-7687.2005.00394.xGoogle Scholar
Palaniyappan, L, Liddle, PF (2014). Diagnostic discontinuity in psychosis: a combined study of cortical gyrification and functional connectivity. Schizophrenia Bulletin 40, 675–684.10.1093/schbul/sbt050Google Scholar
Parrott, B, Lewine, R (2005). Socioeconomic status of origin and the clinical expression of schizophrenia. Schizophrenia Research 75, 417–424.Google Scholar
Rose, D, Pevalin, DJ (2003). A Researcher's Guide to the National Statistics Socio-economic Classification. Sage Publications: London.10.4135/9780857024725Google Scholar
Seal, ML, Yucel, M, Fornito, A, Wood, SJ, Harrison, BJ, Walterfang, M, Pell, GS, Pantelis, C (2008). Abnormal white matter microstructure in schizophrenia: a voxelwise analysis of axial and radial diffusivity. Schizophrenia Research 101, 106–110.Google Scholar
Sidak, Z (1967). Rectangular confidence regions for the means of multivariate normal distributions. Journal of the American Statistical Association 62, 626–633.Google Scholar
Smith, SM (2002). Fast robust automated brain extraction. Human Brain Mapping 17, 143–155.Google Scholar
Smith, SM, Jenkinson, M, Johansen-Berg, H, Rueckert, D, Nichols, TE, Mackay, CE, Watkins, KE, Ciccarelli, O, Cader, MZ, Matthews, PM, Behrens, TEJ (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487–1505.Google Scholar
Sussmann, JE, Lymer, GKS, McKirdy, J, Moorhead, TWJ, Munoz, MS, Job, D, Bastin, ME, Johnstone, EC, Lawrie, SM, McIntosh, AM (2009). White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disorders 11, 11–18.Google Scholar
Whalley, HC, McKirdy, J, Romaniu, L, Sussmann, J, Johnstone, EC, Wan, HI, McIntosh, AM, Lawrie, SM, Hall, J (2009). Functional imaging of emotional memory in bipolar disorder and schizophrenia. Bipolar Disorders 11, 840–856.Google Scholar
WHO Collaborating Centre for Drug Statistics and Methodology (2003). Guidelines for ATC Classification and DDD Assignment. WHO Collaborating Centre for Drug Statistics and Methodology: Oslo, Norway.Google Scholar
Woodberry, KA, Giuliano, AJ, Seidman, LJ (2008). Premorbid IQ in schizophrenia: a meta-analytic review. American Journal of Psychiatry 165, 579–587.10.1176/appi.ajp.2008.07081242Google Scholar
Zalesky, A (2011). Moderating registration misalignment in voxelwise comparisons of DTI data: a performance evaluation of skeleton projection. Magnetic Resonance Imaging 29, 111–125.Google Scholar