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Anatomical integration and rich-club connectivity in euthymic bipolar disorder

Published online by Cambridge University Press:  13 February 2017

S. O'Donoghue ,
L. Kilmartin ,
D. O'Hora ,
L. Emsell ,
C. Langan ,
S. McInerney ,
N. J. Forde ,
A. Leemans ,
B. Jeurissen  and
G. J. Barker
...Show all authors
S. O'Donoghue*
Affiliation:
The Centre for Neuroimaging & Cognitive Genomics (NICOG) and NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Republic of Ireland
L. Kilmartin
Affiliation:
College of Engineering and Informatics, National University of Ireland Galway, Galway, Republic of Ireland
D. O'Hora
Affiliation:
School of Psychology, National University of Ireland Galway, Galway, Republic of Ireland
L. Emsell
Affiliation:
Translational MRI, Department of Imaging & Pathology, KU Leuven & Radiology, University Hospitals Leuven, Leuven, Belgium
C. Langan
Affiliation:
The Centre for Neuroimaging & Cognitive Genomics (NICOG) and NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Republic of Ireland
S. McInerney
Affiliation:
Department of Psychiatry, St Michael's Hospital, Toronto, Ontario, Canada
N. J. Forde
Affiliation:
Department of Psychiatry, University Medical Centre Groningen, Groningen, The Netherlands
A. Leemans
Affiliation:
Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands
B. Jeurissen
Affiliation:
Vision Lab, University of Antwerp, Antwerp, Belgium
G. J. Barker
Affiliation:
Institute of Psychiatry, Psychology and Neuroscience, London, UK
P. McCarthy
Affiliation:
Radiology, University Hospital Galway, Galway, Republic of Ireland
D. M. Cannon
Affiliation:
The Centre for Neuroimaging & Cognitive Genomics (NICOG) and NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Republic of Ireland
C. McDonald
Affiliation:
The Centre for Neuroimaging & Cognitive Genomics (NICOG) and NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Republic of Ireland
*
*Address for correspondence: S. O'Donoghue, The Centre for Neuroimaging & Cognitive Genomics (NICOG) and NCBES Galway Neuroscience Centre, College of Medicine, Nursing and Health Sciences, National University of Ireland Galway, Galway, Republic of Ireland. (Email: [email protected])
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Abstract

Background

Although repeatedly associated with white matter microstructural alterations, bipolar disorder (BD) has been relatively unexplored using complex network analysis. This method combines structural and diffusion magnetic resonance imaging (MRI) to model the brain as a network and evaluate its topological properties. A group of highly interconnected high-density structures, termed the ‘rich-club’, represents an important network for integration of brain functioning. This study aimed to assess structural and rich-club connectivity properties in BD through graph theory analyses.

Method

We obtained structural and diffusion MRI scans from 42 euthymic patients with BD type I and 43 age- and gender-matched healthy volunteers. Weighted fractional anisotropy connections mapped between cortical and subcortical structures defined the neuroanatomical networks. Next, we examined between-group differences in features of graph properties and sub-networks.

Results

Patients exhibited significantly reduced clustering coefficient and global efficiency, compared with controls globally and regionally in frontal and occipital regions. Additionally, patients displayed weaker sub-network connectivity in distributed regions. Rich-club analysis revealed subtly reduced density in patients, which did not withstand multiple comparison correction. However, hub identification in most participants indicated differentially affected rich-club membership in the BD group, with two hubs absent when compared with controls, namely the superior frontal gyrus and thalamus.

Conclusions

This graph theory analysis presents a thorough investigation of topological features of connectivity in euthymic BD. Abnormalities of global and local measures and network components provide further neuroanatomically specific evidence for distributed dysconnectivity as a trait feature of BD.

Keywords

Bipolar disorderdiffusion tensor imaginggraph theorymagnetic resonance imagingnetwork analysis
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 9 , July 2017 , pp. 1609 - 1623
Copyright
Copyright © Cambridge University Press 2017 

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References

American Psychiatric Association (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. APA: Washington, DC.Google Scholar
Bassett, DS, Brown, JA, Deshpande, V, Carlson, JM, Grafton, ST (2011). Conserved and variable architecture of human white matter connectivity. NeuroImage 54, 1262–1279.CrossRefGoogle ScholarPubMed
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). Tract-specific white matter structural disruption in patients with bipolar disorder. Bipolar Disorders 13, 414–424.CrossRefGoogle ScholarPubMed
Benjamini, Y, Hochberg, Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300.CrossRefGoogle Scholar
Bullmore, E, Sporns, O (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews. Neuroscience 10, 186–198.CrossRefGoogle ScholarPubMed
Bullmore, E, Sporns, O (2012). The economy of brain network organization. Nature Reviews. Neuroscience 13, 336–349.CrossRefGoogle ScholarPubMed
Caeyenberghs, K, Leemans, A (2014). Hemispheric lateralization of topological organization in structural brain networks. Human Brain Mapping 35, 4944–4957.CrossRefGoogle ScholarPubMed
Chang, LC, Jones, DK, Pierpaoli, C (2005). RESTORE: Robust Estimation of Tensors by Outlier Rejection. Magnetic Resonance in Medicine 53, 1088–1095.CrossRefGoogle ScholarPubMed
Collin, G, Kahn, RS, De Reus, MA, Cahn, W, Van Den Heuvel, MP (2014). Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophrenia Bulletin 40, 438–448.CrossRefGoogle ScholarPubMed
Collin, G, Sporns, O, Mandl, RCW, Van Den Heuvel, MP (2013). Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex. Cerebral Cortex 24, 2258–2267.CrossRefGoogle ScholarPubMed
Collin, G, van den Heuvel, MP, Abramovic, L, Vreeker, A, de Reus, MA, van Haren, NEM, Boks, MPM, Ophoff, RA, Kahn, RS (2016). Brain network analysis reveals affected connectome structure in bipolar I disorder. Human Brain Mapping 37, 122–134.CrossRefGoogle ScholarPubMed
Crossley, NA, Mechelli, A, Scott, J, Carletti, F, Fox, PT, McGuire, P, Bullmore, ET (2014). The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137, 2382–2395.CrossRefGoogle ScholarPubMed
Crossley, NA, Mechelli, A, Vértes, PE, Winton-Brown, TT, Patel, AX, Ginestet, CE, McGuire, P, Bullmore, ET, Vertes, PE, Winton-Brown, TT, Patel, AX, Ginestet, CE, McGuire, P, Bullmore, ET (2013). Cognitive relevance of the community structure of the human brain functional coactivation network. Proceedings of the National Academy of Sciences of the United States of America 110, 11583–11588.CrossRefGoogle ScholarPubMed
Daianu, M, Jahanshad, N, Nir, TM, Jack, CR, Weiner, MW, Bernstein, MA, Thompson, PM (2015). Rich club analysis in the Alzheimer's disease connectome reveals a relatively undisturbed structural core network. Human Brain Mapping 36, 3087–3103.CrossRefGoogle ScholarPubMed
de Reus, MA, van den Heuvel, MP (2013). The parcellation-based connectome: limitations and extensions. NeuroImage 80, 397–404.CrossRefGoogle ScholarPubMed
Ellison-Wright, I, Nathan, PJ, Bullmore, ET, Zaman, R, Dudas, RB, Agius, M, Fernandez-Egea, E, Müller, U, Dodds, CM, Forde, NJ, Scanlon, C, Leemans, A, McDonald, C, Cannon, DM (2014). Distribution of tract deficits in schizophrenia. BMC Psychiatry 14, 99.CrossRefGoogle ScholarPubMed
Emsell, L, Langan, C, Van Hecke, W, Barker, GJ, Leemans, A, Sunaert, S, McCarthy, P, Nolan, R, Cannon, DM, McDonald, C (2013 a). White matter differences in euthymic bipolar I disorder: a combined magnetic resonance imaging and diffusion tensor imaging voxel-based study. Bipolar Disorders 15, 365–376.CrossRefGoogle ScholarPubMed
Emsell, L, Leemans, A, Langan, C, Van Hecke, W, Barker, GJ, McCarthy, P, Jeurissen, B, Sijbers, J, Sunaert, S, Cannon, DM, McDonald, C (2013 b). Limbic and callosal white matter changes in euthymic bipolar I disorder: an advanced diffusion magnetic resonance imaging tractography study. Biological Psychiatry 73, 194–201.CrossRefGoogle ScholarPubMed
Emsell, L, McDonald, C (2009). The structural neuroimaging of bipolar disorder. International Review of Psychiatry (Abingdon, England) 21, 297–313.CrossRefGoogle ScholarPubMed
Forde, NJ, O'Donoghue, S, Scanlon, C, Emsell, L, Chaddock, C, Leemans, A, Jeurissen, B, Barker, GJ, Cannon, DM, Murray, RM, McDonald, C (2015). Structural brain network analysis in families multiply affected with bipolar I disorder. Psychiatry Research – Neuroimaging 234, 44–51.CrossRefGoogle ScholarPubMed
Fornito, A, Zalesky, A, Breakspear, M (2013). Graph analysis of the human connectome: promise, progress, and pitfalls. NeuroImage 80, 426–444.CrossRefGoogle ScholarPubMed
Fornito, A, Zalesky, A, Breakspear, M (2015). The connectomics of brain disorders. Nature Reviews. Neuroscience 16, 159–172.CrossRefGoogle ScholarPubMed
Fornito, A, Zalesky, A, Pantelis, C, Bullmore, ET (2012). Schizophrenia, neuroimaging and connectomics. NeuroImage 62, 2296–2314.CrossRefGoogle ScholarPubMed
Gadelkarim, JJ, Ajilore, O, Schonfeld, D, Zhan, L, Thompson, PM, Feusner, JD, Kumar, A, Altshuler, LL, Leow, AD (2014). Investigating brain community structure abnormalities in bipolar disorder using path length associated community estimation. Human Brain Mapping 35, 2253–2264.CrossRefGoogle ScholarPubMed
Griffa, A, Baumann, PS, Thiran, JP, Hagmann, P (2013). Structural connectomics in brain diseases. NeuroImage 80, 515–526.CrossRefGoogle ScholarPubMed
Hallahan, B, Newell, J, Soares, JC, Brambilla, P, Strakowski, SM, Fleck, DE, Kieseppä, T, Altshuler, LL, Fornito, A, Malhi, GS, McIntosh, AM, Yurgelun-Todd, DA, Labar, KS, Sharma, V, MacQueen, GM, Murray, RM, McDonald, C (2011). Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biological Psychiatry 69, 326–335.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Haznedar, MM, Roversi, F, Pallanti, S, Baldini-Rossi, N, Schnur, DB, Licalzi, EM, Tang, C, Hof, PR, Hollander, E, Buchsbaum, MS (2005). Fronto-thalamo-striatal gray and white matter volumes and anisotropy of their connections in bipolar spectrum illnesses. Biological Psychiatry 57, 733–742.CrossRefGoogle ScholarPubMed
Hibar, DP, Westlye, LT, van Erp, TGM, Rasmussen, J, Leonardo, CD, Faskowitz, J, Haukvik, UK, Hartberg, CB, Doan, NT, Agartz, I, Dale, AM, Gruber, O, Krämer, B, Trost, S, Liberg, B, Abé, C, Ekman, CJ, Ingvar, M, Landén, M, Fears, SC, Freimer, NB, Bearden, CE, Sprooten, E, Glahn, DC, Pearlson, GD, Emsell, L, Kenney, J, Scanlon, C, McDonald, C, Cannon, DM, Almeida, J, Versace, A, Caseras, X, Lawrence, NS, Phillips, ML, Dima, D, Delvecchio, G, Frangou, S, Satterthwaite, TD, Wolf, D, Houenou, J, Henry, C, Malt, UF, Bøen, E, Elvsåshagen, T, Young, AH, Lloyd, AJ, Goodwin, GM, MacKay, CE, Bourne, C, Bilderbeck, A, Abramovic, L, Boks, MP, van Haren, NEM, Ophoff, RA, Kahn, RS, Bauer, M, Pfennig, A, Alda, M, Hajek, T, Mwangi, B, Soares, JC, Nickson, T, Dimitrova, R, Sussmann, JE, Hagenaars, S, Whalley, HC, McIntosh, AM, Thompson, PM, Andreassen, OA (2016). Subcortical volumetric abnormalities in bipolar disorder. Molecular Psychiatry 21, 1710–1716.CrossRefGoogle ScholarPubMed
Houenou, J, d'Albis, M-A, Vederine, F-E, Henry, C, Leboyer, M, Wessa, M (2012). Neuroimaging biomarkers in bipolar disorder. Frontiers in Bioscience (Elite edition) 4, 593–606.CrossRefGoogle ScholarPubMed
IBM SPSS Amos (2012). IBM SPSS Amos. IBM Software Business Analytics, YTD03114-U, 1–8.Google Scholar
Jeurissen, B, Leemans, A, Jones, DK, Tournier, J-D, Sijbers, J (2011). Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Human Brain Mapping 32, 461–479.CrossRefGoogle ScholarPubMed
Kenney, J, Anderson-Schmidt, H, Scanlon, C, Arndt, S, Scherz, E, McInerney, S, McFarland, J, Byrne, F, Ahmed, M, Donohoe, G, Hallahan, B, McDonald, C, Cannon, DM (2015). Cognitive course in first-episode psychosis and clinical correlates: a 4 year longitudinal study using the MATRICS Consensus Cognitive Battery. Schizophrenia Research 169, 101–108.CrossRefGoogle ScholarPubMed
Kocher, M, Gleichgerrcht, E, Nesland, T, Rorden, C, Fridriksson, J, Spampinato, MV, Bonilha, L (2015). Individual variability in the anatomical distribution of nodes participating in rich club structural networks. Frontiers in Neural Circuits 9, 16.CrossRefGoogle ScholarPubMed
Kumar, J, Iwabuchi, S, Oowise, S, Balain, V, Palaniyappan, L, Liddle, PF (2015). Shared white-matter dysconnectivity in schizophrenia and bipolar disorder with psychosis. Psychological Medicine 45, 759–770.CrossRefGoogle ScholarPubMed
Leemans, A, Jeurissen, B, Sijbers, J, Jones, DK (2009). ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. In Proceedings of the 17th Scientific Meeting, International Society for Magnetic Resonance in Medicine, 3537 (http://cds.ismrm.org/protected/09MProceedings/files/1_program.htm).Google Scholar
Leemans, A, Jones, DK (2009). The B-matrix must be rotated when correcting for subject motion in DTI data. Magnetic Resonance in Medicine 61, 1336–1349.CrossRefGoogle ScholarPubMed
Leow, A, Ajilore, O, Zhan, L, Arienzo, D, GadElkarim, J, Zhang, A, Moody, T, Van Horn, J, Feusner, J, Kumar, A, Thompson, P, Altshuler, L (2013). Impaired inter-hemispheric integration in bipolar disorder revealed with brain network analyses. Biological Psychiatry 73, 183–193.CrossRefGoogle ScholarPubMed
Levitt, JJ, 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.CrossRefGoogle ScholarPubMed
Li, W, Qin, W, Liu, H, Fan, L, Wang, J, Jiang, T, Yu, C (2013). Subregions of the human superior frontal gyrus and their connections. NeuroImage 78, 46–58.CrossRefGoogle ScholarPubMed
McAuley, JJ, da Fontoura Costa, L, Caetano, TS (2007). Rich-club phenomenon across complex network hierarchies. Applied Physics Letters 91, 84103.CrossRefGoogle Scholar
McCarthy, CS, Ramprashad, A, Thompson, C, Botti, J-A, Coman, IL, Kates, WR (2015). A comparison of FreeSurfer-generated data with and without manual intervention. Frontiers in Neuroscience 9, 379.CrossRefGoogle ScholarPubMed
Meskaldji, DE, Ottet, MC, Cammoun, L, Hagmann, P, Meuli, R, Eliez, S, Thiran, JP, Morgenthaler, S (2011). Adaptive strategy for the statistical analysis of connectomes. PLoS ONE 6, e23009.CrossRefGoogle ScholarPubMed
Nortje, G, Stein, DJ, Radua, J, Mataix-Cols, D, Horn, N (2013). Systematic review and voxel-based meta-analysis of diffusion tensor imaging studies in bipolar disorder. Journal of Affective Disorders 150, 192–200.CrossRefGoogle ScholarPubMed
O'Donoghue, S, Cannon, DM, Perlini, C, Brambilla, P, McDonald, C (2015). Applying neuroimaging to detect neuroanatomical dysconnectivity in psychosis. Epidemiology and Psychiatric Sciences 24, 298–302.CrossRefGoogle ScholarPubMed
Phillips, ML, Swartz, HA (2014). A critical appraisal of neuroimaging studies of bipolar disorder: toward a new conceptualization of underlying neural circuitry and a road map for future research. American Journal of Psychiatry 171, 829–843.CrossRefGoogle Scholar
Quigley, SJ, Scanlon, C, Kilmartin, L, Emsell, L, Langan, C, Hallahan, B, Murray, M, Waters, C, Waldron, M, Hehir, S, Casey, H, McDermott, E, Ridge, J, Kenney, J, Donoghue, SO, Nannery, R, Ambati, S, McCarthy, P, Barker, GJ, Cannon, DM (2015). Psychiatry research: neuroimaging volume and shape analysis of subcortical brain structures and ventricles in euthymic bipolar I disorder. Psychiatry Research: Neuroimaging 233, 324–330.CrossRefGoogle ScholarPubMed
Rorden, C, Karnath, H-O, Bonilha, L (2007). Improving lesion–symptom mapping. Journal of Cognitive Neuroscience 19, 1081–1088.CrossRefGoogle ScholarPubMed
RStudio Team (2012). RStudio: integrated development environment for R. RStudio, Inc.: Boston, MA (http://www.rstudio.com/).Google Scholar
Rubinov, M, Sporns, O (2010). Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52, 1059–1069.CrossRefGoogle ScholarPubMed
Scanlon, C, Anderson-Schmidt, H, Kilmartin, L, McInerney, S, Kenney, J, McFarland, J, Waldron, M, Ambati, S, Fullard, A, Logan, S, Hallahan, B, Barker, GJ, Elliott, MA, McCarthy, P, Cannon, DM, McDonald, C (2014). Cortical thinning and caudate abnormalities in first episode psychosis and their association with clinical outcome. Schizophrenia Research 159, 36–42.CrossRefGoogle ScholarPubMed
Senden, M, Deco, G, De Reus, MA, Goebel, R, Van Den Heuvel, MP (2014). Rich club organization supports a diverse set of functional network configurations. NeuroImage 96, 174–182.CrossRefGoogle ScholarPubMed
Skudlarski, P, Schretlen, DJ, Thaker, GK, Stevens, MC, Keshavan, MS, Sweeney, JA, Tamminga, CA, Clementz, BA, O'Neil, K, Pearlson, GD (2013). Diffusion tensor imaging white matter endophenotypes in patients with schizophrenia or psychotic bipolar disorder and their relatives. American Journal of Psychiatry 170, 886–898.CrossRefGoogle ScholarPubMed
Sporns, O (2012). From simple graphs to the connectome: networks in neuroimaging. NeuroImage 62, 881–886.CrossRefGoogle Scholar
Sporns, O, Tononi, G, Edelman, GM (2000). Connectivity and complexity: the relationship between neuroanatomy and brain dynamics. Neural Networks: the Official Journal of the International Neural Network Society 13, 909–922.CrossRefGoogle ScholarPubMed
Sporns, O, Van Den Heuvel, MP (2013). Network maps of the human brain's rich club. Network Science 1, 248–250.CrossRefGoogle Scholar
Strakowski, SM, Adler, CM, DelBello, MP (2002). Volumetric MRI studies of mood disorders: do they distinguish unipolar and bipolar disorder? Bipolar Disorders 4, 80–88.CrossRefGoogle ScholarPubMed
Strakowski, SM, DelBello, MP, Adler, C, Cecil, DM, Sax, KW (2000). Neuroimaging in bipolar disorder. Bipolar Disorders 2, 148–164.CrossRefGoogle ScholarPubMed
Strakowski, SM, Delbello, MP, Adler, CM (2005). The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Molecular Psychiatry 10, 105–116.CrossRefGoogle ScholarPubMed
Strakowski, SM, Eliassen, JC, Lamy, M, Cerullo, MA, Allendorfer, JB, Madore, M, Lee, JH, Welge, JA, Delbello, MP, Fleck, DE, Adler, CM (2011). Functional magnetic resonance imaging brain activation in bipolar mania: evidence for disruption of the ventrolateral prefrontal–amygdala emotional pathway. Biological Psychiatry 69, 381–388.CrossRefGoogle ScholarPubMed
Strakowski, SSM, Adler, CMC, Almeida, J, Altshuler, LL, Blumberg, HP, Chang, KD, DelBello, MP, Frangou, S, McIntosh, A, Phillips, ML, Sussman, JE, Townsend, JD (2012). The functional neuroanatomy of bipolar disorder: a consensus model. Bipolar Disorders 14, 313–325.CrossRefGoogle ScholarPubMed
Sussmann, JE, Lymer, GK, McKirdy, J, Moorhead, TW, Muñoz Maniega, S, Job, D, Hall, J, 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.CrossRefGoogle ScholarPubMed
Tournier, JD, Calamante, F, Connelly, A (2007). Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 35, 1459–1472.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.CrossRefGoogle ScholarPubMed
van den Heuvel, MP, Mandl, RCW, Stam, CJ, Kahn, RS, Hulshoff Pol, HE (2010). Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 30, 15915–15926.CrossRefGoogle ScholarPubMed
van den Heuvel, MP, Sporns, O (2011). Rich-club organization of the human connectome. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 31, 15775–15786.CrossRefGoogle ScholarPubMed
van den Heuvel, MP, Sporns, O, Collin, G, Scheewe, T, Mandl, RCW, Cahn, W, Goñi, J, Hulshoff Pol, HE, Kahn, RS (2013). Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70, 783–792.CrossRefGoogle ScholarPubMed
van Erp, TGM, Hibar, DP, Rasmussen, JM, Glahn, DC, Pearlson, GD, Andreassen, OA, Agartz, I, Westlye, LT, Haukvik, UK, Dale, AM, Melle, I, Hartberg, CB, Gruber, O, Kraemer, B, Zilles, D, Donohoe, G, Kelly, S, McDonald, C, Morris, DW, Cannon, DM, Corvin, A, Machielsen, MWJ, Koenders, L, de Haan, L, Veltman, DJ, Satterthwaite, TD, Wolf, DH, Gur, RC, Gur, RE, Potkin, SG, Mathalon, DH, Mueller, BA, Preda, A, Macciardi, F, Ehrlich, S, Walton, E, Hass, J, Calhoun, VD, Bockholt, HJ, Sponheim, SR, Shoemaker, JM, van Haren, NEM, Pol, HEH, Ophoff, RA, Kahn, RS, Roiz-Santiañez, R, Crespo-Facorro, B, Wang, L, Alpert, KI, Jönsson, EG, Dimitrova, R, Bois, C, Whalley, HC, McIntosh, AM, Lawrie, SM, Hashimoto, R, Thompson, PM, Turner, JA (2016). Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Molecular Psychiatry 21, 547–553.CrossRefGoogle ScholarPubMed
Vargas, C, López-Jaramillo, C, Vieta, E (2013). A systematic literature review of resting state network-functional MRI in bipolar disorder. Journal of Affective Disorders 150, 727–735.CrossRefGoogle ScholarPubMed
Vederine, F-E, Wessa, M, Leboyer, M, Houenou, J (2011). A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35, 1820–1826.CrossRefGoogle ScholarPubMed
Versace, A, Almeida, JRC, Hassel, S, Walsh, ND, Novelli, M, Klein, CR, Kupfer, DJ, Phillips, ML (2008). Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Archives of General Psychiatry 65, 1041–1052.CrossRefGoogle ScholarPubMed
Versace, A, Andreazza, AC, Young, LT, Fournier, JC, Almeida, JRC, Stiffler, RS, Lockovich, JC, Aslam, HA, Pollock, MH, Park, H, Nimgaonkar, VL, Kupfer, DJ, Phillips, ML (2014). Elevated serum measures of lipid peroxidation and abnormal prefrontal white matter in euthymic bipolar adults: toward peripheral biomarkers of bipolar disorder. Molecular Psychiatry 19, 200–208.CrossRefGoogle ScholarPubMed
Wessa, M, Kanske, P, Linke, J (2014). Bipolar disorder: a neural network perspective on a disorder of emotion and motivation. Restorative Neurology and Neuroscience 32, 51–62.CrossRefGoogle ScholarPubMed
Wheeler, AL, Wessa, M, Szeszko, PR, Foussias, G, Chakravarty, MM, Lerch, JP, DeRosse, P, Remington, G, Mulsant, BH, Linke, J, Malhotra, AK, Voineskos, AN (2015). Further neuroimaging evidence for the deficit subtype of schizophrenia. JAMA Psychiatry 72, 446–455.CrossRefGoogle ScholarPubMed
Wise, T, Radua, J, Nortje, G, Cleare, AJ, Young, AH, Arnone, D (2016). Voxel-based meta-analytical evidence of structural disconnectivity in major depression and bipolar disorder. Biological Psychiatry 79, 293–302.CrossRefGoogle ScholarPubMed
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
Zalesky, A, Cocchi, L, Fornito, A, Murray, MM, Bullmore, E (2012). Connectivity differences in brain networks. NeuroImage 60, 1055–1062.CrossRefGoogle ScholarPubMed
Zalesky, A, Fornito, A, Bullmore, ET (2010). Network-based statistic: identifying differences in brain networks. NeuroImage 53, 1197–1207.CrossRefGoogle ScholarPubMed
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