Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-24T17:58:16.729Z Has data issue: false hasContentIssue false
  • English
  • Français

Structural brain network differences in bipolar disorder using with similarity-based approach

Published online by Cambridge University Press:  22 December 2020

Miho Ota Open the ORCID record for Miho Ota [Opens in a new window] ,
Takamasa Noda ,
Noriko Sato ,
Shinsuke Hidese ,
Toshiya Teraishi ,
Hiroshi Matsuda  and
Hiroshi Kunugi
Miho Ota*
Affiliation:
Department of Mental Disorder Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
Takamasa Noda
Affiliation:
Department of Psychiatry, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
Noriko Sato
Affiliation:
Department of Radiology, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
Shinsuke Hidese
Affiliation:
Department of Mental Disorder Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
Toshiya Teraishi
Affiliation:
Department of Mental Disorder Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
Hiroshi Matsuda
Affiliation:
Integrative Brain Imaging Center, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
Hiroshi Kunugi
Affiliation:
Department of Mental Disorder Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo187-8502, Japan
*
Author for correspondence: Miho Ota, Email: ota@ncnp.go.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective: Previous studies have shown differences in the regional brain structure and function between patients with bipolar disorder (BD) and healthy subjects, but little is known about the structural connectivity between BD patients and healthy subjects. In this study, we evaluated the disease-related changes in regional structural connectivity derived from gray matter magnetic resonance imaging (MRI) scans. Methods: The subjects were 73 patients with BD and 80 healthy volunteers who underwent 3-Tesla MRI. Network metrics, such as the small world properties, were computed. We also performed rendering of the network metric images such as the degree, betweenness centrality, and clustering coefficient, on individual brain image. Then, we estimated the differences between them, and evaluate the relationships between the clinical symptoms and the network metrics in the patients with BD. Results: BD patients showed a lower clustering coefficient in the right parietal region and left occipital region, compared with healthy subjects. A weak negative correlation between Young mania rating scale and clustering coefficient was found in left anterior cingulate cortex. Conclusions: We found differences in gray matter structural connectivity between BD patients and healthy subjects by a similarity-based approach. These points may provide objective biological information as an adjunct to the clinical diagnosis of BD.

Keywords

bipolar disorderclustering coefficientdegreesmall world propertystructural brain network
Type
Original Article
Information
Acta Neuropsychiatrica , Volume 33 , Issue 3 , June 2021 , pp. 121 - 125
Check for updates
Copyright
© Scandinavian College of Neuropsychopharmacology 2020

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

Ambrosi, E, Rossi-Espagnet, MC, Kotzalidis, GD, Comparelli, A, Del Casale, A, Carducci, F, Romano, A, Manfredi, G, Tatarelli, R, Bozzao, A and Girardi, P (2013) Structural brain alterations in bipolar disorder II: a combined voxel-based morphometry (VBM) and diffusion tensor imaging (DTI) study. Journal of Affective Disorders 150, 610–615.CrossRefGoogle ScholarPubMed
American Psychiatric Association (1997) Practice Guidelines for the Treatment of Patients with Schizophrenia. American Psychiatric Press: Washington, DC.Google Scholar
American Psychiatric Association (2013) DSM-V: diagnostic and Statistical Manual of Mental Disorders, 5th Edn. American Psychiatric Press: Washington, DC.Google Scholar
Angst, J, Gamma, A, Benazzi, F, Ajdacic, V, Eich, D and Rossler, W (2003) Toward a re-definition of subthreshold bipolarity: epidemiology and proposed criteria for bipolar-II, minor bipolar disorders and hypomania. Journal of Affective Disorders 73, 133–146.CrossRefGoogle Scholar
Ashburner, J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38, 95–113.CrossRefGoogle ScholarPubMed
Blumberg, HP, Stern, E, Martinez, D, Ricketts, S, de Asis, J, White, T, Epstein, J, McBride, PA, Eidelberg, D, Kocsis, JH and Silbersweig, DA (2000) Increased anterior cingulate and caudate activity in bipolar mania. Biologycal Psychiatry 48, 1045–1052.CrossRefGoogle ScholarPubMed
Bullmore, E and Sporns, O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience 10, 186–198.CrossRefGoogle ScholarPubMed
Collin, G, van den Heuvel, MP, Abramovic, L, Vreeker, A, de Reus, MA, van Haren, NE, Boks, MP, Ophoff, RA and Kahn, RS (2016) Brain network analysis reveals affected connectome structure in bipolar I disorder. Human Brain Mapping 37, 122–134.CrossRefGoogle ScholarPubMed
Ellison-Wright, I and Bullmore, E (2010) Anatomy of bipolar disorder and schizophrenia: a meta-analysis. Schizophrenia Research 117, 1–12.CrossRefGoogle ScholarPubMed
Ferrier, IN, Chowdhury, R, Thompson, JM, Watson, S and Young, AH (2004) Neurocognitive function in unaffected first-degree relatives of patients with bipolar disorder: a preliminary report. Bipolar Disorders 6, 319–322.CrossRefGoogle ScholarPubMed
Forde, NJ, O’Donoghue, S, Scanlon, C, Emsell, L, Chaddock, C, Leemans, A, Jeurissen, B, Barker, GJ, Cannon, DM, Murray, RM and McDonald, C (2015) Structural brain network analysis in families multiply affected with bipolar I disorder. Psychiatry Research 234, 44–51.CrossRefGoogle ScholarPubMed
Ganzola, R and Duchesne, S (2017) Voxel-Based morphometry meta-analysis of gray and white matter finds significant areas of differences in bipolar patients from healthy controls. Bipolar Disorders 19, 74–83.CrossRefGoogle ScholarPubMed
Gasquoine, PG (2013) Localization of function in anterior cingulate cortex: from psychosurgery to functional neuroimaging. Neuroscience & Biobehavioral Reviews 37, 340–348.CrossRefGoogle ScholarPubMed
Goodwin, GM, Cavanagh, JT, Glabus, MF, Kehoe, RF, O’Carroll, RE and Ebmeier, KP (1997) Uptake of 99mTc-exametazime shown by single photon emission computed tomography before and after lithium withdrawal in bipolar patients: associations with mania. British Journal of Psychiatry 170, 426–430.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 and 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 of depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle Scholar
Hirschfeld, RM and Vornik, LA (2005) Bipolar disorder - costs and comorbidity. The American Journal of Managed Care 11, S85–S90.Google ScholarPubMed
Hosseini, SM, Hoeft, F and Kesler, SR (2012) GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain networks. PLoS One 7, e40709.CrossRefGoogle ScholarPubMed
Houenou, J, Frommberger, J, Carde, S, Glasbrenner, M, Diener, C, Leboyer, M and Wessa, M (2011) Neuroimaging-Based markers of bipolar disorder: evidence from two meta-analyses. Journal of Affective Disorders 132, 344–355.CrossRefGoogle ScholarPubMed
Humphries, MD, Gurney, K and Prescott, TJ (2006) The brainstem reticular formation is a small-world, not scale-free, network. Proceedings of the Royal Society B: Biological Sciences 273, 503–511.CrossRefGoogle Scholar
Inada, T and Inagaki, A (2015) Psychotropic dose equivalence in Japan. Psychiatry and Clinical Neurosciences 69, 440–447.CrossRefGoogle ScholarPubMed
Jenkins, LM, Barba, A, Campbell, M, Lamar, M, Shankman, SA, Leow, AD, Ajilore, O and Langenecker, SA (2016) Shared white matter alterations across emotional disorders: a voxel-based meta-analysis of fractional anisotropy. Neuroimage. Clinical 12, 1022–1034.CrossRefGoogle ScholarPubMed
Kate, MT, Visser, PJ, Bakardjian, H, Barkhof, F, Sikkes, SAM, van der Flier, WM, Scheltens, P, Hampel, H, Habert, MO, Dubois, B and Tijms, BM (2018) Gray matter network disruptions and regional amyloid beta in cognitively normal adults. Frontiers in Aging Neuroscience 10, 67.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 and Altshuler, L (2013) Impaired inter-hemispheric integration in bipolar disorder revealed with brain network analyses. Biological Psychiatry 73, 183–193.CrossRefGoogle ScholarPubMed
Makris, N, Kennedy, DN, McInerney, S, Sorensen, AG, Wang, R, Caviness, VS Jr and Pandya, DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cerebral Cortex 15, 854–869.CrossRefGoogle ScholarPubMed
Merikangas, KR, Akiskal, HS, Angst, J, Greenberg, PE, Hirschfeld, RM, Petukhova, M and Kessler, RC (2007) Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. Archives of General Psychiatry 64, 543–552.CrossRefGoogle ScholarPubMed
Narrow, WE, Rae, DS, Robins, LN and Regier, DA (2002) Revised prevalence estimates of mental disorders in the United States: using a clinical significance criterion to reconcile two surveys’ estimates. Archives of General Psychiatry 59, 115–123.CrossRefGoogle Scholar
Noble, WS (2009) How does multiple testing correction work? Nature Biotechnology 27, 1135–1137.CrossRefGoogle ScholarPubMed
Nortje, G, Stein, DJ, Radua, J, Mataix-Cols, D and 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, Kilmartin, L, O’Hora, D, Emsell, L, Langan, C, McInerney, S, Forde, NJ, Leemans, A, Jeurissen, B, Barker, GJ, McCarthy, P, Cannon, DM and McDonald, C (2017) Anatomical integration and rich-club connectivity in euthymic bipolar disorder. Psychological Medicine 47, 1609–1623.CrossRefGoogle ScholarPubMed
Perry, A, Roberts, G, Mitchelle, PB, Breakspea, M (2019) Connectomics of bipolar disorder: a critical review, and evidence for dynamic instabilities within interoceptive networks. Molecular Psychiatry 24, 1296–318.CrossRefGoogle ScholarPubMed
Rimol, LM, Hartberg, CB, Nesvåg, R, Fennema-Notestine, C, Hagler, DJ Jr, Pung, CJ, Jennings, RG, Haukvik, UK, Lange, E, Nakstad, PH, Melle, I, Andreassen, OA, Dale, AM and Agartz, I (2010) Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry 68, 41–50.CrossRefGoogle ScholarPubMed
Rinkus, CM, Schoonheim, MM, Steenwijk, MD, Vrenken, H, Eijlers, AJC, Killestein, J, Wattjes, MP, Leite, CC, Barkhof, F and Tijms, BM (2019) Gray matter networks and cognitive impairment in multiple sclerosis. Multiple Sclerosis 25, 382–391.CrossRefGoogle Scholar
Roberts, G, Perry, A, Lord, A, Frankland, A, Leung, V, Holmes-Preston, E, Levy, F, Lenroot, RK, Mitchell, PB and Breakspear, M (2016) Structural dysconnectivity of key cognitive and emotional hubs in young people at high genetic risk for bipolar disorder. Molecular Psychiatry 23, 413–421.CrossRefGoogle ScholarPubMed
Rubinsztein, JS, Fletcher, PC, Rogers, RD, Ho, LW, Aigbirhio, FI, Paykel, ES, Robbins, TW and Sahakian, BJ (2001) Decision-Making in mania: a PET study. Brain 124, 2550–2563.CrossRefGoogle ScholarPubMed
Schmahmann, JD (2004) Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. Journal of Neuropsychiatry and Clinical Neuroscience 16, 367–378.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R and Dunbar, GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59: 22–57.Google ScholarPubMed
Strakowski, SM, Delbello, MP and Adler, CM (2005) The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Molecular Psychiatry 10, 105–116.CrossRefGoogle ScholarPubMed
Sweeney, JA, Kmiec, JA and Kupfer, DJ (2000) Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biological Psychiatry 48, 674–684.CrossRefGoogle ScholarPubMed
Tijms, BM, Seriès, P, Willshaw, DJ and Lawrie, SM (2012) Similarity-Based extraction of individual networks from gray matter MRI scans. Cerebral Cortex 22, 1530–1541.CrossRefGoogle ScholarPubMed
Tijms, BM, Möller, C, Vrenken, H, Wink, AM, de Haan, W, van der Flier, WM, Stam, CJ, Scheltens, P and Barkhof, F (2013) Single-subject grey matter graphs in Alzheimer’s disease. PLoS One 8, e58921.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B and 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
Versace, A, Almeida, JR, Quevedo, K, Thompson, WK, Terwilliger, RA, Hassel, S, Kupfer, DJ and Phillips, ML (2010) Right orbitofrontal corticolimbic and left corticocortical white matter connectivity differentiate bipolar and unipolar depression. Biological Psychiatry 68: 560–567.CrossRefGoogle ScholarPubMed
Wang, Y, Wang, J, Jia, Y, Zhong, S, Zhong, M, Sun, Y, Niu, M, Zhao, L, Zhao, L, Pan, J, Huang, L and Huang, R (2017) Topologically convergent and divergent functional connectivity patterns in unmedicated unipolar depression and bipolar disorder. Translational Psychiatry 7: e1165.CrossRefGoogle ScholarPubMed
Young, RC, Biggs, JT, Ziegler, VE and Meyer, DA (1978) A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133: 429–435.CrossRefGoogle ScholarPubMed