Connectome organization is related to longitudinal changes in general functioning, symptoms and IQ in chronic schizophrenia

Schizophrenia Research

Volumn 173, Issue 3, 2016, Pages 166-173

  Collin, G ^a   de Nijs, J ^a   Hulshoff Pol, H E ^a   Cahn, W ^a   van den Heuvel, M P ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Brain hubs; Connectome; Diffusion weighted imaging; Outcome; Rich club; Schizophrenia

Indexed keywords

ADULT; ARTICLE; CHRONIC PATIENT; CLINICAL ARTICLE; COHORT ANALYSIS; CONNECTOME; CONTROLLED STUDY; FEMALE; FOLLOW UP; HUMAN; INTELLIGENCE; INTELLIGENCE QUOTIENT; LONGITUDINAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; SCHIZOPHRENIA; SYMPTOM; BIPOLAR DISORDER; BRAIN; CHRONIC DISEASE; DIAGNOSTIC IMAGING; INTELLIGENCE TEST; MIDDLE AGED; NERVE TRACT; PATHOPHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; PSYCHOSIS; SIBLING; YOUNG ADULT;

ADULT; BIPOLAR DISORDER; BRAIN; CHRONIC DISEASE; CONNECTOME; FEMALE; FOLLOW-UP STUDIES; HUMANS; INTELLIGENCE; INTELLIGENCE TESTS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; PSYCHIATRIC STATUS RATING SCALES; PSYCHOTIC DISORDERS; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SIBLINGS; YOUNG ADULT;

EID: 84926139369     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2015.03.012     Document Type: Article

References (85)

1. Allen P., Luigjes J., Howes O.D., Egerton A., Hirao K., Valli I., Kambeitz J., Fusar-Poli P., Broome M., McGuire P. Transition to psychosis associated with prefrontal and subcortical dysfunction in ultra high-risk individuals. Schizophr. Bull. 2012, 38(6):1268-1276.
2. Allen P., Chaddock C.A., Egerton A., Howes O.D., Barker G., Bonoldi I., Fusar-Poli P., Murray R., McGuire P. Functional outcome in people at high risk for psychosis predicted by thalamic glutamate levels and prefronto-striatal activation. Schizophr. Bull. 2014, 41(2):429-439.
3. American Psychiatric Association Diagnostical and Statistical Manual of Mental Disorders 2000, (Washington, DC). 4th Ed. Text Rev.
4. Andreasen N.C., Flaum M., Arndt S. The comprehensive assessment of symptoms and history (CASH): an instrument for assessing diagnosis and psychopathology. Arch. Gen. Psychiatry 1992, 49(8):615-623.
5. Andreasen N.C., Carpenter W.T., Kane J.M., Lasser R.A., Marder S.R., Weinberger D.R. Remission in schizophrenia: proposed criteria and rationale for consensus. Am. J. Psychiatry 2005, 162:441-449.
6. Barder H.E., Sundet K., Rund B.R., Evensen J., Haahr U., Ten Velden Hegelstad W., Joa I., Johannessen J.O., Langeveld J., Larsen T.K., Melle I., Opjordsmoen S., Røssberg J.I., Simonsen E., Vaglum P., McGlashan T., Friis S. Ten year neurocognitive trajectories in first-episode psychosis. Front. Hum. Neurosci. 2013, 7(643):1-11.
7. Bassett D.S., Bullmore E.T., Verchinski B.A., Mattay V.S., Weinberger D.R., Meyer-Lindenberg A. Hierarchical organization of human cortical networks in health and schizophrenia. J. Neurosci. 2008, 28(37):9239-9248.
8. Bassett D.S., Bullmore E.T., Meyer-Lindenberg A., Apud J.A., Weinberger D.R., Coppola R. Cognitive fitness of cost-efficient brain functional networks. PNAS 2009, 106(28):11747-11752.
9. Behere R.V. Dorsolateral prefontal love volume and neurological soft signs as predictors of clinical social and functional outcome in schizophrenia: a longitudinal study. Indian J. Psychiatry 2013, 55(2):111-116.
10. Bewick V., Cheek L., Ball J. Statistics review 10: further nonparametric methods. Crit. Care 2004, 8(3):196-199.
11. Cahn W., Rais M., Stigter F.P., Van Haren N.E.M., Caspers E., Hulshoff Pol H.E., Xu Z., Schnack H.G., Kahn R.S. Psychosis and brain volume changes during the first five years of schizophrenia. Eur. Neuropsychopharmacol. 2009, 19(2):147-151.
12. Cheung V., Cheung C., McAlonan G.M., Deng Y., Wong J.G., Yip L., Tai K.S., Khong P.L., Sham P., Chua S.E. A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychol. Med. 2008, 38:877-885.
13. Colizza V., Flammini A., Serrano M., Vespignani A. Detecting rich-club ordering in complex networks. Nat. Phys. 2006, 2:110-115.
14. Collin G., Van den Heuvel M.P. The ontogeny of the human connectome: development and dynamic changes of brain connectivity across the life span. Neuroscientist 2013, 19(6):616-628.
15. Collin G., Kahn R., De Reus M., Cahn W., Van den Heuvel M. Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophr. Bull. 2014, 40(2):438-448.
16. Crossley N.A., Mechelli A., Scott J., Carletti F., Fox P.T., McGuire P., Bullmore E.T. The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 2014, 137:2382-2395.
17. Dauvermann M.R., Whalley H.C., Schmidt A., Lee G.L., Romaniuk L., Roberts N., Johnstone E.C., Lawrie S.M., Moorhead T.W.J. Computational neuropsychiatry-schizophrenia as a cognitive brain network disorder. Front. Psychiatry 2014, 5(30):1-19.
18. De Reus M.A., Van den Heuvel M.P. Estimating false positives and negatives in brain networks. NeuroImage 2013, 70:402-409.
19. De Reus M.A., Van den Heuvel M.P. Rich club organization and intermodule communication in the cat connectome. J. Neurosci. 2013, 33(32):12929-12939.
20. De Reus M.A., Van den Heuvel M.P. Simulated rich club lesioning in brain networks: a scaffold for communication and integration?. Front. Hum. Neurosci. 2014, 8(647):1-5.
21. Fischl B. FreeSurfer. NeuroImage 2012, 62(2):774-781.
22. Fornito A., Zalesky A., Pantelis C., Bullmore E.T. Schizophrenia, neuroimaging and connectomics. NeuroImage 2012, 62(4):2296-2314.
23. Fornito A., Harrison B.J., Goodby E., Dean A., Ooi C., Nathan P.J., Lennox B.R., Jones P.B., Suckling J., Bullmore E.T. Functional dysconnectivity of corticostriatal circuitry as a risk phenotype for psychosis. JAMA Psychiatry 2013, 70(11):1143-1151.
24. Hagmann P. From diffusion MRI to brain connectomics 2005, (PhD Thesis), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, (127 pp.).
25. Harriger L., Van den Heuvel M.P., Sporns O. Rich club organization of macaque cerebral cortex and its role in network communication. PLoS ONE 2012, 7:e46497.
26. Harvey P.D., Velligan D.I. International assessment of functional skills in people with schizophrenia. Innov. Clin. Neurosci. 2011, 8(1):15-18.
27. Harvey P.D., Helldin L., Bowie C.R., Heaton R.K., Olsson A., Hjärthag F., Norlander T., Patterson T.L. Performance-based measurement of functional disability in schizophrenia: a cross-national study in the United States and Sweden. Am. J. Psychiatry 2009, 166:821-827.
28. Hermes E.D.A., Sokoloff D.M., Stroup T.S., Rosenheck R.A. Minimum clinically important difference in the Positive and Negative Syndrome Scale using data from the CATIE Schizophrenia Trial. J. Clin. Psychiatry 2012, 73(4):526-532.
29. Ho B.C., Andreasen N.C., Nopoulos P., Arndt S., Magnotta V., Flaum M. Progressive structural brain abnormalities and their relationship to clinical outcome. Arch. Gen. Psychiatry 2003, 60:585-594.
30. Howes O.D., Bose S.K., Turkheimer F., Valli I., Egerton A., Valmaggia L.R., Murray R.M., McGuire P. Dopamine synthesis capacity before onset of psychosis: a prospective [18F]-DOPA PET imaging study. Am. J. Psychiatry 2011, 168:1311-1317.
31. Hulshoff Pol H.E., Kahn R.S. What happens after the first episode? A review of progressive brain changes in chronically ill patients with schizophrenia. Schizophr. Bull. 2008, 34(2):354-355.
32. Jahshan C., Heaton R.K., Golshan S., Cadenhead K.S. Course of neurocognitive deficits in the prodrome and first episode of schizophrenia. Neuropsychology 2010, 24(1):109-120.
33. Jbabdi S., Johansen-Berg H. Tractography: where do we go from here?. Brain Connect. 2011, 1(3):169-183.
34. Kasparek T., Prikryl R., Schwarz D., Kucerova H., Marecek R., Mikl M., Vanicek J., Ceskova E. Gray matter morphology and the level of functioning in one-year follow-up of first-episode schizophrenia patients. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:1438-1446.
35. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13(2):261-276.
36. Khodayari-Rostamabad A., Hasey G.M., Maccrimmon D.J., Reilly J.P., De Bruin H. A pilot study to determine whether machine learning methodologies using pre-treatment electroencephalography can predict the symptomatic response to clozapine therapy. Clin. Neurophysiol. 2010, 121:1998-2006.
37. Korver N., Quee P.J., Boos H.B.M., Simons C.J.P., De Haan L. Genetic Risk and Outcome of Psychosis (GROUP), a multi site longitudinal cohort study focused on gene-environment interaction: objectives, sample characteristics, recruitment and assessment methods. Int. J. Methods Psychiatr. Res. 2012, 21(3):205-221.
38. Leifker F.R., Bowie C.R., Harvey P.D. Determinants of everyday outcomes in schizophrenia: the influences of cognitive impairment, functional capacity, and symptoms. Schizophr. Res. 2009, 115:82-87.
39. Lieberman J.A. Is schizophrenia a neurodegenerative disorder? A clinical and neurobiological perspective. Biol. Psychiatry 1999, 46:729-739.
40. Lynall M., Bassett D.S., Kerwin R., Mckenna P.J., Müller U., Bullmore E.T. Functional connectivity and brain networks in schizophrenia. J. Neurosci. 2010, 30(28):9477-9487.
41. Mandl R.C.W., Rais M., Van Baal G.C.M., Van Haren N.E.M., Cahn W., Kahn R.S., Hulshoff Pol H.E. Altered white matter connectivity in never-medicated patients with schizophrenia. Hum. Brain Mapp. 2013, 34(9):2353-2365.
42. Martin E.A., Öngür D., Cohen B.M., Lewandowski K.E. Social functioning and age across affective and nonaffective psychoses. J. Nerv. Ment. Dis. 2015, 203(1):37-42.
43. McCrum-Gardner E. Which is the correct statistical test to use?. Br. J. Oral Maxillofac. Surg. 2008, 46(1):38-41.
44. Mechelli A., Riecher-Rossler A., Meisenzahl E.M., Tognin S., Wood S.J., Borgwardt S.J., Koutsouleris N., Yung A.R., Stone J.M., Phillips L.J., McGorry P.D., Valli I., Velakoulis D., Woolley J., Pantelis C., McGuire P. Neuroanatomical abnormalities that predate the onset of psychosis: a multicenter study. Arch. Gen. Psychiatry 2011, 68(5):489-495.
45. Mori S., Van Zijl P.C.M. Fiber tracking: principles and strategies-a technical review. NMR Biomed. 2002, 15(7-8):468-480.
46. Nejad A.B., Ebdrup B.H., Glenthøj B.Y., Siebner H.R. Brain connectivity studies in schizophrenia: unravelling the effects of antipsychotics. Curr. Neuropharmacol. 2012, 10:219-230.
47. Nejad A.B., Madsen K.H., Ebdrup B.H., Siebner H.R., Rasmussen H., Aggernæs B., Glenthøj B.Y., Baaré W.F. Neural markers of negative symptom outcomes in distributed working memory brain activity of antipsychotic-naïve schizophrenia patients. Int. J. Neuropsychopharmacol. 2013, 16:1195-1204.
48. Prasad K.M.R., Sahni S.D., Rohm B.R., Keshavan M.S. Dorsolateral prefrontal cortex morphology and short-term outcome in first-episode schizophrenia. Psychiatry Res. 2005, 140:147-155.
49. Rapoport J.L., Gogtay N. Childhood onset schizophrenia: support for a progressive neurodevelopmental disorder. Int. J. Dev. Neurosci. 2011, 29:251-258.
50. Repovs G., Csernansky J.G., Barch D.M. Brain network connectivity in individuals with schizophrenia and their siblings. Biol. Psychiatry 2011, 69(10):967-973.
51. Rubinov M., Bassett D.S. Emerging evidence of connectomic abnormalities in schizophrenia. J. Neurosci. 2011, 31(17):6263-6265.
52. Rubinov M., Bullmore E.T. Schizophrenia and abnormal brain network hubs. Dialogues Clin. Neurosci. 2013, 15(3):339-349.
53. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. NeuroImage 2010, 52(3):1059-1069.
54. Scholtens L.H., Schmidt R., De Reus M.A., Van den Heuvel M.P. Linking macroscale graph analytical organization to microscale neuroarchitectonics in the macaque connectome. J. Neurosci. 2014, 34(36):12192-12205.
55. Schultz S.K., Andreasen N.C. Schizophrenia. Lancet 1999, 353:1425-1430.
56. Senden M., Deco G., De Reus M.A., Goebel R., Van den Heuvel M.P. Rich club organization supports a diverse set of functional network configurations. NeuroImage 2014, 96:174-182.
57. Shanahan M., Bingman V.P., Shimizu T., Wild M., Güntürkün O. Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis. Front. Comput. Neurosci. 2013, 7(89):1-16.
58. Skudlarski P., Jagannathan K., Anderson K., Stevens M.C., Calhoun V.D., Skudlarska B.A., Pearlson G. Brain connectivity is not only lower but different in schizophrenia: a combined anatomical and functional approach. Biol. Psychiatry 2010, 68(1):61-69.
59. Skudlarski P., Schretlen D.J., Thaker G.K., Stevens M.C., Keshavan M.S., Sweeney J.A., Tamminga C.A., Clementz B.A., O'Neil K., Pearlson G.D. Diffusion tensor imaging white matter endophenotypes in patients with schizophrenia or psychotic bipolar disorder and their relatives. Am. J. Psychiatry 2013, 170:886-898.
60. Sporns O., Tononi G., Kötter R. The human connectome: a structural description of the human brain. PLoS Comput. Biol. 2005, 1(4):e42. (245-251).
61. Stefanis N.C., Hanssen M., Smirnis N.K., Avramopoulos D.A., Evdokimidis I.K., Stefanis C.N., Verdoux H., Van Os J. Evidence that three dimensions of psychosis have a distribution in the general population. Psychol. Med. 2002, 32(2):347-358.
62. Stephan K.E., Friston K.J., Frith C.D. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr. Bull. 2009, 35(3):509-527.
63. Stinissen J., Willems P.J., Coetsier P., Hulsman W.L.L. Manual to the Dutch Version of the Wechsler Adult Intelligence Scale (W.A.I.S.) 1970, Swets & Zeitlinger, Amsterdam, Lisse.
64. Swapnil G., Kulhara P. What is schizophrenia: a neurodevelopmental or neurodegenerative disorder or a combination of both? A critical analysis. Indian J. Psychiatry 2010, 52(1):21-27.
65. Szeszko P.R., Robinson D.G., Ikuta T., Peters B.D., Gallego J.A., Kane J., Malhotra A.K. White matter changes associated with antipsychotic treatment in first-episode psychosis. Neuropsychopharmacology 2014, 39:1324-1331.
66. Terwisscha van Scheltinga A.F., Bakker S.C., Van Haren N.E.M., Derks E.M., Buizer-Voskamp J.E., Boos H.B.M., Cahn W., Hulshoff Pol H.E., Ripke S., Ophoff R.A., Kahn R.S. Genetic schizophrenia risk variants jointly modulate total brain and white matter volume. Biol. Psychiatry 2013, 73:525-531.
67. Thompson W.K., Savla G.N., Vahia I.V., Depp D.A., O'Hara R., Jeste D.V., Palmer B.W. Characterizing trajectories of cognitive functioning in older adults with schizophrenia: does method matter?. Schizophr. Res. 2013, 143:90-95.
68. Tognin S., Pettersson-Yeo W., Valli I., Hutton C., Woolley J., Allen P., McGuire Philip, Mechelli Andrea Using structural neuroimaging to make quantitative predictions of symptom progression in individuals at ultra-high risk for psychosis. Front. Psychiatry 2013, 4(187):1-9.
69. Towlson E.K., Vértes P.E., Ahnert S.E., Schafer W.R., Bullmore E.T. The rich club of the C. elegans neuronal connectome. J. Neurosci. 2013, 33(15):6380-6387.
70. Van den Heuvel M.P., De Reus M.A. Chasing the dreams of early connectionists. ACS Chem. 2014, 5:491-493.
71. Van den Heuvel M.P., Fornito A. Brain networks in schizophrenia. Neuropsychol. Rev. 2014, 24(1):32-48.
72. Van den Heuvel M.P., Kahn R.S. Abnormal brain wiring as a pathogenetic mechanism in schizophrenia. Biol. Psychiatry 2011, 70(12):1107-1108.
73. Van den Heuvel M.P., Sporns O. Rich-club organization of the human connectome. J. Neurosci. 2011, 31(44):15775-15786.
74. Van den Heuvel M.P., Sporns O. Network hubs in the human brain. Trends Cogn. Sci. 2013, 17(12):683-696.
75. Van den Heuvel M.P., Mandl R.C.W., Stam C.J., Kahn R.S., Hulshoff Pol H.E. Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J. Neurosci. 2010, 30(47):15915-15926.
76. Van den Heuvel M.P., Kahn R.S., Goñi J., Sporns O. High-cost, high-capacity backbone for global brain communication. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(28):11372-11377.
77. Van den Heuvel M.P., Sporns O., Collin G., Scheewe T., Mandl R.C.W., Cahn W., Goñi J., Hulshoff Pol H.E., Kahn R.S. Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 2013, 70(8):783-792.
78. Van Veelen N.M.J., Vink M., Ramsey N.F., Van Buuren M., Hoogendam J.M., Kahn R.S. Prefrontal lobe dysfunction predicts treatment response in medication-naive first-episode schizophrenia. Schizophr. Res. 2011, 129(2-3):156-162.
79. Vita A., De Peri L., Deste G., Sacchetti E. Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Transl. Psychiatry 2012, 2(e190):1-13.
80. Wang Q., Su T.P., Zhou Y., Chou K.H., Chen I.Y., Jiang T., Lin C.P. Anatomical insights into disrupted small-world networks in schizophrenia. NeuroImage 2012, 59:1085-1093.
81. Wheeler A.L., Voineskos A.N. A review of structural neuroimaging in schizophrenia: from connectivity to connectomics. Front. Hum. Neurosci. 2014, 8(e653):1-18.
82. Woods B.T. Is schizophrenia a progressive neurodevelopmental disorder? Toward a unitary pathogenetic mechanism. Am. J. Psychiatry 1998, 155(12):1661-1670.
83. Yu Q., Sui J., Rachakonda S., He H., Gruner W., Pearlson G., Kiehl K.A., Calhoun V.D. Altered topological properties of functional network connectivity in schizophrenia during resting state: a small world brain network study. PLoS ONE 2011, 6(9):e25423. (1-12).
84. Zamora-López G., Zhou C., Kurths J. Graph analysis of cortical networks reveals complex anatomical communication substrate. Chaos 2009, 19(1):015117.
85. Zanelli J. Trajectory of Neurocognitive Functioning in Psychotic Disorders 2012, (PhD Thesis), Institute of Psychiatry, King's college London, London, (153 pp.).