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Abnormal Structural Network Communication Reflects Cognitive Deficits in Schizophrenia

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Abstract

Schizophrenia has long been thought to be a disconnection syndrome and several previous studies have reported widespread abnormalities in white matter tracts in individuals with schizophrenia. Furthermore, reductions in structural connectivity may also impair communication between anatomically unconnected pairs of brain regions, potentially impacting global signal traffic in the brain. Therefore, we used different communication models to examine direct and indirect structural connections (polysynaptic) communication in large-scale brain networks in schizophrenia. Diffusion-weighted magnetic resonance imaging scans were acquired from 62 patients diagnosed with schizophrenia and 35 controls. In this study, we used five network communication models including, shortest paths, navigation, diffusion, search information and communicability to examine polysynaptic communication in large-scale brain networks in schizophrenia. We showed less efficient communication between spatially widespread brain regions particulary encompassing cortico-subcortical basal ganglia network in schizophrenia group relative to controls. Then, we also examined whether reduced communication efficiency was related to clinical symptoms in schizophrenia group. Among different measures of communication efficiency, only navigation efficiency was associated with global cognitive impairment across multiple cognitive domains including verbal learning, processing speed, executive functions and working memory, in individuals with schizophrenia. We did not find any association between communication efficiency measures and positive or negative symptoms within the schizophrenia group. Our findings are important for improving our mechanistic understanding of neurobiological process underlying cognitive symptoms in schizophrenia.

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References

  • Abdelnour F, Voss HU, Raj A (2014) Network diffusion accurately models the relationship between structural and functional brain connectivity networks. Neuroimage 90:335–347

    Article  PubMed  Google Scholar 

  • Addington D, Addington J, Maticka-Tyndale E (1994) Specificity of the calgary depression scale for schizophrenics. Schizophr Res 11(3):239–244

    Article  CAS  PubMed  Google Scholar 

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    Article  CAS  PubMed  Google Scholar 

  • Alloza C, Bastin ME, Cox SR, Gibson J, Duff B, Semple SI, Whalley HC, Lawrie SM (2017) Central and non-central networks, cognition, clinical symptoms, and polygenic risk scores in schizophrenia. Hum Brain Mapp 38(12):5919–5930

    Article  PubMed  PubMed Central  Google Scholar 

  • Andersson JL, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078

    Article  PubMed  Google Scholar 

  • Andreasen NC (1984) Scale for the assessment of positive symptoms. University of Iowa, Iowa City

    Google Scholar 

  • Andreotti J, Jann K, Melie-Garcia L, Giezendanner S, Abela E, Wiest R, Dierks T, Federspiel A (2014) Validation of network communicability metrics for the analysis of brain structural networks. PLoS ONE 9(12):e115503

    Article  PubMed  PubMed Central  Google Scholar 

  • Aquila R, Citrome L (2015) Cognitive impairment in schizophrenia: the great unmet need. CNS Spectr 20(1):32–40

    Article  Google Scholar 

  • Avena-Koenigsberger A, Misic B, Hawkins RX, Griffa A, Hagmann P, Goni J, Sporns O (2017) Path ensembles and a tradeoff between communication efficiency and resilience in the human connectome. Brain Struct Funct 222(1):603–618

    Article  PubMed  Google Scholar 

  • Avena-Koenigsberger A, Misic B, Sporns O (2018) Communication dynamics in complex brain networks. Nat Rev Neurosci 19(1):17–33

    Article  CAS  Google Scholar 

  • Avram M, Brandl F, Bauml J, Sorg C (2018) Cortico-thalamic hypo- and hyperconnectivity extend consistently to basal ganglia in schizophrenia. Neuropsychopharmacology 43(11):2239–2248

    Article  PubMed  PubMed Central  Google Scholar 

  • Avram M, Brandl F, Cabello J, Leucht C, Scherr M, Mustafa M, Leucht S, Ziegler S, Sorg C (2019) Reduced striatal dopamine synthesis capacity in patients with schizophrenia during remission of positive symptoms. Brain 142(6):1813–1826

    Article  PubMed  Google Scholar 

  • Aydemir Ö, Esen Danacı A, Deveci A, İçelli İ (2000) Calgary Şizofrenide Depresyon Ölçeği’nin Türkçe versiyonunun güvenilirliği ve geçerliliği. Nöropsikiyatri Arşivi 37(1):82–86

    Google Scholar 

  • Bassett DS, Bullmore E (2006) Small-world brain networks. Neuroscientist 12(6):512–523

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodo 57(1):289–300

    Google Scholar 

  • Boguñá M, Krioukov D, Claffy KC (2009) Navigability of complex networks. Nat Phys 5(1):74–80

    Article  Google Scholar 

  • Bora E, Yucel M, Pantelis C (2009) Cognitive functioning in schizophrenia, schizoaffective disorder and affective psychoses: meta-analytic study. Br J Psychiatry 195(6):475–482

    Article  PubMed  Google Scholar 

  • Bora E, Yucel M, Pantelis C (2010) Cognitive impairment in schizophrenia and affective psychoses: implications for DSM-V criteria and beyond. Schizophr Bull 36(1):36–42

    Article  PubMed  Google Scholar 

  • Bora E, Binnur Akdede B, Alptekin K (2017) Neurocognitive impairment in deficit and non-deficit schizophrenia: a meta-analysis. Psychol Med 47(14):2401–2413

    Article  CAS  PubMed  Google Scholar 

  • Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13(5):336–349

    Article  CAS  PubMed  Google Scholar 

  • Cea-Canas B, de Luis R, Lubeiro A, Gomez-Pilar J, Sotelo E, Del Valle P, Gomez-Garcia M, Alonso-Sanchez A, Molina V (2019) Structural connectivity in schizophrenia and bipolar disorder: effects of chronicity and antipsychotic treatment. Prog Neuropsychopharmacol Biol Psychiatry 92:369–377

    Article  CAS  PubMed  Google Scholar 

  • Cocchi L, Harding IH, Lord A, Pantelis C, Yucel M, Zalesky A (2014) Disruption of structure-function coupling in the schizophrenia connectome. Neuroimage Clin 4:779–787

    Article  PubMed  PubMed Central  Google Scholar 

  • Collin G, Kahn RS, de Reus MA, Cahn W, van den Heuvel MP (2014) Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophr Bull 40(2):438–448

    Article  PubMed  Google Scholar 

  • Conn KA, Burne THJ, Kesby JP (2020) Subcortical dopamine and cognition in schizophrenia: looking beyond psychosis in preclinical models. Front Neurosci 14:542

    Article  PubMed  PubMed Central  Google Scholar 

  • Crofts JJ, Higham DJ (2009) A weighted communicability measure applied to complex brain networks. J R Soc Interface 6(33):411–414

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui LB, Wei Y, Xi YB, Griffa A, De Lange SC, Kahn RS, Yin H, Van den Heuvel MP (2019) Connectome-based patterns of first-episode medication-naive patients with schizophrenia. Schizophr Bull 45(6):1291–1299

    Article  PubMed  PubMed Central  Google Scholar 

  • Dikmeer N, Besiroglu L, Di Biase MA, Zalesky A, Kasal MI, Bilge A, Durmaz E, Polat S, Gelal F, Zorlu N (2021) White matter microstructure and connectivity in patients with obsessive-compulsive disorder and their unaffected siblings. Acta Psychiatr Scand 143(1):72–81

    Article  PubMed  Google Scholar 

  • Dong D, Wang Y, Chang X, Luo C, Yao D (2018) Dysfunction of large-scale brain networks in schizophrenia: a meta-analysis of resting-state functional connectivity. Schizophr Bull 44(1):168–181

    Article  PubMed  Google Scholar 

  • Dong D, Yao D, Wang Y, Hong SJ, Genon S, Xin F, Jung K, He H, Chang X, Duan M, Bernhardt BC, Margulies DS, Sepulcre J, Eickhoff SB, Luo C (2021) Compressed sensorimotor-to-transmodal hierarchical organization in schizophrenia. Psychol Med. https://doi.org/10.1017/S0033291721002129

    Article  PubMed  Google Scholar 

  • Drakesmith M, Caeyenberghs K, Dutt A, Zammit S, Evans CJ, Reichenberg A, Lewis G, David AS, Jones DK (2015) Schizophrenia-like topological changes in the structural connectome of individuals with subclinical psychotic experiences. Hum Brain Mapp 36(7):2629–2643

    Article  PubMed  PubMed Central  Google Scholar 

  • Estrada E, Hatano N (2008) Communicability in complex networks. Phys Rev E Stat Nonlin Soft Matter Phys 77(3):036111

    Article  PubMed  Google Scholar 

  • Fornito A, Harrison BJ, Goodby E, Dean A, Ooi C, Nathan PJ, Lennox BR, Jones PB, Suckling J, Bullmore ET (2013) Functional dysconnectivity of corticostriatal circuitry as a risk phenotype for psychosis. JAMA Psychiat 70(11):1143–1151

    Article  Google Scholar 

  • Friston KJ, Frith CD (1995) Schizophrenia: a disconnection syndrome? Clin Neurosci 3(2):89–97

    CAS  PubMed  Google Scholar 

  • Girardi-Schappo M, Fadaie F, Lee HM, Caldairou B, Sziklas V, Crane J, Bernhardt BC, Bernasconi A, Bernasconi N (2021) Altered communication dynamics reflect cognitive deficits in temporal lobe epilepsy. Epilepsia 62(4):1022–1033

    Article  PubMed  Google Scholar 

  • Goni J, Avena-Koenigsberger A, Velez de Mendizabal N, van den Heuvel MP, Betzel RF, Sporns O (2013) Exploring the morphospace of communication efficiency in complex networks. PLoS ONE 8(3):e58070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goni J, Van Den Heuvel MP, Avena-Koenigsberger A, De Mendizabal NV, Betzel RF, Griffa A, Hagmann P, Corominas-Murtra B, Thiran J-P, Sporns O (2014) Resting-brain functional connectivity predicted by analytic measures of network communication. Proc Natl Acad Sci USA 111(2):833–838

    Article  CAS  PubMed  Google Scholar 

  • Green MF (1996) What are the functional consequences of neurocognitive deficits in schizophrenia? Am J Psychiatry 153(3):321–330

    Article  CAS  PubMed  Google Scholar 

  • Green MF, Horan WP, Lee J (2019) Nonsocial and social cognition in schizophrenia: current evidence and future directions. World Psychiatry 18(2):146–161

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffa A, Baumann PS, Ferrari C, Do KQ, Conus P, Thiran JP, Hagmann P (2015) Characterizing the connectome in schizophrenia with diffusion spectrum imaging. Hum Brain Mapp 36(1):354–366

    Article  PubMed  Google Scholar 

  • Guo JY, Ragland JD, Carter CS (2019) Memory and cognition in schizophrenia. Mol Psychiatry 24(5):633–642

    Article  CAS  PubMed  Google Scholar 

  • Haber SN (2016) Corticostriatal circuitry. Dialogues Clin Neurosci 18(1):7–21

    Article  PubMed  PubMed Central  Google Scholar 

  • Hinault T, Kraut M, Bakker A, Dagher A, Courtney SM (2020) Disrupted neural synchrony mediates the relationship between white matter integrity and cognitive performance in older adults. Cereb Cortex 30(10):5570–5582

    Article  CAS  PubMed  Google Scholar 

  • Imms P, Domínguez DJF, Burmester A, Seguin C, Clemente A, Dhollander T, Wilson PH, Poudel G, Caeyenberghs K (2021) Navigating the link between processing speed and network communication in the human brain. Brain Struct Funct 226(4):1281–1302

    Article  PubMed  Google Scholar 

  • Jbabdi S, Johansen-Berg H (2011) Tractography: where do we go from here? Brain Connect 1(3):169–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaiser M, Hilgetag CC (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2(7):e95

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaufmann T, Skatun KC, Alnaes D, Doan NT, Duff EP, Tonnesen S, Roussos E, Ueland T, Aminoff SR, Lagerberg TV, Agartz I, Melle IS, Smith SM, Andreassen OA, Westlye LT (2015) Disintegration of sensorimotor brain networks in schizophrenia. Schizophr Bull 41(6):1326–1335

    Article  PubMed  PubMed Central  Google Scholar 

  • Kellner E, Dhital B, Kiselev VG, Reisert M (2016) Gibbs-ringing artifact removal based on local subvoxel-shifts. Magn Reson Med 76(5):1574–1581

    Article  PubMed  Google Scholar 

  • Kelly S, Jahanshad N, Zalesky A et al (2018) Widespread white matter microstructural differences in schizophrenia across 4322 individuals: results from the ENIGMA Schizophrenia DTI Working Group. Mol Psychiatry 23(5):1261–1269

    Article  CAS  PubMed  Google Scholar 

  • Kesby JP, Eyles DW, McGrath JJ, Scott JG (2018) Dopamine, psychosis and schizophrenia: the widening gap between basic and clinical neuroscience. Transl Psychiatry 8(1):30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirkpatrick B, Strauss GP, Nguyen L, Fischer BA, Daniel DG, Cienfuegos A, Marder SR (2011) The brief negative symptom scale: psychometric properties. Schizophr Bull 37(2):300–305

    Article  PubMed  Google Scholar 

  • Klauser P, Baker ST, Cropley VL, Bousman C, Fornito A, Cocchi L, Fullerton JM, Rasser P, Schall U, Henskens F, Michie PT, Loughland C, Catts SV, Mowry B, Weickert TW, Shannon Weickert C, Carr V, Lenroot R, Pantelis C, Zalesky A (2017) White matter disruptions in schizophrenia are spatially widespread and topologically converge on brain network hubs. Schizophr Bull 43(2):425–435

    PubMed  Google Scholar 

  • Kochunov P, Coyle TR, Rowland LM, Jahanshad N, Thompson PM, Kelly S, Du X, Sampath H, Bruce H, Chiappelli J, Ryan M, Fisseha F, Savransky A, Adhikari B, Chen S, Paciga SA, Whelan CD, Xie Z, Hyde CL, Chen X, Schubert CR, O’Donnell P, Hong LE (2017) Association of White matter with core cognitive deficits in patients with schizophrenia. JAMA Psychiat 74(9):958–966

    Article  Google Scholar 

  • Koshiyama D, Miyakoshi M, Thomas ML, Joshi YB, Molina JL, Tanaka-Koshiyama K, Sprock J, Braff DL, Swerdlow NR, Light GA (2021) Unique contributions of sensory discrimination and gamma synchronization deficits to cognitive, clinical, and psychosocial functional impairments in schizophrenia. Schizophr Res 228:280–287

    Article  PubMed  Google Scholar 

  • Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701

    Article  CAS  PubMed  Google Scholar 

  • Levitt JJ, Nestor PG, Levin L, Pelavin P, Lin P, Kubicki M, McCarley RW, Shenton ME, Rathi Y (2017) Reduced structural connectivity in frontostriatal white matter tracts in the associative loop in schizophrenia. Am J Psychiatry 174(11):1102–1111

    Article  PubMed  Google Scholar 

  • Lezak MD, Howieson DB, Loring DW, Fischer JS (2004) Neuropsychological assessment. Oxford University Press

    Google Scholar 

  • Lv J, Di Biase M, Cash RFH, Cocchi L, Cropley VL, Klauser P, Tian Y, Bayer J, Schmaal L, Cetin-Karayumak S, Rathi Y, Pasternak O, Bousman C, Pantelis C, Calamante F, Zalesky A (2021) Individual deviations from normative models of brain structure in a large cross-sectional schizophrenia cohort. Mol Psychiatry 26(7):3512–3523

    Article  PubMed  Google Scholar 

  • Mesulam MM (1998) From sensation to cognition. Brain 121(6):1013–1052

    Article  PubMed  Google Scholar 

  • Meunier D, Lambiotte R, Bullmore ET (2010) Modular and hierarchically modular organization of brain networks. Front Neurosci 4:200

    Article  PubMed  PubMed Central  Google Scholar 

  • Misic B, Betzel RF, Nematzadeh A, Goni J, Griffa A, Hagmann P, Flammini A, Ahn YY, Sporns O (2015) Cooperative and competitive spreading dynamics on the human connectome. Neuron 86(6):1518–1529

    Article  CAS  PubMed  Google Scholar 

  • Parkes L, Moore TM, Calkins ME, Cieslak M, Roalf DR, Wolf DH, Gur RC, Gur RE, Satterthwaite TD, Bassett DS (2021) Network controllability in transmodal cortex predicts positive psychosis spectrum symptoms. Biol Psychiatry 90(6):409–418

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng X, Zhang R, Yan W, Zhou M, Lu S, Xie S (2020) Reduced white matter integrity associated with cognitive deficits in patients with drug-naive first-episode schizophrenia revealed by diffusion tensor imaging. Am J Transl Res 12(8):4410–4421

    PubMed  PubMed Central  Google Scholar 

  • Polat Nazli I, Ergul C, Aydemir O, Chandhoke S, Ucok A, Gonul AS (2016) Validation of Turkish version of brief negative symptom scale. Int J Psychiatry Clin Pract 20(4):265–271

    Article  PubMed  Google Scholar 

  • Quan M, Lee SH, Kubicki M, Kikinis Z, Rathi Y, Seidman LJ, Mesholam-Gately RI, Goldstein JM, McCarley RW, Shenton ME, Levitt JJ (2013) White matter tract abnormalities between rostral middle frontal gyrus, inferior frontal gyrus and striatum in first-episode schizophrenia. Schizophr Res 145(1–3):1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Reitan RM (1959) Manual for administration of neuropsychological test batteries for adults and children. Indiana University Medical Center, Neuropsychology Laboratory

    Google Scholar 

  • Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069

    Article  PubMed  Google Scholar 

  • Samartzis L, Dima D, Fusar-Poli P, Kyriakopoulos M (2014) White matter alterations in early stages of schizophrenia: a systematic review of diffusion tensor imaging studies. J Neuroimaging 24(2):101–110

    Article  PubMed  Google Scholar 

  • Schmidt M (1996) Rey auditory verbal learning test: A handbook. Western Psychological Services, Los Angeles

    Google Scholar 

  • Seguin C, van den Heuvel MP, Zalesky A (2018) Navigation of brain networks. Proc Natl Acad Sci USA 115(24):6297–6302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seguin C, Razi A, Zalesky A (2019) Inferring neural signalling directionality from undirected structural connectomes. Nat Commun 10(1):4289

    Article  PubMed  PubMed Central  Google Scholar 

  • Seguin C, Tian Y, Zalesky A (2020) Network communication models improve the behavioral and functional predictive utility of the human structural connectome. Netw Neurosci 4(4):980–1006

    Article  PubMed  PubMed Central  Google Scholar 

  • Seitz J, Zuo JX, Lyall AE, Makris N, Kikinis Z, Bouix S, Pasternak O, Fredman E, Duskin J, Goldstein JM, Petryshen TL, Mesholam-Gately RI, Wojcik J, McCarley RW, Seidman LJ, Shenton ME, Koerte IK, Kubicki M (2016) Tractography analysis of 5 white matter bundles and their clinical and cognitive correlates in early-course schizophrenia. Schizophr Bull 42(3):762–771

    Article  PubMed  PubMed Central  Google Scholar 

  • Sha Z, Wager TD, Mechelli A, He Y (2019) Common dysfunction of large-scale neurocognitive networks across psychiatric disorders. Biol Psychiatry 85(5):379–388

    Article  PubMed  Google Scholar 

  • Shon SH, Yoon W, Kim H, Joo SW, Kim Y, Lee J (2018) Deterioration in global organization of structural brain networks in schizophrenia: a diffusion MRI tractography study. Front Psychiatry 9:272

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86(2):353–387

    CAS  PubMed  Google Scholar 

  • Smith RE, Tournier JD, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62(3):1924–1938

    Article  PubMed  Google Scholar 

  • Smith RE, Tournier JD, Calamante F, Connelly A (2013) SIFT: Spherical-deconvolution informed filtering of tractograms. Neuroimage 67:298–312

    Article  PubMed  Google Scholar 

  • Smucny J, Dienel SJ, Lewis DA, Carter CS (2022) Mechanisms underlying dorsolateral prefrontal cortex contributions to cognitive dysfunction in schizophrenia. Neuropsychopharmacology 47(1):292–308

    Article  PubMed  Google Scholar 

  • Strauss E, Sherman EM, Spreen O (2006) A compendium of neuropsychological tests: Administration, norms, and commentary. American Chemical Society

    Google Scholar 

  • Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18(6):643

    Article  Google Scholar 

  • Suarez LE, Markello RD, Betzel RF, Misic B (2020) Linking structure and function in macroscale brain networks. Trends Cogn Sci 24(4):302–315

    Article  PubMed  Google Scholar 

  • Thune H, Recasens M, Uhlhaas PJ (2016) The 40-Hz auditory steady-state response in patients with schizophrenia: a meta-analysis. JAMA Psychiat 73(11):1145–1153

    Article  Google Scholar 

  • 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(4):1459–1472

    Article  PubMed  Google Scholar 

  • Tournier JD, Calamante F, Connelly A (2013) Determination of the appropriate b value and number of gradient directions for high-angular-resolution diffusion-weighted imaging. NMR Biomed 26(12):1775–1786

    Article  PubMed  Google Scholar 

  • Tournier JD, Smith R, Raffelt D, Tabbara R, Dhollander T, Pietsch M, Christiaens D, Jeurissen B, Yeh CH, Connelly A (2019) MRtrix3: A fast, flexible and open software framework for medical image processing and visualisation. Neuroimage 202:116137

    Article  PubMed  Google Scholar 

  • Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29(6):1310–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(1):273–289

    Article  CAS  PubMed  Google Scholar 

  • Uhlhaas PJ, Singer W (2015) Oscillations and neuronal dynamics in schizophrenia: the search for basic symptoms and translational opportunities. Biol Psychiatry 77(12):1001–1009

    Article  PubMed  Google Scholar 

  • van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goni J, Hulshoff Pol HE, Kahn RS (2013) Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiat 70(8):783–792

    Article  Google Scholar 

  • van Wijk BC, Stam CJ, Daffertshofer A (2010) Comparing brain networks of different size and connectivity density using graph theory. PLoS ONE 5(10):e13701

    Article  PubMed  PubMed Central  Google Scholar 

  • Veraart J, Novikov DS, Christiaens D, Ades-Aron B, Sijbers J, Fieremans E (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406

    Article  PubMed  Google Scholar 

  • Wagshal D, Knowlton BJ, Suthana NA, Cohen JR, Poldrack RA, Bookheimer SY, Bilder RM, Asarnow RF (2014) Evidence for corticostriatal dysfunction during cognitive skill learning in adolescent siblings of patients with childhood-onset schizophrenia. Schizophr Bull 40(5):1030–1039

    Article  PubMed  Google Scholar 

  • Wang X, Seguin C, Zalesky A, Wong WW, Chu WC, Tong RK (2019) Synchronization lag in post stroke: relation to motor function and structural connectivity. Netw Neurosci 3(4):1121–1140

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang S, Gong G, Zhong S, Duan J, Yin Z, Chang M, Wei S, Jiang X, Zhou Y, Tang Y, Wang F (2020) Neurobiological commonalities and distinctions among 3 major psychiatric disorders: a graph theoretical analysis of the structural connectome. J Psychiatry Neurosci 45(1):15–22

    Article  PubMed  Google Scholar 

  • Wannan CMJ, Bartholomeusz CF, Pantelis C, Di Biase MA, Syeda WT, Chakravarty MM, Bousman CA, Everall IP, McGorry PD, Zalesky A, Cropley VL (2022) Disruptions in white matter microstructure associated with impaired visual associative memory in schizophrenia-spectrum illness. Eur Arch Psychiatry Clin Neurosci 272(6):971–983

    Article  PubMed  Google Scholar 

  • Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393(6684):440–442

    Article  CAS  PubMed  Google Scholar 

  • Wechsler D (1997) WAIS-III: Administration and scoring manual. Wechsler adult intelligence scale: Psychological corporation. San Antonio

    Google Scholar 

  • Yeo RA, Ryman SG, van den Heuvel MP, de Reus MA, Jung RE, Pommy J, Mayer AR, Ehrlich S, Schulz SC, Morrow EM, Manoach D, Ho BC, Sponheim SR, Calhoun VD (2016) Graph metrics of structural brain networks in individuals with schizophrenia and healthy controls: group differences, relationships with intelligence, and genetics. J Int Neuropsychol Soc 22(2):240–249

    Article  PubMed  Google Scholar 

  • Zalesky A, Fornito A, Bullmore ET (2010) Network-based statistic: identifying differences in brain networks. Neuroimage 53(4):1197–1207

    Article  PubMed  Google Scholar 

  • Zalesky A, Fornito A, Seal ML, Cocchi L, Westin CF, Bullmore ET, Egan GF, Pantelis C (2011) Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry 69(1):80–89

    Article  PubMed  Google Scholar 

  • Zeng B, Ardekani BA, Tang Y, Zhang T, Zhao S, Cui H, Fan X, Zhuo K, Li C, Xu Y, Goff DC, Wang J (2016) Abnormal white matter microstructure in drug-naive first episode schizophrenia patients before and after eight weeks of antipsychotic treatment. Schizophr Res 172(1–3):1–8

    Article  PubMed  Google Scholar 

  • Zhao W, Guo S, Linli Z, Yang AC, Lin CP, Tsai SJ (2020) Functional, anatomical, and morphological networks highlight the role of basal ganglia-thalamus-cortex circuits in schizophrenia. Schizophr Bull 46(2):422–431

    PubMed  Google Scholar 

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Funding

This work was supported by Research Fund of Izmir Katip Celebi University (Project Number: 2018-GAP-TIPF-0003) which had no role in the design of the study, collection and analysis of data and decision to publish. Research Fund of Izmir Katip Celebi University, 2018-GAP-TIPF-0003

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NZ, EO,MK and EB designed the study and wrote the protocol. AB, FG, BY and FG collected data. Authors NZ, AZ, CS and YT undertook the statistical analysis, and author N.Z wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.

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Correspondence to Nabi Zorlu.

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Zorlu, N., Bayrakçı, A., Karakılıç, M. et al. Abnormal Structural Network Communication Reflects Cognitive Deficits in Schizophrenia. Brain Topogr 36, 294–304 (2023). https://doi.org/10.1007/s10548-023-00954-z

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