Alterations of functional and structural networks in schizophrenia patients with auditory verbal hallucinations

Frontiers in Human Neuroscience

Volumn 10, Issue MAR2016, 2016, Pages

  Zhu, Jiajia ^a   Wang, Chunli ^b   Liu, Feng ^a   Qin, Wen ^a   Li, Jie ^b   Zhuo, Chuanjun ^a,b,c  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b SHANDONG MENTAL HEALTH CENTER   (China)

^c PR China   (China)

Author keywords

Auditoryverbal hallucinations; Diffusion tensor imaging; Functional magnetic resonance imaging; Schizophrenia; Small world network

Indexed keywords

ADULT; ARTICLE; AUDITORY HALLUCINATION; AUDITORY VERBAL HALLUCINATION; CHARACTERISTIC PATH LENGTH; CLUSTERING COEFFICIENT; CONNECTOME; CONTROLLED STUDY; DATA PROCESSING; DIFFUSION TENSOR IMAGING; FEMALE; FUNCTIONAL BRAIN NETWORK; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBAL EFFICIENCY; GRAPH THEORY; HUMAN; LOCAL EFFICIENCY; MAJOR CLINICAL STUDY; MALE; MATHEMATICAL ANALYSIS; NERVE CELL NETWORK; NERVOUS SYSTEM PARAMETERS; REST; SCHIZOPHRENIA; SMALL WORLD TOPOLOGY; STRUCTURAL BRAIN NETWORK;

EID: 84961762813     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2016.00114     Document Type: Article

References (60)

1. Achard, S. and Bullmore, E. (2007). Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 3:e17. doi: 10.1371/journal.pcbi.0030017
2. Achard, S. Salvador, R. Whitcher, B. Suckling, J. and Bullmore, E. (2006). A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 26, 63-72. doi: 10.1523/JNEUR0SCI.3874-05.2006
3. Allen, P. Laroi, F. Mcguire, P. K. and Aleman, A. (2008). The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci. Biobehav. Rev. 32, 175-191. doi: 10.1016/j.neubiorev.2007.07.012
4. Allen, P. Modinos, G. Hubl, D. Shields, G. Cachia, A. Jardri, R. et al. (2012). Neuroimaging auditory hallucinations in schizophrenia: from neuroanatomy to neurochemistry and beyond. Schizophr. Bull. 38, 695-703. doi: 10.1093/schbul/sbs066
5. Andreasen, N. C. and Flaum, M. (1991). Schizophrenia: the characteristic symptoms. Schizophr. Bull. 17, 27-49. doi: 10.1093/schbul/17.1.27
6. Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage 38, 95-113. doi: 10.1016/j.neuroimage.2007.07.007
7. Baggio, H. C. Segura, B. Junque, C. De Reus, M. A. Sala-Llonch, R. and Van Den Heuvel, M. P. (2015). Rich club organization and cognitive performance in healthy older participants. J. Cogn. Neurosci. 27, 1801-1810. doi: 10.1162/jocn_a_00821
8. Bai, F. Shu, N. Yuan, Y. Shi, Y. Yu, H. Wu, D. et al. (2012). Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J. Neurosci. 32,4307-4318. doi: 10.1523/JNEUR0SCI.5061-11.2012
9. Bassett, D. S. and Bullmore, E. (2006). Small-world brain networks. Neuroscientist 12, 512-523. doi: 10.1177/1073858406293182
10. Bassett, D. S. Meyer-Lindenberg, A. Achard, S. Duke, T. and Bullmore, E. (2006). Adaptive reconfiguration of fractal small-world human brain functional networks. Proc. Natl. Acad. Sci. U.S.A. 103, 19518-19523. doi: 10.1073/pnas.0606005103
11. Bassett, D. S. Wymbs, N. F. Porter, M. A. Mucha, P. J. Carlson, J. M. and Grafton, S. T. (2011). Dynamic reconfiguration of human brain networks during learning. Proc. Natl. Acad. Sci. U.S.A. 108, 7641-7646. doi: 10.1073/pnas.1018985108
12. Bullmore, E. and Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186-198. doi: 10.1038/nrn2575
13. Bullmore, E. T. and Bassett, D. S. (2011). Brain graphs: graphical models of the human brain connectome. Annu. Rev. Clin. Psychol. 7, 113-140. doi: 10.1146/annurev-clinpsy-040510-143934
14. David, A. S. (2004). The cognitive neuropsychiatry of auditory verbal hallucinations: an overview. Cogn. Neuropsychiatry 9, 107-123. doi: 10.1080/13546800344000183
15. Fitzsimmons, J. Kubicki, M. and Shenton, M. E. (2013). Review of functional and anatomical brain connectivity findings in schizophrenia. Curr. Opin. Psychiatry 26, 172-187. doi: 10.1097/YC0.0b013e32835d9e6a
16. Fornito, A. and Bullmore, E. T. (2015). Reconciling abnormalities ofbrainnetwork structure and function in schizophrenia. Curr. Opin. Neurobiol. 30, 44-50. doi: 10.1016/j.conb.2014.08.006
17. Fornito, A. Zalesky, A. and Bullmore, E. T. (2010). Network scaling effects in graph analytic studies of human resting-state FMRI data. Front. Syst. Neurosci. 4:22. doi: 10.3389/fnsys.2010.00022
18. Fornito, A. Zalesky, A. Pantelis, C. and Bullmore, E. T. (2012). Schizophrenia, neuroimaging and connectomics. Neuroimage 62, 2296-2314. doi: 10.1016/j.neuroimage.2011.12.090
19. Fox, M. D. Zhang, D. Snyder, A. Z. and Raichle, M. E. (2009). The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 101, 3270-3283. doi: 10.1152/jn.90777.2008
20. Gaite, L. Vazquez-Barquero, J. L. Borra, C. Ballesteros, J. Schene, A. Welcher, B. et al. (2002). Quality of life in patients with schizophrenia in five European countries: the EPSIL0N study. Acta Psychiatr. Scand. 105, 283-292. doi: 10.1034/j.1600-0447.2002.1169.x
21. Geoffroy, P. A. Houenou, J. Duhamel, A. Amad, A. De Weijer, A. D. Curcic- Blake, B. et al. (2014). The Arcuate Fasciculus in auditory-verbal hallucinations: a meta-analysis of diffusion-tensor-imaging studies. Schizophr. Res. 159, 234-­237. doi: 10.1016/j.schres.2014.07.014
22. Gong, G. He, Y. Concha, L. Lebel, C. Gross, D. W. Evans, A. C. et al. (2009). Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb. Cortex 19, 524-536. doi: 10.1093/cercor/bhn102
23. Hagmann, P. Kurant, M. Gigandet, X. Thiran, P. Wedeen, V. J. Meuli, R. et al. (2007). Mapping human whole-brain structural networks with diffusion MRI. PLoS ONE 2:e597. doi: 10.1371/journal.pone.0000597
24. Hayasaka, S. and Laurienti, P. J. (2010). Comparison of characteristics between region-and voxel-based network analyses in resting-state fMRI data. Neuroimage 50, 499-508. doi: 10.1016/j.neuroimage.2009.12.051
25. He, Y. Chen, Z. J. and Evans, A. C. (2007). Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb. Cortex 17, 2407-2419. doi: 10.1093/cercor/bhl149
26. He, Y. and Evans, A. (2010). Graph theoretical modeling of brain connectivity. Curr. Opin. Neurol. 23, 341-350. doi: 10.1097/WC0.0b013e32833aa567
27. Hoffman, R. E. and Hampson, M. (2011). Functional connectivity studies of patients with auditory verbal hallucinations. Front. Hum. Neurosci. 6:6. doi: 10.3389/fnhum.2012.00006
28. Hoffman, R. E. Hawkins, K. A. Gueorguieva, R. Boutros, N. N. Rachid, F. Carroll, K. et al. (2003). Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch. Gen. Psychiatry 60, 49-56. doi: 10.1001/archpsyc.60.1.49
29. Jardri, R. Pouchet, A. Pins, D. and Thomas, P. (2011). Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am. J. Psychiatry 168, 73-81. doi: 10.1176/appi.ajp.2010.09101522
30. Kay, S. R. Fiszbein, A. and Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13, 261-276. doi: 10.1093/schbul/13.2.261
31. Kompus, K. Westerhausen, R. and Hugdahl, K. (2011). The “paradoxical” engagement of the primary auditory cortex in patients with auditory verbal hallucinations: a meta-analysis of functional neuroimaging studies. Neuropsychologia 49, 3361-3369. doi: 10.1016/j.neuropsychologia.2011.08.010
32. Kuhn, S. and Gallinat, J. (2012). Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. Schizophr. Bull. 38, 779-786. doi: 10.1093/schbul/sbq152
33. Latora, V. and Marchiori, M. (2001). Efficient behavior of small-world networks. Phys. Rev. Lett. 87:198701. doi: 10.1103/PhysRevLett.87.198701
34. Li, Y. Liu, Y. Li, J. Qin, W. Li, K. Yu, C. et al. (2009). Brain anatomical network and intelligence. PLoS Comput. Biol. 5:e1000395. doi: 10.1371/journal.pcbi.1000395
35. Liu, Y. Liang, M. Zhou, Y. He, Y. Hao, Y. Song, M. et al. (2008). Disrupted small-world networks in schizophrenia. Brain 131, 945-961. doi: 10.1093/brain/awn018
36. Lo, C. Y. Wang, P. N. Chou, K. H. Wang, J. He, Y. and Lin, C. P. (2010). Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer's disease. J. Neurosci. 30, 16876­-16885. doi: 10.1523/JNEUR0SCI.4136-10.2010
37. Maslov, S. and Sneppen, K. (2002). Specificity and stability in topology of protein networks. Science 296, 910-913. doi: 10.1126/science.1065103
38. Micheloyannis, S. (2012). Graph-based network analysis in schizophrenia. World J. Psychiatry 2, 1-12. doi: 10.5498/wjp.v2.i1.1
39. Micheloyannis, S. Pachou, E. Stam, C. J. Breakspear, M. Bitsios, P. Vourkas, M. et al. (2006). Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr. Res. 87, 60-66. doi: 10.1016/j.schres.2006.06.028
40. Modinos, G. Costafreda, S. G. Van Tol, M. J. Mcguire, P. K. Aleman, A. and Allen, P. (2013). Neuroanatomy of auditory verbal hallucinations in schizophrenia: a quantitative meta-analysis of voxel-based morphometry studies. Cortex 49, 1046-1055. doi: 10.1016/j.cortex.2012.01.009
41. Mori, S. Crain, B. J. Chacko, V. P. and Van Zijl, P. C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45, 265-269. doi: 10.1002/1531-8249
42. Murphy, K. Birn, R. M. Handwerker, D. A. Jones, T. B. and Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44, 893-905. doi: 10.1016/j.neuroimage.2008.09.036
43. Palaniyappan, L. Balain, V. Radua, J. and Liddle, P. F. (2012). Structural correlates of auditory hallucinations in schizophrenia: a meta-analysis. Schizophr. Res. 137, 169-173. doi: 10.1016/j.schres.2012.01.038
44. Power, J. D. Barnes, K. A. Snyder, A. Z. Schlaggar, B. L. and Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154. doi: 10.1016/j.neuroimage.2011.10.018
45. Rubinov, M. and Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52, 1059-1069. doi: 10.1016/j.neuroimage.2009.10.003
46. Salvador, R. Suckling, J. Coleman, M. R. Pickard, J. D. Menon, D. and Bullmore, E. (2005). Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb. Cortex 15, 1332-1342. doi: 10.1093/cercor/bhi016
47. Shergill, S. S. Murray, R. M. and Mcguire, P. K. (1998). Auditory hallucinations: a review of psychological treatments. Schizophr. Res. 32, 137-150. doi: 10.1016/S0920-9964(98)00052-8
48. Shu, N. Liu, Y. Li, J. Li, Y. Yu, C. and Jiang, T. (2009). Altered anatomical network in early blindness revealed by diffusion tensor tractography. PLoS ONE 4:e7228. doi: 10.1371/journal.pone.0007228
49. Tzourio-Mazoyer, N. Landeau, B. Papathanassiou, D. Crivello, F. Etard, O. Delcroix, N. et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289. doi: 10.1006/nimg.2001.0978
50. van den Heuvel, M. P. and Fornito, A. (2014). Brain networks in schizophrenia. Neuropsychol. Rev. 24, 32-48. doi: 10.1007/s11065-014-9248-7
51. van Swam, C. Federspiel, A. Hubl, D. Wiest, R. Boesch, C. Vermathen, P. et al. (2012). Possible dysregulation of cortical plasticity in auditory verbal hallucinations-A cortical thickness study in schizophrenia. J. Psychiatr. Res. 46, 1015-1023. doi: 10.1016/j.jpsychires.2012.03.016
52. Wang, J. Wang, L. Zang, Y. Yang, H. Tang, H. Gong, Q. et al. (2009). Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum. Brain Mapp. 30, 1511-1523. doi: 10.1002/hbm.20623
53. Wang, J. Wang, X. He, Y. Yu, X. and Wang, H. (2015a). Apolipoprotein E epsilon4 modulates functional brain connectome in Alzheimer's disease. Hum. Brain Mapp. 36, 1828-1846. doi: 10.1002/hbm.22740
54. Wang, J. Wang, X. Xia, M. Liao, X. Evans, A. and He, Y. (2015b). GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front. Hum. Neurosci. 9:386. doi: 10.3389/fnhum.2015.00386
55. Wang, J. Zuo, X. Dai, Z. Xia, M. Zhao, Z. Zhao, X. et al. (2013). Disrupted functional brain connectome in individuals at risk for Alzheimer's disease. Biol. Psychiatry 73,472-481. doi: 10.1016/j.biopsych.2012.03.026
56. Watts, D. J. and Strogatz, S. H. (1998). Collective dynamics of 'small-world' networks. Nature 393, 440-442. doi: 10.1038/30918
57. Wigand, M. Kubicki, M. Clemm Von Hohenberg, C. Leicht, G. Karch, S. Eckbo, R. et al. (2015). Auditory verbal hallucinations and the interhemispheric auditory pathway in chronic schizophrenia. World J. Biol. Psychiatry 16, 31-44. doi: 10.3109/15622975.2014.948063
58. Zalesky, A. Fornito, A. Harding, I. H. Cocchi, L. Yucel, M. Pantelis, C. et al. (2010). Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50, 970-983. doi: 10.1016/j.neuroimage.2009.12.027
59. Zalesky, A. Fornito, A. Seal, M. L. Cocchi, L. Westin, C. F. Bullmore, E. T. et al. (2011). Disrupted axonal fiber connectivity in schizophrenia. Biol. Psychiatry 69, 80-89. doi: 10.1016/j.biopsych.2010.08.022
60. Zhao, T. Cao, M. Niu, H. Zuo, X. N. Evans, A. He, Y. et al. (2015). Age- related changes in the topological organization of the white matter structural connectome across the human lifespan. Hum. Brain Mapp. 36, 3777-3792. doi: 10.1002/hbm.22877