Impaired coupling of local and global functional feedbacks underlies abnormal synchronization and negative symptoms of schizophrenia

BMC Systems Biology

Volumn 7, Issue , 2013, Pages

  Noh, Kyungchul ^a   Shin, Kyung Soon ^b   Shin, Dongkwan ^a   Hwang, Jae Yeon ^b,d   Kim, June Sic ^c   Jang, Joon Hwan ^c   Chung, Chun Kee ^c   Kwon, Jun Soo ^b,c   Cho, Kwang Hyun ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University College of Medicine   (South Korea)

^d Seoul National University Boramae Hospital   (South Korea)

Author keywords

Abnormal synchrony; Coupled feedback; Negative symptom; Network topology; Schizophrenia

Indexed keywords

ARTICLE; BIOLOGICAL MODEL; COMPARATIVE STUDY; COMPUTER SIMULATION; CORTICAL SYNCHRONIZATION; FEEDBACK SYSTEM; HUMAN; MAGNETOENCEPHALOGRAPHY; PATHOPHYSIOLOGY; PHYSIOLOGY; SCHIZOPHRENIA; SOUTH KOREA; TIME;

COMPUTER SIMULATION; CORTICAL SYNCHRONIZATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; MAGNETOENCEPHALOGRAPHY; MODELS, NEUROLOGICAL; REPUBLIC OF KOREA; SCHIZOPHRENIA; TIME FACTORS;

MLCS; MLOWN;

EID: 84875949948     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-7-30     Document Type: Article

References (57)

1. Uhlhaas PJ, Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 2010, 11:100-113. 10.1038/nrn2774, 20087360.
2. Uhlhaas PJ, Haenschel C, Nikolic D, Singer W. The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophrenia Bull 2008, 34:927-943.
3. Bob P, Palus M, Susta M, Glaslova K. EEG phase synchronization in patients with paranoid schizophrenia. Neurosci Lett 2008, 447:73-77. 10.1016/j.neulet.2008.09.055, 18835328.
4. Lee KH, Williams LM, Haig A, Gordon E. "Gamma (40 Hz) phase synchronicity" and symptom dimensions in schizophrenia. Cogn Neuropsychiatry 2003, 8:57-71. 10.1080/713752240, 16571550.
5. Sponheim SR, Clementz BA, Iacono WG, Beiser M. Clinical and biological concomitants of resting state EEG power abnormalities in schizophrenia. Biol Psychiat 2000, 48:1088-1097. 10.1016/S0006-3223(00)00907-0, 11094142.
6. Lee SH, Wynn JK, Green MF, Kim H, Lee KJ, Nam M, Park JK, Chung YC. Quantitative EEG and low resolution electromagnetic tomography (LORETA) imaging of patients with persistent auditory hallucinations. Schizophr Res 2006, 83:111-119. 10.1016/j.schres.2005.11.025, 16524699.
7. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW. Neural synchrony indexes disordered perception and cognition in schizophrenia. P Natl Acad Sci USA 2004, 101:17288-17293.
8. Uhlhaas PJ, Linden DEJ, Singer W, Haenschel C, Lindner M, Maurer K, Rodriguez E. Dysfunctional long-range coordination of neural activity during Gestalt perception in schizophrenia. J Neurosci 2006, 26:8168-8175. 10.1523/JNEUROSCI.2002-06.2006, 16885230.
9. Douglas RJ, Martin KAC. Neuronal circuits of the neocortex. Annu Rev Neurosci 2004, 27:419-451. 10.1146/annurev.neuro.27.070203.144152, 15217339.
10. Douglas RJ, Martin KAC. Recurrent neuronal circuits in the neocortex. Curr Biol 2007, 17:R496-R500. 10.1016/j.cub.2007.04.024, 17610826.
11. Garrido MI, Kilner JM, Kiebel SJ, Friston KJ. Evoked brain responses are generated by feedback loops. P Natl Acad Sci USA 2007, 104:20961-20966.
12. Pollen DA. Feature article on the neural correlates of visual perception. Cereb Cortex 1999, 9:4-19. 10.1093/cercor/9.1.4, 10022491.
13. Vicente R, Gollo LL, Mirasso CR, Fischer I, Pipa G. Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays. P Natl Acad Sci USA 2008, 105:17157-17162.
14. Gollo LL, Mirasso CR, Atienza M, Crespo-Garcia M, Cantero JL. Theta Band Zero-Lag Long-Range Cortical Synchronization via Hippocampal Dynamical Relaying. PLoS One 2011, 6.
15. Kopell N, Ermentrout GB, Whittington MA, Traub RD. Gamma rhythms and beta rhythms have different synchronization properties. P Natl Acad Sci USA 2000, 97:1867-1872.
16. Shin SY, Rath O, Zebisch A, Choo SM, Kolch W, Cho KH. Functional Roles of Multiple Feedback Loops in Extracellular Signal-Regulated Kinase and Wnt Signaling Pathways That Regulate Epithelial-Mesenchymal Transition. Cancer Res 2010, 70:6715-6724. 10.1158/0008-5472.CAN-10-1377, 3012452, 20736375.
17. Shin SY, Yang HW, Kim JR, Do Heo W, Cho KH. A hidden incoherent switch regulates RCAN1 in the calcineurin-NFAT signaling network. J Cell Sci 2011, 124:82-90. 10.1242/jcs.076034, 21172821.
18. Shin SY, Rath O, Choo SM, Fee F, McFerran B, Kolch W, Cho KH. Positive- and negative-feedback regulations coordinate the dynamic behavior of the Ras-Raf-MEK-ERK signal transduction pathway. Journal of Cell Science 2009, 122:425-435. 10.1242/jcs.036319, 19158341.
19. Kim JR, Shin D, Jung SH, Heslop-Harrison P, Cho KH. A design principle underlying the synchronization of oscillations in cellular systems. Journal of Cell Science 2010, 123:537-543. 10.1242/jcs.060061, 20103537.
20. Kim JR, Yoon Y, Cho KH. Coupled feedback loops form dynamic motifs of cellular networks. Biophys J 2008, 94:359-365. 10.1529/biophysj.107.105106, 2157222, 17951298.
21. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional Connectivity in the Motor Cortex of Resting Human Brain Using Echo-Planar Mri. Magnet Reson Med 1995, 34:537-541.
22. Lowe MJ, Mock BJ, Sorenson JA. Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. NeuroImage 1998, 7:119-132. 10.1006/nimg.1997.0315, 9558644.
23. Greicius MD, Krasnow B, Reiss AL, Menon V. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. P Natl Acad Sci USA 2003, 100:253-258.
24. Rogers BP, Morgan VL, Newton AT, Gore JC. Assessing functional connectivity in the human brain by fMRI. Magn Reson Imaging 2007, 25:1347-1357. 10.1016/j.mri.2007.03.007, 2169499, 17499467.
25. Shin KS, Kim JS, Kim SN, Koh Y, Jang JH, An SK, O'Donnell BF, Chung CK, Kwon JS. Aberrant Auditory Processing in Schizophrenia and in Subjects at Ultra-High-Risk for Psychosis. Schizophr Bull 2011,
26. Kay SR, Fiszbein A, Opler LA. The Positive and Negative Syndrome Scale (Panss) for Schizophrenia. Schizophrenia Bull 1987, 13:261-276.
27. Taulu S, Simola J. Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Phys Med Biol 2006, 51:1759-1768. 10.1088/0031-9155/51/7/008, 16552102.
28. Sinkkonen J, Tiitinen H, Naatanen R. Gabor Filters - an Informative Way for Analyzing Event-Related Brain Activity. J Neurosci Meth 1995, 56:99-104.
29. Combes JM, Grossmann A, Tchamitchian P. Wavelets: time-frequency methods and phase space: proceedings of the international conference, Marseille, France, December 14-18, 1987. Berlin 1989, New York: Springer.
30. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004, 134:9-21. 10.1016/j.jneumeth.2003.10.009, 15102499.
31. Pereda E, Quiroga RQ, Bhattacharya J. Nonlinear multivariate analysis of neurophysiological signals. Prog Neurobiol 2005, 77:1-37. 10.1016/j.pneurobio.2005.10.003, 16289760.
32. Dong CY, Lim J, Nam Y, Cho KH. Systematic analysis of synchronized oscillatory neuronal networks reveals an enrichment for coupled direct and indirect feedback motifs. Bioinformatics 2009, 25:1680-1685. 10.1093/bioinformatics/btp271, 19389738.
33. Dong CY, Yoon TW, Bates DG, Cho KH. Identification of feedback loops embedded in cellular circuits by investigating non-causal impulse response components. J Math Biol 2010, 60:285-312. 10.1007/s00285-009-0263-x, 19333603.
34. Wilson HR, Cowan JD. Excitatory and Inhibitory Interactions in Localized Populations of Model Neurons. Biophys J 1972, 12:1. 1484078, 4332108.
35. Miller R. Distribution and Properties of Commissural and Other Neurons in Cat Sensorimotor Cortex. J Comp Neurol 1975, 164:361-373. 10.1002/cne.901640307, 1184789.
36. Swadlow HA. Efferent Neurons and Suspected Interneurons in S-1 Forelimb Representation of the Awake Rabbit - Receptive-Fields and Axonal Properties. J Neurophysiol 1990, 63:1477-1498.
37. Hauptmann C, Popovych O, Tass PA. Delayed feedback control of synchronization in locally coupled neuronal networks. Neurocomputing 2005, 65:759-767.
38. Ferraina S, Pare M, Wurtz RH. Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. J Neurophysiol 2002, 87:845-858.
39. Gariano RF, Groves PM. Burst Firing Induced in Midbrain Dopamine Neurons by Stimulation of the Medial Prefrontal and Anterior Cingulate Cortices. Brain Res 1988, 462:194-198. 10.1016/0006-8993(88)90606-3, 3179734.
40. Simmons PA, Pearlman AL. Receptive-Field Properties of Transcallosal Visual Cortical-Neurons in the Normal and Reeler Mouse. J Neurophysiol 1983, 50:838-848.
41. Foussias G, Remington G. Negative symptoms in schizophrenia: avolition and Occam's razor. Schizophr Bull 2010, 36:359-369. 10.1093/schbul/sbn094, 2833114, 18644851.
42. Dong CY, Cho KH. An optimally evolved connective ratio of neural networks that maximizes the occurrence of synchronized bursting behavior. BMC Syst Biol 2012, 6.
43. Hillebrand A, Barnes GR. A quantitative assessment of the sensitivity of whole-head MEG to activity in the adult human cortex. NeuroImage 2002, 16:638-650. 10.1006/nimg.2002.1102, 12169249.
44. Alonso JF, Poza J, Mananas MA, Romero S, Fernandez A, Hornero R. MEG Connectivity Analysis in Patients with Alzheimer's Disease Using Cross Mutual Information and Spectral Coherence. Ann Biomed Eng 2011, 39:524-536. 10.1007/s10439-010-0155-7, 20824340.
45. Gaetz M, Weinberg H, Rzempoluck E, Jantzen KJ. Neural network classifications and correlation analysis of EEG and MEG activity accompanying spontaneous reversals of the Necker cube. Cognitive Brain Res 1998, 6:335-346.
46. Schmithorst VJ, Holland SK. Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis. NeuroImage 2007, 35:406-419. 10.1016/j.neuroimage.2006.11.046, 2100392, 17223578.
47. Owen JP, Wipf DP, Attias HT, Sekihara K, Nagarajan SS. Accurate reconstruction of brain activity and functional connectivity from noisy MEG data. Conf Proc IEEE Eng Med Biol Soc 2009, 2009:65-68. 2944402, 19965115.
48. Dhamala M, Rangarajan G, Ding M. Analyzing information flow in brain networks with nonparametric Granger causality. NeuroImage 2008, 41:354-362. 10.1016/j.neuroimage.2008.02.020, 2685256, 18394927.
49. Kissler J, Muller MM, Fehr T, Rockstroh B, Elbert T. MEG gamma band activity in schizophrenia patients smd healthy subjects in a mental arithmetic task and at rest. Clin Neurophysiol 2000, 111:2079-2087. 10.1016/S1388-2457(00)00425-9, 11068245.
50. Rutter L, Carver FW, Holroyd T, Nadar SR, Mitchell-Francis J, Apud J, Weinberger DR, Coppola R. Magnetoencephalographic Gamma Power Reduction in Patients with Schizophrenia During Resting Condition. Hum Brain Mapp 2009, 30:3254-3264. 10.1002/hbm.20746, 2748144, 19288463.
51. van Wijk BCM, Daffertshofer A, Roach N, Praamstra P. A Role of Beta Oscillatory Synchrony in Biasing Response Competition?. Cereb Cortex 2009, 19:1294-1302. 10.1093/cercor/bhn174, 18836098.
52. Northoff G, Qin PM. How can the brain's resting state activity generate hallucinations? A 'resting state hypothesis' of auditory verbal hallucinations. Schizophr Res 2011, 127:202-214. 10.1016/j.schres.2010.11.009, 21146961.
53. Stephan KE, Friston KJ, Frith CD. Dysconnection in Schizophrenia: From Abnormal Synaptic Plasticity to Failures of Self-monitoring. Schizophrenia Bull 2009, 35:509-527.
54. Bullmore E, Barnes A, Bassett DS, Fornito A, Kitzbichler M, Meunier D, Suckling J. Generic aspects of complexity in brain imaging data and other biological systems. NeuroImage 2009, 47:1125-1134. 10.1016/j.neuroimage.2009.05.032, 19460447.
55. Bassett DS, Gazzaniga MS. Understanding complexity in the human brain. Trends Cogn Sci 2011, 15:200-209. 10.1016/j.tics.2011.03.006, 3170818, 21497128.
56. Albert R, Barabasi AL. Statistical mechanics of complex networks. Rev Mod Phys 2002, 74:47-97.
57. Jhung K, Cho S-H, Jang J-H, Park JY, Shin D, Kim KR, Lee E, Cho K-H, An SK. Small-world networks in individuals at ultra-high risk for psychosis and first-episode schizophrenia during a working memory task. Neurosci Lett 2013, 535:35-39.