Disrupted modular architecture of cerebellum in schizophrenia: A graph theoretic analysis

Schizophrenia Bulletin

Volumn 40, Issue 6, 2014, Pages 1216-1226

  Kim, Dae Jin ^a   Kent, Jerillyn S ^a   Bolbecker, Amanda R ^a,b,c   Sporns, Olaf ^a   Cheng, Hu ^a   Newman, Sharlene D ^a   Puce, Aina ^a   O'Donnell, Brian F ^a,b,c   Hetrick, William P ^a,b,c  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c Larue D Carter Memorial Hospital   (United States)

Author keywords

Cerebellum; Diffusion tensor imaging; Modular architecture; Schizophrenia; Structural connectivity; Structural network

Indexed keywords

ADULT; ARTICLE; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; NERVE CELL NETWORK; NEUROLOGIC EXAMINATION; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; SCHIZOPHRENIA; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

ADULT; CEREBELLUM; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; NERVE NET; SCHIZOPHRENIA;

EID: 84986581728     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbu059     Document Type: Article

References (100)

1. Thach WT, Goodkin HP, Keating JG. The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci. 1992;15:403-442.
2. Morton SM, Bastian AJ. Relative contributions of balance and voluntary leg-coordination deficits to cerebellar gait ataxia. J Neurophysiol. 2003;89:1844-1856.
3. Bastian AJ, Martin TA, Keating JG, Thach WT. Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol. 1996;76:492-509.
4. Horak FB, Diener HC. Cerebellar control of postural scaling and central set in stance. J Neurophysiol. 1994;72:479-493.
5. Robinson FR, Fuchs AF. The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci. 2001;24:981-1004.
6. Marr D. A theory of cerebellar cortex. J Physiol. 1969;202:437-470.
7. Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25-61.
8. Glickstein M. The cerebellum and motor learning. Curr Opin Neurobiol. 1992;2:802-806.
9. Imamizu H, Miyauchi S, Tamada T, et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 2000;403:192-195.
10. Schmahmann JD. Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn Sci. 1998;2:362-371.
11. Timmann D, Daum I. Cerebellar contributions to cognitive functions: a progress report after two decades of research. Cerebellum. 2007;6:159-162.
12. Fiez JA, Raichle ME, Balota DA, Tallal P, Petersen SE. PET activation of posterior temporal regions during auditory word presentation and verb generation. Cereb Cortex. 1996;6:1-10.
13. de Zubicaray GI, Williams SC, Wilson SJ, et al. Prefrontal cortex involvement in selective letter generation: a functional magnetic resonance imaging study. Cortex. 1998;34:389-401.
14. Baker SC, Rogers RD, Owen AM, et al. Neural systems engaged by planning: a PET study of the Tower of London task. Neuropsychologia. 1996;34:515-526.
15. Fliessbach K, Trautner P, Quesada CM, Elger CE, Weber B. Cerebellar contributions to episodic memory encoding as revealed by fMRI. Neuroimage. 2007;35:1330-1337.
16. Hayter AL, Langdon DW, Ramnani N. Cerebellar contributions to working memory. Neuroimage. 2007;36:943-954.
17. Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432-8444.
18. Ramnani N. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 2006;7:511-522.
19. Habas C, Kamdar N, Nguyen D, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29:8586-8594.
20. O'Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex. 2010;20:953-965.
21. Lu CF, Wang PS, Lao YL, Wu HM, Soong BW, Wu YT. Medullo-ponto-cerebellar white matter degeneration altered brain network organization and cortical morphology in multiple system atrophy. Brain struct funct. 2013.
22. Filip P, Lungu OV, Bareš M. Dystonia and the cerebellum: a new field of interest in movement disorders? Clin Neurophysiol. 2013;124:1269-1276.
23. Humbert S, Saudou F. The ataxia-ome: connecting disease proteins of the cerebellum. Cell. 2006;125:645-647.
24. Bonthius DJ. Ataxia and the cerebellum. Semin Pediatr Neurol. 2011;18:69-71.
25. Colebatch JG, Findley LJ, Frackowiak RS, Marsden CD, Brooks DJ. Preliminary report: activation of the cerebellum in essential tremor. Lancet. 1990;336:1028-1030.
26. Striano P, Louis ED, Manto M. Autosomal dominant cortical tremor, myoclonus, and epilepsy: is the origin in the cerebellum? Editorial. Cerebellum. 2013;12:145-146.
27. Wu T, Hallett M. The cerebellum in Parkinson's disease. Brain. 2013;136:696-709.
28. Hoppenbrouwers SS, Schutter DJ, Fitzgerald PB, Chen R, Daskalakis ZJ. The role of the cerebellum in the pathophysiology and treatment of neuropsychiatric disorders: a review. Brain Res Rev. 2008;59:185-200.
29. Diamond A. Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. Child Dev. 2000;71:44-56.
30. Andreasen NC, Pierson R. The role of the cerebellum in schizophrenia. Biol Psychiatry. 2008;64:81-88.
31. Picard H, Amado I, Mouchet-Mages S, Olié JP, Krebs MO. The role of the cerebellum in schizophrenia: an update of clinical, cognitive, and functional evidences. Schizophr Bull. 2008;34:155-172.
32. Nopoulos PC, Ceilley JW, Gailis EA, Andreasen NC. An MRI study of cerebellar vermis morphology in patients with schizophrenia: evidence in support of the cognitive dysmetria concept. Biol Psychiatry. 1999;46:703-711.
33. Ichimiya T, Okubo Y, Suhara T, Sudo Y. Reduced volume of the cerebellar vermis in neuroleptic-naive schizophrenia. Biol Psychiatry. 2001;49:20-27.
34. Varnäs K, Okugawa G, Hammarberg A, et al. Cerebellar volumes in men with schizophrenia and alcohol dependence. Psychiatry Clin Neurosci. 2007;61:326-329.
35. Deicken RF, Feiwell R, Schuff N, Soher B. Evidence for altered cerebellar vermis neuronal integrity in schizophrenia. Psychiatry Res. 2001;107:125-134.
36. Ende G, Hubrich P, Walter S, et al. Further evidence for altered cerebellar neuronal integrity in schizophrenia. Am J Psychiatry. 2005;162:790-792.
37. Rüsch N, Spoletini I, Wilke M, et al. Prefrontal-thalamiccerebellar gray matter networks and executive functioning in schizophrenia. Schizophr Res. 2007;93:79-89.
38. Bolbecker AR, Mehta CS, Edwards CR, Steinmetz JE, O'Donnell BF, Hetrick WP. Eye-blink conditioning deficits indicate temporal processing abnormalities in schizophrenia. Schizophr Res. 2009;111:182-191.
39. Forsyth JK, Bolbecker AR, Mehta CS, et al. Cerebellardependent eyeblink conditioning deficits in schizophrenia spectrum disorders. Schizophr Bull. 2012;38:751-759.
40. Carroll CA, O'Donnell BF, Shekhar A, Hetrick WP. Timing dysfunctions in schizophrenia as measured by a repetitive finger tapping task. Brain Cogn. 2009;71:345-353.
41. Marvel CL, Schwartz BL, Rosse RB. A quantitative measure of postural sway deficits in schizophrenia. Schizophr Res. 2004;68:363-372.
42. Magnotta VA, Adix ML, Caprahan A, Lim K, Gollub R, Andreasen NC. Investigating connectivity between the cerebellum and thalamus in schizophrenia using diffusion tensor tractography: a pilot study. Psychiatry Res. 2008;163:193-200.
43. Okugawa G, Nobuhara K, Minami T, et al. Neural disorganization in the superior cerebellar peduncle and cognitive abnormality in patients with schizophrenia: A diffusion tensor imaging study. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30:1408-1412.
44. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186-198.
45. van den Heuvel MP, Mandl RC, Stam CJ, Kahn RS, Hulshoff Pol HE. Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J Neurosci. 2010;30:15915-15926.
46. Zhang Y, Lin L, Lin CP, et al. Abnormal topological organization of structural brain networks in schizophrenia. Schizophr Res. 2012;141:109-118.
47. van den Heuvel MP, Sporns O, Collin G, et al. Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA psychiatry. 2013;70:783-792.
48. Wang L, Metzak PD, Honer WG, Woodward TS. Impaired efficiency of functional networks underlying episodic memory-for-context in schizophrenia. J Neurosci. 2010;30:13171-13179.
49. Lynall ME, Bassett DS, Kerwin R, et al. Functional connectivity and brain networks in schizophrenia. J Neurosci. 2010;30:9477-9487.
50. Alexander-Bloch AF, Gogtay N, Meunier D, et al. Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front Syst Neurosci. 2010;4:147.
51. Park HJ, Friston K. Structural and functional brain networks: from connections to cognition. Science. 2013;342:1238411.
52. Sporns O. Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol. 2013;23:162-171.
53. Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL. Functional-anatomic fractionation of the brain's default network. Neuron. 2010;65:550-562.
54. Ding JR, Liao W, Zhang Z, et al. Topological fractionation of resting-state networks. PLoS One. 2011;6:e26596.
55. Nakanishi S. Synaptic mechanisms of the cerebellar cortical network. Trends Neurosci. 2005;28:93-100.
56. Kanaan RA, Borgwardt S, McGuire PK, et al. Microstructural organization of cerebellar tracts in schizophrenia. Biol Psychiatry. 2009;66:1067-1069.
57. Lu CF, Soong BW, Wu HM, Teng S, Wang PS, Wu YT. Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy. Mov Disord. 2013;28:362-369.
58. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13:261-276.
59. First MB, Spitzer RI, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV Axis I Disorders, Patient Edition (SCID-I/P, Version 2.0). New York: Biometrics Research Department, New York State Psychiatric Institute; 1995.
60. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. NeuroImage. 2006;33:127-138.
61. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage. 2009;46:39-46.
62. Diedrichsen J, Maderwald S, Küper M, et al. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage. 2011;54:1786-1794.
63. Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 1999;45:265-269.
64. Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B. 1994;103:247-254.
65. Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage. 2010;52:1059-1069.
66. Onnela JP, Saramäki J, Kertész J, Kaski K. Intensity and coherence of motifs in weighted complex networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2005;71:065103.
67. Humphries MD, Gurney K. Network 'small-world-ness': a quantitative method for determining canonical network equivalence. PLoS One. 2008;3:e0002051.
68. Newman ME. Finding community structure in networks using the eigenvectors of matrices. Phys Rev E Stat Nonlin Soft Matter Phys. 2006;74:036104.
69. Kim DJ, Skosnik PD, Cheng H, et al. Structural network topology revealed by white matter tractography in cannabis users: a graph theoretical analysis. Brain Connect. 2011;1:473-483.
70. Kim DJ, Bolbecker AR, Howell J, et al. Disturbed resting state EEG synchronization in bipolar disorder: A graph-theoretic analysis. Neuroimage Clin. 2013;2:414-423.
71. van Wijk BC, Stam CJ, Daffertshofer A. Comparing brain networks of different size and connectivity density using graph theory. PLoS One. 2010;5:e13701.
72. Radicchi F, Castellano C, Cecconi F, Loreto V, Parisi D. Defining and identifying communities in networks. Proc Natl Acad Sci U S A. 2004;101:2658-2663.
73. Blondel VD, Guillaume JL, Lambiotte R, Lefebvre E. Fast unfolding of communities in large networks. J Stat Mech Theory Exp. 2008;10:P10008.
74. Sun Y, Danila B, Josic K, Bassler KE. Improved community structure detection using a modified fine-tuning strategy. Europhysics Lett. 2009;86:28004.
75. Newman ME. Modularity and community structure in networks. Proc Natl Acad Sci U S A. 2006;103:8577-8582.
76. Zhang D, Snyder AZ, Fox MD, Sansbury MW, Shimony JS, Raichle ME. Intrinsic functional relations between human cerebral cortex and thalamus. J Neurophysiol. 2008;100:1740-1748.
77. Kim DJ, Park B, Park HJ. Functional connectivity-based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI. Hum Brain Mapp. 2013;34:1371-1385.
78. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B. 1995;57:289-300.
79. Meunier D, Achard S, Morcom A, Bullmore E. Age-related changes in modular organization of human brain functional networks. Neuroimage. 2009;44:715-723.
80. Friston KJ, Frith CD. Schizophrenia: a disconnection syndrome? Clin Neurosci. 1995;3:89-97.
81. Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A. Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci. 2008;28:9239-9248.
82. Marvel CL, Desmond JE. Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev. 2010;20:271-279.
83. Schmahmann JD, Doyon J, McDonald D, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage. 1999;10:233-260.
84. Jansen J, Borodal A. Experimental studies on the intrinsic fibers of the cerebellum. II. The cortico-nuclear projection. J Comp Neurol. 1940;73:267-321.
85. Coffman KA, Dum RP, Strick PL. Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc Natl Acad Sci U S A. 2011;108:16068-16073.
86. Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9:304-313.
87. Kühn S, Romanowski A, Schubert F, Gallinat J. Reduction of cerebellar grey matter in Crus I and II in schizophrenia. Brain Struct Funct. 2012;217:523-529.
88. Blackwood N, Ffytche D, Simmons A, Bentall R, Murray R, Howard R. The cerebellum and decision making under uncertainty. Brain Res Cogn Brain Res. 2004;20:46-53.
89. Shenton ME, Dickey CC, Frumin M, McCarley RW. A review of MRI findings in schizophrenia. Schizophr Res. 2001;49:1-52.
90. Kyriakopoulos M, Vyas NS, Barker GJ, Chitnis XA, Frangou S. A diffusion tensor imaging study of white matter in earlyonset schizophrenia. Biol Psychiatry. 2008;63:519-523.
91. Okugawa G, Nobuhara K, Sugimoto T, Kinoshita T. Diffusion tensor imaging study of the middle cerebellar peduncles in patients with schizophrenia. Cerebellum. 2005;4:123-127.
92. Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci. 2005;6:297-311.
93. Lungu O, Barakat M, Laventure S, et al. The incidence and nature of cerebellar findings in schizophrenia: a quantitative review of fMRI literature. Schizophr Bull. 2013;39:797-806.
94. Takahashi E, Song JW, Folkerth RD, Grant PE, Schmahmann JD. Detection of postmortem human cerebellar cortex and white matter pathways using high angular resolution diffusion tractography: a feasibility study. Neuroimage. 2013;68:105-111.
95. Argyelan M, Carbon M, Niethammer M, et al. Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci. 2009;29:9740-9747.
96. Law N, Bouffet E, Laughlin S, et al. Cerebello-thalamocerebral connections in pediatric brain tumor patients: impact on working memory. Neuroimage. 2011;56:2238-2248.
97. Ramnani N, Behrens TE, Johansen-Berg H, et al. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. Cereb Cortex. 2006;16:811-818.
98. Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89:634-639.
99. Clower DM, Dum RP, Strick PL. Basal ganglia and cerebellar inputs to 'AIP'. Cereb Cortex. 2005;15:913-920.
100. Fang PC, Stepniewska I, Kaas JH. Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti. J Comp Neurol. 2005;490:305-333.