Aberrant cerebellar connectivity in motor and association networks in schizophrenia

Frontiers in Human Neuroscience

Volumn 9, Issue MAR, 2015, Pages

  Shinn, Ann K ^a,b   Baker, Justin T ^a,b   Lewandowski, Kathryn E ^a,b   Öngür, Dost ^a,b   Cohen, Bruce M ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Association cortex; Cerebellum; Functional connectivity; Motor; Networks; Schizophrenia

Indexed keywords

NEUROLEPTIC AGENT;

17 NETWORK CEREBRAL CORTICAL PARCELLATION SYSTEM; ADULT; AGED; ARTICLE; BRAIN CORTEX; CEREBELLUM; CEREBELLUM DISEASE; CEREBRO CEREBELLAR FUNCTIONAL CONNECTIVITY; CLINICAL ARTICLE; CONNECTOME; CONTROL NETWORK; CONTROLLED STUDY; DEFAULT MODE NETWORK; FEMALE; FUNCTIONAL NEUROIMAGING; HUMAN; IMAGE ANALYSIS; MALE; NERVE CELL NETWORK; PATHOPHYSIOLOGY; SALIENCE NETWORK; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; SCHIZOPHRENIFORM DISORDER; SOMATOMOTOR NETWORK; VENTRAL ATTENTION NETWORK;

EID: 84933671105     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2015.00134     Document Type: Article

References (89)

1. APA. (2013) Diagnostic and Statistical Manual of Mental Disorders, 5th Edn. Washington, DC: American Psychiatric Press.
2. Adrian, E. D. (1943). Afferent areas in the cerebellum connected with the limbs. Brain 66, 289-315. doi: 10.1093/brain/66.4.289
3. Alexander-Bloch, A. F., Gogtay, N., Meunier, D., Birn, R., Clasen, L., Lalonde, F., et al. (2010). Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front. Syst. Neurosci. 4:147. doi: 10.3389/fnsys.2010.00147
4. Andreasen, N. (1983). Scale for the Assessment of Negative Symptoms (SANS), Iowa: University of Iowa.
5. Andreasen, N. C. (1984). The Scale for the Assessment of Positive Symptoms (SAPS), Iowa: University of Iowa.
6. Andreasen, N. C. (1999). A unitary model of schizophrenia. Bleuler's "Fragmented Phrene" as schizencephaly. Arch. Gen. Psychiatry 56, 781-787. doi: 10.1001/archpsyc.56.9.781
7. Andreasen, N. C., Nopoulos, P., O'leary, D. S., Miller, D. D., Wassink, T., and Flaum, M. (1999). Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol. Psychiatry 46, 908-920. doi: 10.1016/S0006-3223(99)00152-3
8. Andreasen, N. C., O'leary, D. S., Cizadlo, T., Arndt, S., Rezai, K., Ponto, L. L., et al. (1996). Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry. Proc. Natl. Acad. Sci. U.S.A. 93, 9985-9990. doi: 10.1073/pnas.93.18.9985
9. Andreasen, N. C., O'leary, D. S., Cizadlo, T., Arndt, S., Rezai, K., Watkins, G. L., et al. (1995). Remembering the past: two facets of episodic memory explored with positron emission tomography. Am. J. Psychiatry 152, 1576-1585. doi: 10.1176/ajp.152.11.1576
10. Andreasen, N. C., Paradiso, S., and O'leary, D. S. (1998). "Cognitive dysmetria" as an integrative theory of schizophrenia: a dysfunction in cortical-subcortical-cerebellar circuitry? Schizophr. Bull 24, 203-218.
11. Anticevic, A., Cole, M. W., Repovs, G., Murray, J. D., Brumbaugh, M. S., Winkler, A. M., et al. (2014). Characterizing thalamo-cortical disturbances in schizophrenia and bipolar illness. Cereb. Cortex. 24, 3116-3130. doi: 10.1093/cercor/bht165
12. Baker, J. T., Holmes, A. J., Masters, G. A., Yeo, B. T., Krienen, F., Buckner, R. L., et al. (2014). Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. JAMA Psychiatry 71, 109-118. doi: 10.1001/jamapsychiatry.2013.3469
13. Bluhm, R. L., Miller, J., Lanius, R. A., Osuch, E. A., Boksman, K., Neufeld, R. W., et al. (2007). Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. Schizophr. Bull. 33, 1004-1012. doi: 10.1093/schbul/sbm052
14. Bombin, I., Arango, C., and Buchanan, R. W. (2005). Significance and meaning of neurological signs in schizophrenia: two decades later. Schizophr. Bull. 31, 962-977. doi: 10.1093/schbul/sbi028
15. Bostan, A. C., Dum, R. P., and Strick, P. L. (2013). Cerebellar networks with the cerebral cortex and basal ganglia.Trends Cogn. Sci. 17, 241-254. doi: 10.1016/j.tics.2013.03.003
16. Buckley, P. F., Miller, B. J., Lehrer, D. S., and Castle, D. J. (2009). Psychiatric comorbidities and schizophrenia.Schizophr. Bull. 35, 383-402. doi: 10.1093/schbul/sbn135
17. Buckner, R. L. (2013). The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging.Neuron 80, 807-815. doi: 10.1016/j.neuron.2013.10.044
18. Buckner, R. L., Andrews-hanna, J. R., and Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124, 1-38. doi: 10.1196/annals.1440.011
19. Buckner, R. L., and Krienen, F. M. (2013). The evolution of distributed association networks in the human brain.Trends Cogn. Sci. 17, 648-665. doi: 10.1016/j.tics.2013.09.017
20. Buckner, R. L., Krienen, F. M., Castellanos, A., Diaz, J. C., and Yeo, B. T. (2011). The organization of the human cerebellum estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 2322-2345. doi: 10.1152/jn.00339.2011
21. Chen, Y. L., Tu, P. C., Lee, Y. C., Chen, Y. S., Li, C. T., and Su, T. P. (2013). Resting-state fMRI mapping of cerebellar functional dysconnections involving multiple large-scale networks in patients with schizophrenia. Schizophr. Res. 149, 26-34. doi: 10.1016/j.schres.2013.05.029
22. Christensen, A., Giese, M. A., Sultan, F., Mueller, O. M., Goericke, S. L., Ilg, W., et al. (2014). An intact action-perception coupling depends on the integrity of the cerebellum. J. Neurosci. 34, 6707-6716. doi: 10.1523/JNEUROSCI.3276-13.2014
23. Collin, G., Hulshoff Pol, H. E., Haijma, S. V., Cahn, W., Kahn, R. S., and van den Heuvel, M. P. (2011). Impaired cerebellar functional connectivity in schizophrenia patients and their healthy siblings. Front. Psychiatry 2:73. doi: 10.3389/fpsyt.2011.00073
24. Conley, R. R., Ascher-Svanum, H., Zhu, B., Faries, D. E., and Kinon, B. J. (2007). The burden of depressive symptoms in the long-term treatment of patients with schizophrenia. Schizophr. Res. 90, 186-197. doi: 10.1016/j.schres.2006.09.027
25. D'angelo, E., and Casali, S. (2013). Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition. Front. Neural Circuits 6:116. doi: 10.3389/fncir.2012.00116
26. Daskalakis, Z. J., Christensen, B. K., Fitzgerald, P. B., Fountain, S. I., and Chen, R. (2005). Reduced cerebellar inhibition in schizophrenia: a preliminary study. Am. J. Psychiatry 162, 1203-1205. doi: 10.1176/appi.ajp.162.6.1203
27. Daskalakis, Z. J., Paradiso, G. O., Christensen, B. K., Fitzgerald, P. B., Gunraj, C., and Chen, R. (2004). Exploring the connectivity between the cerebellum and motor cortex in humans. J. Physiol. 557, 689-700. doi: 10.1113/jphysiol.2003.059808
28. David, A. S. (1994). Dysmodularity: a neurocognitive model for schizophrenia. Schizophr. Bull. 20, 249-255. doi: 10.1093/schbul/20.2.249
29. de Arruda, G. F., Fontoura Costa, L., Schubert, D., and Rodrigues, F. A. (2014). Structure and dynamics of functional networks in child-onset schizophrenia. Clin. Neurophysiol. 125, 1589-1595. doi: 10.1016/j.clinph.2013.11.036
30. Demirtas-Tatlidede, A., Freitas, C., Cromer, J. R., Safar, L., Ongur, D., Stone, W. S., et al. (2010). Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr. Res. 124, 91-100. doi: 10.1016/j.schres.2010.08.015
31. Dobromyslin, V. I., Salat, D. H., Fortier, C. B., Leritz, E. C., Beckmann, C. F., Milberg, W. P., et al. (2012). Distinct functional networks within the cerebellum and their relation to cortical systems assessed with independent component analysis. Neuroimage 60, 2073-2085. doi: 10.1016/j.neuroimage.2012.01.139
32. First, M. B., Spitzer, R. L., Gibbon, M., and Williams, J. B. W. (1995). Structured Clinical Interview for DSM-IV Axis I Disorders, New York, NY: New York State Psychiatric Institute, Biometrics Research.
33. Fodor, J. A. (1983). The Modularity of Mind, Cambridge, MA: MIT Press.
34. Gapenne, O. (2014). The co-constitution of the self and the world: action and proprioceptive coupling. Front. Psychol. 5:594. doi: 10.3389/fpsyg.2014.00594
35. Gold, J. M., and Harvey, P. D. (1993). Cognitive deficits in schizophrenia. Psychiatr. Clin. North Am. 16, 295-312.
36. Gupta, S., Andreasen, N. C., Arndt, S., Flaum, M., Schultz, S. K., Hubbard, W. C., et al. (1995). Neurological soft signs in neuroleptic-naive and neuroleptic-treated schizophrenic patients and in normal comparison subjects. Am. J. Psychiatry 152, 191-196. doi: 10.1176/ajp.152.2.191
37. Gusnard, D. A., Akbudak, E., Shulman, G. L., and Raichle, M. E. (2001). Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 4259-4264. doi: 10.1073/pnas.071043098
38. Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C. F., Menon, V., et al. (2009). Distinct cerebellar contributions to intrinsic connectivity networks. J. Neurosci. 29, 8586-8594. doi: 10.1523/JNEUROSCI.1868-09.2009
39. Haddock, G., McCarron, J., Tarrier, N., and Faragher, E. B. (1999). Scales to measure dimensions of hallucinations and delusions: the psychotic symptom rating scales (PSYRATS). Psychol. Med. 29, 879-889. doi: 10.1017/S0033291799008661
40. Halko, M. A., Farzan, F., Eldaief, M. C., Schmahmann, J. D., and Pascual-Leone, A. (2014). Intermittent theta-burst stimulation of the lateral cerebellum increases functional connectivity of the default network. J. Neurosci. 34, 12049-12056. doi: 10.1523/JNEUROSCI.1776-14.2014
41. Heatherton, T. F., Kozlowski, L. T., Frecker, R. C., and Fagerstrom, K. O. (1991). The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance questionnaire. Br. J. Addict. 86, 1119-1127. doi: 10.1111/j.1360-0443.1991.tb01879.x
42. Heinrichs, D. W., and Buchanan, R. W. (1988). Significance and meaning of neurological signs in schizophrenia. Am. J. Psychiatry 145, 11-18. doi: 10.1176/ajp.145.1.11
43. Hoppenbrouwers, S. S., Schutter, D. J., Fitzgerald, P. B., Chen, R., and Daskalakis, Z. J. (2008). The role of the cerebellum in the pathophysiology and treatment of neuropsychiatric disorders: a review. Brain Res. Rev. 59, 185-200. doi: 10.1016/j.brainresrev.2008.07.005
44. Jenkinson, M., Bannister, P., Brady, M., and Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825-841. doi: 10.1006/nimg.2002.1132
45. Kelly, R. M., and Strick, P. L. (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 23, 8432-8444.
46. Keshavan, M., Montrose, D. M., Rajarethinam, R., Diwadkar, V., Prasad, K., and Sweeney, J. A. (2008). Psychopathology among offspring of parents with schizophrenia: relationship to premorbid impairments.Schizophr. Res. 103, 114-120. doi: 10.1016/j.schres.2008.03.006
47. Kim, D. J., Kent, J. S., Bolbecker, A. R., Sporns, O., Cheng, H., Newman, S. D., et al. (2014). Disrupted modular architecture of cerebellum in schizophrenia: a graph theoretic analysis. Schizophr. Bull. 40, 1216-1226. doi: 10.1093/schbul/sbu059
48. Krienen, F. M., and Buckner, R. L. (2009). Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 19, 2485-2497. doi: 10.1093/cercor/bhp135
49. Lane, A., Colgan, K., Moynihan, F., Burke, T., Waddington, J. L., Larkin, C., et al. (1996). Schizophrenia and neurological soft signs: gender differences in clinical correlates and antecedent factors. Psychiatry Res. 64, 105-114.
50. Liang, M., Zhou, Y., Jiang, T., Liu, Z., Tian, L., Liu, H., et al. (2006). Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. Neuroreport 17, 209-213. doi: 10.1097/01.wnr.0000198434.06518.b8
51. Liu, H., Fan, G., Xu, K., and Wang, F. (2011). Changes in cerebellar functional connectivity and anatomical connectivity in schizophrenia: a combined resting-state functional MRI and diffusion tensor imaging study. J. Magn. Reson. Imaging 34, 1430-1438. doi: 10.1002/jmri.22784
52. Lungu, O., Barakat, M., Laventure, S., Debas, K., Proulx, S., Luck, D., et al. (2013). The incidence and nature of cerebellar findings in schizophrenia: a quantitative review of fMRI literature. Schizophr Bull, 39, 797-806. doi: 10.1093/schbul/sbr193
53. Meunier, D., Achard, S., Morcom, A., and Bullmore, E. (2009). Age-related changes in modular organization of human brain functional networks. Neuroimage 44, 715-723. doi: 10.1016/j.neuroimage.2008.09.062
54. Meunier, D., Lambiotte, R., and Bullmore, E. T. (2010). Modular and hierarchically modular organization of brain networks. Front. Neurosci. 4:200. doi: 10.3389/fnins.2010.00200
55. Montgomery, S., and Asberg, M. (1979). A new depression scale designed to be sensitive to change. Br. J. Psychiatry 134, 382-389.
56. Newman, M. E. (2006a). Finding community structure in networks using the eigenvectors of matrices. Phys. Rev. E Stat. Nonlin. Soft. Matter Phys. 74:036104. doi: 10.1103/PhysRevE.74.036104
57. Newman, M. E. (2006b). Modularity and community structure in networks. Proc. Natl. Acad. Sci. U.S.A. 103, 8577-8582. doi: 10.1073/pnas.0601602103
58. Newman, M. E., and Girvan, M. (2004). Finding and evaluating community structure in networks. Phys. Rev. E Stat. Nonlin. Soft. Matter Phys. 69:026113. doi: 10.1103/PhysRevE.69.026113
59. Parnas, J. (1999). From predisposition to psychosis: progression of symptoms in schizophrenia. Acta Psychiatr. Scand.Suppl. 395, 20-29.
60. Parnas, J., Moller, P., Kircher, T., Thalbitzer, J., Jansson, L., Handest, P., et al. (2005). EASE: Examination of anomalous self-experience. Psychopathology 38, 236-258. doi: 10.1159/000088441
61. Picard, H., Amado, I., Mouchet-Mages, S., Olie, J. P., and Krebs, M. O. (2008). The role of the cerebellum in schizophrenia: an update of clinical, cognitive, and functional evidences. Schizophr. Bull. 34, 155-172. doi: 10.1093/schbul/sbm049
62. Pinkham, A. E. (2014). Social cognition in schizophrenia. J. Clin. Psychiatry 75(Suppl. 2), 14-19. doi: 10.4088/JCP.13065su1.04
63. Prasad, K. M., Sanders, R., Sweeney, J., Montrose, D., Diwadkar, V., Dworakowski, D., et al. (2009). Neurological abnormalities among offspring of persons with schizophrenia: relation to premorbid psychopathology. Schizophr. Res. 108, 163-169. doi: 10.1016/j.schres.2008.11.019
64. Reichenberg, A., and Harvey, P. D. (2007). Neuropsychological impairments in schizophrenia: Integration of performance-based and brain imaging findings. Psychol Bull, 133, 833-858. doi: 10.1037/0033-2909.133.5.833
65. Repovs, G., Csernansky, J. G., and Barch, D. M. (2011). Brain network connectivity in individuals with schizophrenia and their siblings. Biol. Psychiatry 69, 967-973. doi: 10.1016/j.biopsych.2010.11.009
66. Salmi, J., Pallesen, K. J., Neuvonen, T., Brattico, E., Korvenoja, A., Salonen, O., et al. (2009). Cognitive and motor loops of the human cerebro-cerebellar system. J. Cogn. Neurosci. 22, 2663-2676. doi: 10.1162/jocn.2009.21382
67. Schmahmann, J. D. (1991). An emerging concept. The cerebellar contribution to higher function. Arch Neurol, 48, 1178-1187.
68. Schmahmann, J. D. (1998). Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn. Sci. 2, 362-371.
69. Schmahmann, J. D., and Pandya, D. N. (1997). The cerebrocerebellar system. Int. Rev. Neurobiol. 41, 31-60.
70. Sepulcre, J., Liu, H., Talukdar, T., Martincorena, I., Yeo, B. T., and Buckner, R. L. (2010). The organization of local and distant functional connectivity in the human brain. PLoS Comput. Biol. 6:e1000808. doi: 10.1371/journal.pcbi.1000808
71. Shen, H., Wang, L., Liu, Y., and Hu, D. (2010). Discriminative analysis of resting-state functional connectivity patterns of schizophrenia using low dimensional embedding of fMRI. Neuroimage 49, 3110-3121. doi: 10.1016/j.neuroimage.2009.11.011
72. Shinn, A. K., Baker, J. T., Cohen, B. M., and Ongur, D. (2013a). Functional connectivity of left Heschl's gyrus in vulnerability to auditory hallucinations in schizophrenia. Schizophr Res. 143, 260-268. doi: 10.1016/j.schres.2012.11.037
73. Shinn, A. K., Heckers, S., and Ongur, D. (2013b). The special treatment of first rank auditory hallucinations and bizarre delusions in the diagnosis of schizophrenia. Schizophr Res. 146, 17-21. doi: 10.1016/j.schres.2013.02.040
74. Sim, K., Mahendran, R., Siris, S. G., Heckers, S., and Chong, S. A. (2004). Subjective quality of life in first episode schizophrenia spectrum disorders with comorbid depression. Psychiatry Res. 129, 141-147. doi: 10.1016/j.psychres.2004.07.007
75. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl. 1), S208-S219. doi: 10.1016/j.neuroimage.2004.07.051
76. Snider, R. S., and Stowell, A. (1944). Receiving areas of the tactile, auditory, and visual systems in the cerebellum.J. Neurophysiol. 7, 331-357. doi: 10.1016/j.neuroimage.2008.08.039
77. Stoodley, C. J., and Schmahmann, J. D. (2009). Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44, 489-501. doi: 10.1016/j.neuroimage.2008.08.039
78. Strick, P. L., Dum, R. P., and Fiez, J. A. (2009). Cerebellum and nonmotor function. Annu. Rev. Neurosci. 32, 413-434. doi: 10.1146/annurev.neuro.31.060407.125606
79. Su, T. W., Lan, T. H., Hsu, T. W., Biswal, B. B., Tsai, P. J., Lin, W. C., et al. (2013). Reduced neuro-integration from the dorsolateral prefrontal cortex to the whole brain and executive dysfunction in schizophrenia patients and their relatives. Schizophr. Res. 148, 50-58. doi: 10.1016/j.schres.2013.05.005
80. 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
81. van Dijk, K. R., Sabuncu, M. R., and Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59, 431-438. doi: 10.1016/j.neuroimage.2011.07.044
82. Wellsby, M., and Pexman, P. M. (2014). Developing embodied cognition: insights from children's concepts and language processing. Front. Psychol. 5:506. doi: 10.3389/fpsyg.2014.00506
83. Whitty, P. F., Owoeye, O., and Waddington, J. L. (2009). Neurological signs and involuntary movements in schizophrenia: intrinsic to and informative on systems pathobiology. Schizophr. Bull. 35, 415-424. doi: 10.1093/schbul/sbn126
84. Woodward, N. D., Karbasforoushan, H., and Heckers, S. (2012). Thalamocortical dysconnectivity in schizophrenia.Am. J. Psychiatry 169, 1092-1099. doi: 10.1176/appi.ajp.2012.12010056
85. Woolrich, M. W., Behrens, T. E., Beckmann, C. F., Jenkinson, M., and Smith, S. M. (2004). Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21, 1732-1747. doi: 10.1016/j.neuroimage.2003.12.023
86. Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., et al. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125-1165. doi: 10.1152/jn.00338.2011
87. Young, R. C., Biggs, J. T., Ziegler, V. E., and Meyer, D. A. (1978). A rating scale for mania: reliability, validity and sensitivity. Br. J. Psychiatry 133, 429-435.
88. Yu, Q., Plis, S. M., Erhardt, E. B., Allen, E. A., Sui, J., Kiehl, K. A., et al. (2012). Modular Organization of functional network connectivity in healthy controls and patients with Schizophrenia during the Resting State. Front. Syst. Neurosci. 5:103. doi: 10.3389/fnsys.2011.00103
89. Zabala, A., Robles, O., Parellada, M., Moreno, D. M., Ruiz-Sancho, A., Burdalo, M., et al. (2006). Neurological soft signs in adolescents with first episode psychosis. Eur. Psychiatry 21, 283-287. doi: 10.1016/j.eurpsy.2005.09.006