Aberrant hyperconnectivity in the motor system at rest is linked to motor abnormalities in schizophrenia spectrum disorders

Schizophrenia Bulletin

Volumn 43, Issue 5, 2017, Pages 982-992

  Walther, Sebastian ^a   Stegmayer, Katharina ^a   Federspiel, Andrea ^a   Bohlhalter, Stephan ^b   Wiest, Roland ^a   Viher, Petra V ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b LUZERNER KANTONSSPITAL   (Switzerland)

Author keywords

basal ganglia; cerebellum; dysconnectivity; STN

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BASAL GANGLION; CATATONIA; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; COORDINATION; DORSAL ANTERIOR CINGULATE CORTEX; DYSKINESIA; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MOTOR CORTEX; MOTOR DYSFUNCTION; MOTOR SYSTEM; PARKINSONISM; POSITIVE AND NEGATIVE SYNDROME SCALE; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA SPECTRUM DISORDER; SUBTHALAMIC NUCLEUS; SUPPLEMENTARY MOTOR AREA; THALAMUS; UNIFIED PARKINSON DISEASE RATING SCALE; BRAIN CORTEX; COMPLICATION; CONNECTOME; DIAGNOSTIC IMAGING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROCEDURES; SCHIZOPHRENIA; YOUNG ADULT;

ADULT; CATATONIA; CEREBELLUM; CEREBRAL CORTEX; CONNECTOME; DYSKINESIAS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR CORTEX; SCHIZOPHRENIA; SUBTHALAMIC NUCLEUS; THALAMUS; YOUNG ADULT;

EID: 85032034862     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbx091     Document Type: Article

References (90)

1. Walther S, Strik W. Motor symptoms and schizophrenia. Neuropsychobiology. 2012;66:77-92.
2. Koning JP, Tenback DE, van Os J, Aleman A, Kahn RS, van Harten PN. Dyskinesia and parkinsonism in antipsychotic-naive patients with schizophrenia, first-degree relatives and healthy controls: A meta-analysis. Schizophr Bull. 2010;36:723-731.
3. Kindler J, Schultze-Lutter F, Michel C, et al. Abnormal involuntary movements are linked to psychosis-risk in children and adolescents: Results of a population-based study. Schizophr Res. 2016;174:58-64.
4. Mittal VA, Orr JM, Turner JA, et al. Striatal abnormalities and spontaneous dyskinesias in non-clinical psychosis. Schizophr Res. 2013;151:141-147.
5. Bachmann S, Bottmer C, Schroder J. Neurological soft signs in first-episode schizophrenia: A follow-up study. Am J Psychiatry 2005;162:2337-2343.
6. Cuesta MJ, Sanchez-Torres AM, de Jalon EG, et al. Spontaneous parkinsonism is associated with cognitive impairment in antipsychotic-naive patients with first-episode psychosis: A 6-month follow-up study. Schizophr Bull. 2014;40:1164-1173.
7. McKenna PJ, Lund CE, Mortimer AM, Biggins CA. Motor, volitional and behavioural disorders in schizophrenia. 2: The 'conflict of paradigms' hypothesis. Br J Psychiatry. 1991;158:328-336.
8. Peralta V, Campos MS, De Jalon EG, Cuesta MJ. Motor behavior abnormalities in drug-naive patients with schizophrenia spectrum disorders. Mov Disord. 2010;25:1068-1076.
9. Peralta V, Cuesta MJ. Motor features in psychotic disorders. I. Factor structure and clinical correlates. Schizophr Res. 2001;47:107-116.
10. Docx L, Morrens M, Bervoets C, et al. Parsing the components of the psychomotor syndrome in schizophrenia. Acta Psychiatr Scand. 2012;126:256-265.
11. Walther S. Psychomotor symptoms of schizophrenia map on the cerebral motor circuit. Psychiatry Res. 2015;233:293-298.
12. Douaud G, Smith S, Jenkinson M, et al. Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain. 2007;130:2375-2386.
13. Haijma SV, Van Haren N, Cahn W, Koolschijn PC, Hulshoff Pol HE, Kahn RS. Brain volumes in schizophrenia: A meta-analysis in over 18 000 subjects. Schizophr Bull. 2013;39:1129-1138.
14. Schneiderman JS, Hazlett EA, Chu KW, et al. Brodmann area analysis of white matter anisotropy and age in schizophrenia. Schizophr Res. 2011;130:57-67.
15. Ellison-Wright I, Nathan PJ, Bullmore ET, et al. Distribution of tract deficits in schizophrenia. BMC Psychiatry. 2014;14:99.
16. Liu J, Qiu M, Constable RT, Wexler BE. Does baseline cerebral blood flow affect task-related blood oxygenation level dependent response in schizophrenia? Schizophr Res. 2012;140:143-148.
17. Walther S, Federspiel A, Horn H, et al. Resting state cerebral blood flow and objective motor activity reveal basal ganglia dysfunction in schizophrenia. Psychiatry Res. 2011;192:117-124.
18. Pinkham A, Loughead J, Ruparel K, et al. Resting quantitative cerebral blood flow in schizophrenia measured by pulsed arterial spin labeling perfusion MRI. Psychiatry Res. 2011;194:64-72.
19. Pinkham AE, Liu P, Lu H, Kriegsman M, Simpson C, Tamminga C. Amygdala hyperactivity at rest in paranoid individuals with schizophrenia. Am J Psychiatry. 2015;172:784-792.
20. Kindler J, Schultze-Lutter F, Hauf M, et al. Increased striatal and reduced prefrontal cerebral blood flow in clinical high risk for psychosis. Schizophr Bull. In press.
21. Stegmayer K, Strik W, Federspiel A, Wiest R, Bohlhalter S, Walther S. Specific cerebral perfusion patterns in three schizophrenia symptom dimensions [published online ahead of print March 17, 2017]. Schizophr Res. doi:10.1016/j. schres.2017.03.018.
22. Bernard JA, Mittal VA. Dysfunctional activation of the cerebellum in schizophrenia: A functional neuroimaging metaanalysis. Clin Psychol Sci. 2015;3:545-566.
23. Bernard JA, Russell CE, Newberry RE, Goen JR, Mittal VA. Patients with schizophrenia show aberrant patterns of basal ganglia activation: Evidence from ALE meta-analysis. NeuroImage Clinical. 2017;14:450-463.
24. Viher PV, Stegmayer K, Giezendanner S, et al. Cerebral white matter structure is associated with DSM-5 schizophrenia symptom dimensions. NeuroImage Clinical. 2016;12:93-99.
25. Bracht T, Schnell S, Federspiel A, et al. Altered cortico-basal ganglia motor pathways reflect reduced volitional motor activity in schizophrenia. Schizophr Res. 2013;143:269-276.
26. Walther S, Federspiel A, Horn H, et al. Alterations of white matter integrity related to motor activity in schizophrenia. Neurobiol Dis. 2011;42:276-283.
27. Bai YM, Chou KH, Lin CP, et al. White matter abnormalities in schizophrenia patients with tardive dyskinesia: A diffusion tensor image study. Schizophr Res. 2009;109:167-181.
28. Docx L, Emsell L, Van Hecke W, et al. White matter microstructure and volitional motor activity in schizophrenia: A diffusion kurtosis imaging study. Psychiatry Res 2016;260:29-36.
29. Hirjak D, Wolf RC, Stieltjes B, et al. Cortical signature of neurological soft signs in recent onset schizophrenia. Brain Topography. 2014;27:296-306.
30. Stegmayer K, Horn H, Federspiel A, et al. Supplementary motor area (SMA) volume is associated with psychotic aberrant motor behaviour of patients with schizophrenia. Psychiatry Res. 2014;223:49-51.
31. Dazzan P, Morgan KD, Orr KG, et al. The structural brain correlates of neurological soft signs in AESOP first-episode psychoses study. Brain. 2004;127(Pt 1):143-153.
32. Hirjak D, Wolf RC, Stieltjes B, Seidl U, Schroder J, Thomann PA. Neurological soft signs and subcortical brain morphology in recent onset schizophrenia. J Psychiatr Res 2012;46:533-539.
33. Walther S, Schappi L, Federspiel A, et al. Resting-state hyperperfusion of the supplementary motor area in catatonia. Schizophr Bull. In press.
34. Zhao Q, Li Z, Huang J, et al. Neurological soft signs are not "soft" in brain structure and functional networks: Evidence from ALE meta-analysis. Schizophr Bull. 2014;40:626-641.
35. Scheuerecker J, Ufer S, Kapernick M, et al. Cerebral network deficits in post-acute catatonic schizophrenic patients measured by fMRI. J Psychiatr Res. 2009;43:607-614.
36. Anticevic A, Cole MW, Repovs G, et al. Characterizing thalamo-cortical disturbances in schizophrenia and bipolar illness. Cereb Cortex. 2014;24:3116-3130.
37. Klingner CM, Langbein K, Dietzek M, et al. Thalamocortical connectivity during resting state in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2014;264:111-119.
38. Woodward ND, Karbasforoushan H, Heckers S. Thalamocortical dysconnectivity in schizophrenia. Am J Psychiatry. 2012;169:1092-1099.
39. Anticevic A, Haut K, Murray JD, et al. Association of thalamic dysconnectivity and conversion to psychosis in youth and young adults at elevated clinical risk. JAMA Psychiatry. 2015;72:882-891.
40. Bernard JA, Dean DJ, Kent JS, et al. Cerebellar networks in individuals at ultra high-risk of psychosis: Impact on postural sway and symptom severity. Hum Brain Mapp. 2014;35:4064-4078.
41. Kaufmann T, Skatun KC, Alnaes D, et al. Disintegration of sensorimotor brain networks in schizophrenia. Schizophr Bull. 2015;41:1326-1335.
42. Berman RA, Gotts SJ, McAdams HM, et al. Disrupted sensorimotor and social-cognitive networks underlie symptoms in childhood-onset schizophrenia. Brain. 2016;139(Pt 1):276-291.
43. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia. 1971;9:97-113.
44. Sheehan DV, Lecrubier Y, Sheehan KH, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59(suppl 20):22-33;quiz 34-57.
45. Andreasen NC, Flaum M, Arndt S. The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. Arch Gen Psychiatry. 1992;49:615-623.
46. Brown L, Sherbenou RJ, Johnsen SK. Test of Nonverbal Intelligence. Austin, TX: PRO-ED; 1982.
47. Bush G, Fink M, Petrides G, Dowling F, Francis A. Catatonia. I. Rating scale and standardized examination. Acta Psychiatr Scand. 1996;93:129-136.
48. Lund CE, Mortimer AM, Rogers D, McKenna PJ. Motor, volitional and behavioural disorders in schizophrenia. 1: Assessment using the Modified Rogers Scale. Br J Psychiatry 1991;158:323-327, 333-326.
49. Fahn S, Elton RL, Members UP. Unified Parkinson's disease rating scale. In: Fahn S, Marsden CD, Goldstein M, Calne DB, eds. Recent Developments in Parkinson's Disease. Vol 2. Florham Park, NJ: Macmillan Healthcare Information; 1987.
50. Guy W. ECDEU Assessment Manual for Psychopharmacology. Rockville, MD: US Department of Health, Education and Welfare; 1976.
51. Buchanan RW, Heinrichs DW. The Neurological Evaluation Scale (NES): A structured instrument for the assessment of neurological signs in schizophrenia. Psychiatry Res. 1989;27:335-350.
52. Walther S, Koschorke P, Horn H, Strik W. Objectively measured motor activity in schizophrenia challenges the validity of expert ratings. Psychiatry Res. 2009;169:187-190.
53. Deichmann R, Schwarzbauer C, Turner R. Optimisation of the 3D MDEFT sequence for anatomical brain imaging: Technical implications at 1.5 and 3 T. Neuroimage. 2004;21:757-767.
54. Whitfield-Gabrieli S, Nieto-Castanon A. Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012;2:125-141.
55. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage. 2012;59:2142-2154.
56. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19:1233-1239.
57. Haber SN, Behrens TE. The neural network underlying incentive-based learning: Implications for interpreting circuit disruptions in psychiatric disorders. Neuron. 2014;83:1019-1039.
58. Haber SN. Corticostriatal circuitry. Dialogues Clin Neurosci. 2016;18:7-21.
59. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. Neuroimage. 2009;44:489-501.
60. 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.
61. Nieuwenhuys R, Voogd J, van Huijzen C. The Human Central Nervous System. 4th ed. Heidelberg, Germany: Steinkopff; 2008.
62. Vogt BA. Regions and subregions of the cingulate cortex. In: Vogt BA, ed. Cingulate Neurobiology and Disease. Vol 1. New York, NY: Oxford University Press, Inc.; 2009.
63. Habas C. Functional connectivity of the human rostral and caudal cingulate motor areas in the brain resting state at 3T. Neuroradiology. 2010;52:47-59.
64. Bernard JA, Mittal VA. Updating the research domain criteria: The utility of a motor dimension. Psychol Med. 2015;45:2685-2689.
65. Cheng W, Palaniyappan L, Li M, et al. Voxel-based, brainwide association study of aberrant functional connectivity in schizophrenia implicates thalamocortical circuitry. NPJ Schizophr. 2015;1:15016.
66. Chen YL, Tu PC, Lee YC, Chen YS, Li CT, Su TP. Restingstate fMRI mapping of cerebellar functional dysconnections involving multiple large-scale networks in patients with schizophrenia. Schizophr Res. 2013;149:26-34.
67. Bernard JA, Orr JM, Mittal VA. Cerebello-thalamo-cortical networks predict positive symptom progression in individuals at ultra-high risk for psychosis. NeuroImage Clinical. 2017;14:622-628.
68. Picazio S, Koch G. Is motor inhibition mediated by cerebellocortical interactions? Cerebellum. 2015;14:47-49.
69. Panyakaew P, Cho HJ, Srivanitchapoom P, Popa T, Wu T, Hallett M. Cerebellar brain inhibition in the target and surround muscles during voluntary tonic activation. Eur J Neurosci. 2016;43:1075-1081.
70. Zavala B, Zaghloul K, Brown P. The subthalamic nucleus, oscillations, and conflict. Mov Disord. 2015;30:328-338.
71. Hamani C, Saint-Cyr JA, Fraser J, Kaplitt M, Lozano AM. The subthalamic nucleus in the context of movement disorders. Brain. 2004;127:4-20.
72. Kahan J, Urner M, Moran R, et al. Resting state functional MRI in Parkinson's disease: The impact of deep brain stimulation on 'effective' connectivity. Brain 2014;137:1130-1144.
73. Kurani AS, Seidler RD, Burciu RG, et al. Subthalamic nucleus-sensorimotor cortex functional connectivity in de novo and moderate Parkinson's disease. Neurobiol Aging. 2015;36:462-469.
74. Baudrexel S, Witte T, Seifried C, et al. Resting state fMRI reveals increased subthalamic nucleus-motor cortex connectivity in Parkinson's disease. Neuroimage. 2011;55:1728-1738.
75. Herz DM, Christensen MS, Bruggemann N, et al. Motivational tuning of fronto-subthalamic connectivity facilitates control of action impulses. J Neurosci. 2014;34:3210-3217.
76. Alkemade A, Schnitzler A, Forstmann BU. Topographic organization of the human and non-human primate subthalamic nucleus. Brain Struct Funct. 2015;220:3075-3086.
77. Barbalat G, Chambon V, Domenech PJ, et al. Impaired hierarchical control within the lateral prefrontal cortex in schizophrenia. Biol Psychiatry. 2011;70:73-80.
78. Groenewegen HJ. The basal ganglia and motor control. Neural Plast. 2003;10:107-120.
79. Oguri T, Sawamoto N, Tabu H, et al. Overlapping connections within the motor cortico-basal ganglia circuit: FMRItractography analysis. Neuroimage. 2013;78:353-362.
80. Bostan AC, Dum RP, Strick PL. The basal ganglia communicate with the cerebellum. Proc Natl Acad Sci U S A. 2010;107:8452-8456.
81. Pool EM, Rehme AK, Fink GR, Eickhoff SB, Grefkes C. Network dynamics engaged in the modulation of motor behavior in healthy subjects. Neuroimage. 2013;82:68-76.
82. Docx L, Sabbe B, Provinciael P, Merckx N, Morrens M. Quantitative psychomotor dysfunction in schizophrenia: A loss of drive, impaired movement execution or both? Neuropsychobiology. 2013;68:221-227.
83. Wilson JE, Niu K, Nicolson SE, Levine SZ, Heckers S. The diagnostic criteria and structure of catatonia. Schizophr Res. 2015;164:256-262.
84. Northoff G, Kotter R, Baumgart F, et al. Orbitofrontal cortical dysfunction in akinetic catatonia: A functional magnetic resonance imaging study during negative emotional stimulation. Schizophr Bull. 2004;30:405-427.
85. Northoff G, Steinke R, Nagel DC, et al. Right lower prefronto-parietal cortical dysfunction in akinetic catatonia: A combined study of neuropsychology and regional cerebral blood flow. Psychol Med. 2000;30:583-596.
86. Kraguljac NV, White DM, Hadley JA, et al. Abnormalities in large scale functional networks in unmedicated patients with schizophrenia and effects of risperidone. NeuroImage Clinical. 2016;10:146-158.
87. Sarpal DK, Robinson DG, Lencz T, et al. Antipsychotic treatment and functional connectivity of the striatum in firstepisode schizophrenia. JAMA Psychiatry. 2015;72:5-13.
88. Hutcheson NL, Sreenivasan KR, Deshpande G, et al. Effective connectivity during episodic memory retrieval in schizophrenia participants before and after antipsychotic medication. Hum Brain Mapp. 2015;36:1442-1457.
89. Gass N, Schwarz AJ, Sartorius A, et al. Haloperidol modulates midbrain-prefrontal functional connectivity in the rat brain. Eur Neuropsychopharmacol. 2013;23:1310-1319.
90. Peralta V, Cuesta MJ. The effect of antipsychotic medication on neuromotor abnormalities in neuroleptic-naive nonaffective psychotic patients: A naturalistic study with haloperidol, risperidone, or olanzapine. Prim Care Companion J Clin Psychiatry. 2010;12. doi:10.4088/PCC.09m00799gry