Abnormal resting-state connectivity in a substantia nigra-related striato-thalamo-cortical network in a large sample of first-episode drug-naïve patients with schizophrenia

Schizophrenia Bulletin

Volumn 44, Issue 2, 2018, Pages 419-431

  Martino, Matteo ^a,b   Magioncalda, Paola ^a,b   Yu, Hua ^a   Li, Xiaojing ^a   Wang, Qiang ^a   Meng, Yajing ^a   Deng, Wei ^a   Li, Yinfei ^a   Li, Mingli ^a   Ma, Xiaohong ^a   Lane, Timothy ^c   Duncan, Niall W ^c,d   Northoff, Georg ^c,d,e,f,g,h   Li, Tao ^a  

^a SICHUAN UNIVERSITY   (China)

^b UNIVERSITY OF GENOA   (Italy)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d HANGZHOU NORMAL UNIVERSITY   (China)

^e UNIVERSITY OF OTTAWA   (Canada)

^f UNIVERSITY OF OTTAWA   (Canada)

^g NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

^h ZHEJIANG UNIVERSITY   (China)

Author keywords

Functional connectivity; Neural synchronization; Resting state fMRI; Schizophrenia; Slow frequency bands; Substantia nigra

Indexed keywords

ADULT; CONNECTOME; CORPUS STRIATUM; DIAGNOSTIC IMAGING; FEMALE; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROCEDURES; SCHIZOPHRENIA; SENSORIMOTOR CORTEX; SUBSTANTIA NIGRA; THALAMUS; YOUNG ADULT;

ADULT; CONNECTOME; CORPUS STRIATUM; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; SCHIZOPHRENIA; SENSORIMOTOR CORTEX; SUBSTANTIA NIGRA; THALAMUS; YOUNG ADULT;

EID: 85049005726     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbx067     Document Type: Article

References (85)

1. American Psychiatrich Association. Diagnostic and Statistical Manual for Mental Disorders. 5th ed. (DSM-5). Washington, DC: American Psychiatrich Association; 2013.
2. Abi-Dargham A. Schizophrenia: overview and dopamine dysfunction. J Clin Psychiatry. 2014;75:e31.
3. Lewis DA, Gonzalez-Burgos G. Pathophysiologically based treatment interventions in schizophrenia. Nat Med. 2006;12:1016-1022.
4. Weinberger DR. The biological basis of schizophrenia: new directions. J Clin Psychiatry. 1997;58(suppl 10):22-27.
5. Meltzer HY, Stahl SM. The dopamine hypothesis of schizophrenia: a review. Schizophr Bull. 1976;2:19-76.
6. Grace AA. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience. 1991;41:1-24.
7. Davis KL, Kahn RS, Ko G, Davidson M. Dopamine in schizophrenia: a review and reconceptualization. Am J Psychiatry. 1991;148:1474-1486.
8. Howes OD, Kapur S. The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr Bull. 2009;35:549-562.
9. Howes OD, Kambeitz J, Kim E, et al. The nature of dopamine dysfunction in schizophrenia and what this means for treatment. Arch Gen Psychiatry. 2012;69:776-786.
10. Kambeitz J, Abi-Dargham A, Kapur S, Howes OD. Alterations in cortical and extrastriatal subcortical dopamine function in schizophrenia: systematic review and meta-analysis of imaging studies. Br J Psychiatry. 2014;204:420-429.
11. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci. 2007;8:700-711.
12. Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304:1926-1929.
13. Zhang D, Raichle ME. Disease and the brain's dark energy. Nat Rev Neurol. 2010;6:15-28.
14. Zuo XN, Di Martino A, Kelly C, et al. The oscillating brain: complex and reliable. Neuroimage. 2010;49:1432-1445.
15. Balduzzi D, Riedner BA, Tononi G. A BOLD window into brain waves. Proc Natl Acad Sci U S A. 2008;105:15641-15642.
16. Cole DM, Beckmann CF, Oei NY, Both S, van Gerven JM, Rombouts SA. Differential and distributed effects of dopamine neuromodulations on resting-state network connectivity. Neuroimage. 2013;78:59-67.
17. Kelly C, de Zubicaray G, Di Martino A, et al. L-dopa modulates functional connectivity in striatal cognitive and motor networks: a double-blind placebo-controlled study. J Neurosci. 2009;29:7364-7378.
18. Nagano-Saito A, Leyton M, Monchi O, Goldberg YK, He Y, Dagher A. Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. J Neurosci. 2008;28:3697-3706.
19. Cole DM, Oei NY, Soeter RP, et al. Dopamine-dependent architecture of cortico-subcortical network connectivity. Cereb Cortex. 2013;23:1509-1516.
20. Metzger CD, Wiegers M, Walter M, Abler B, Graf H. Local and global resting state activity in the noradrenergic and dopaminergic pathway modulated by reboxetine and amisulpride in healthy subjects. Int J Neuropsychopharmacol 2015;19:1-9. doi:10.1093/ijnp/pyv080.
21. Weinberger DR, Radulescu E. Finding the elusive psychiatric "lesion" with 21st-century neuroanatomy: a note of caution. Am J Psychiatry. 2016;173:27-33.
22. Pergola G, Selvaggi P, Trizio S, Bertolino A, Blasi G. The role of the thalamus in schizophrenia from a neuroimaging perspective. Neurosci Biobehav Rev. 2015;54:57-75.
23. Kaufmann T, Skåtun KC, Alnæs D, et al. Disintegration of sensorimotor brain networks in schizophrenia. Schizophr Bull. 2015;41:1326-1335.
24. Li T, Wang Q, Zhang J, et al. Brain-wide analysis of functional connectivity in first-episode and chronic stages of schizophrenia. Schizophr Bull. 2017;43:436-448.
25. Hadley JA, Nenert R, Kraguljac NV, et al. Ventral tegmental area/midbrain functional connectivity and response to antipsychotic medication in schizophrenia. Neuropsychopharmacology. 2014;39:1020-1030.
26. White TP, Wigton R, Joyce DW, Collier T, Fornito A, Shergill SS. Dysfunctional striatal systems in treatmentresistant schizophrenia. Neuropsychopharmacology. 2016;41:1274-1285.
27. Xue SW, Li D, Weng XC, Northoff G, Li DW. Different neural manifestations of two slow frequency bands in resting functional magnetic resonance imaging: a systemic survey at regional, interregional, and network levels. Brain Connect. 2014;4:242-255.
28. Martino M, Magioncalda P, Huang Z, et al. Contrasting variability patterns in the default mode and sensorimotor networks balance in bipolar depression and mania. Proc Natl Acad Sci U S A. 2016;113:4824-4829.
29. Buzsaki G. Rhythms of the brain. New York, NY: Oxford University Press; 2006.
30. Huang Z, Zhang J, Longtin A, et al. Is there a nonadditive interaction between spontaneous and evoked activity? Phasedependence and its relation to the temporal structure of scale-free brain activity. Cereb Cortex. 2015;27:1037-1059.
31. Penttonen M, Buszsaki G. Natural logarithmic relationship between brain oscillators. Thalamus Relat Syst. 2003;48:1-8.
32. Peralta V, Campos MS, De Jalón EG, Cuesta MJ. Motor behavior abnormalities in drug-naïve patients with schizophrenia spectrum disorders. Mov Disord. 2010;25:1068-1076.
33. Javitt DC, Sweet RA. Auditory dysfunction in schizophrenia: integrating clinical and basic features. Nat Rev Neurosci. 2015;16:535-550.
34. Putzhammer A, Klein HE. Quantitative analysis of motor disturbances in schizophrenic patients. Dialogues Clin Neurosci. 2006;8:123-130.
35. Bachmann S, Degen C, Geider FJ, Schröder J. Neurological soft signs in the clinical course of schizophrenia: results of a meta-analysis. Front Psychiatry. 2014;5:185.
36. Dazzan P, Murray RM. Neurological soft signs in first-episode psychosis: a systematic review. Br J Psychiatry Suppl. 2002;43:s50-s57.
37. Northoff G, Duncan NW. How do abnormalities in the brain's spontaneous activity translate into symptoms in schizophrenia? From an overview of resting state activity findings to a proposed spatiotemporal psychopathology. Prog Neurobiol. 2016;145-146:26-45.
38. Northoff G. What catatonia can tell us about "top-down modulation": a neuropsychiatric hypothesis. Behav Brain Sci. 2002;25:555-77; discussion 578.
39. Walker EF, Savoie T, Davis D. Neuromotor precursors of schizophrenia. Schizophr Bull. 1994;20:441-451.
40. Walker E, Lewis N, Loewy R, Palyo S. Motor dysfunction and risk for schizophrenia. Dev Psychopathol. 1999;11:509-523.
41. Javitt DC, Freedman R. Sensory processing dysfunction in the personal experience and neuronal machinery of schizophrenia. Am J Psychiatry. 2015;172:17-31.
42. Schultze-Lutter F. Subjective symptoms of schizophrenia in research and the clinic: the basic symptom concept. Schizophr Bull. 2009;35:5-8.
43. Docx L, Morrens M, Bervoets C, et al. Parsing the components of the psychomotor syndrome in schizophrenia. Acta Psychiatr Scand. 2012;126:256-265.
44. Javitt DC. Sensory processing in schizophrenia: neither simple nor intact. Schizophr Bull. 2009;35:1059-1064.
45. He Z, Deng W, Li M, et al. Aberrant intrinsic brain activity and cognitive deficit in first-episode treatment-naive patients with schizophrenia. Psychol Med. 2013;43:769-780.
46. Lei W, Li M, Deng W, et al. Sex-specific patterns of aberrant brain function in first-episode treatment-naive patients with schizophrenia. Int J Mol Sci. 2015;16:16125-16143.
47. Molochnikov I, Cohen D. Hemispheric differences in the mesostriatal dopaminergic system. Front Syst Neurosci. 2014;8:110.
48. Ribolsi M, Daskalakis ZJ, Siracusano A, Koch G. Abnormal asymmetry of brain connectivity in schizophrenia. Front Hum Neurosci. 2014;8:1010.
49. Keuken MC, Bazin PL, Crown L, et al. Quantifying interindividual anatomical variability in the subcortex using 7 T structural MRI. Neuroimage. 2014;94:40-46.
50. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 2002;15:1-25.
51. Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44:83-98.
52. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13:261-276.
53. Tomasi D, Volkow ND. Functional connectivity of substantia nigra and ventral tegmental area: maturation during adolescence and effects of ADHD. Cereb Cortex. 2014;24:935-944.
54. Haber SN, Fudge JL. The primate substantia nigra and VTA: integrative circuitry and function. Crit Rev Neurobiol. 1997;11:323-342.
55. Albin RL, Young AB, Penney JB. The functional anatomy of disorders of the basal ganglia. Trends Neurosci. 1995;18:63-64.
56. Amalric M, Koob GF. Functionally selective neurochemical afferents and efferents of the mesocorticolimbic and nigrostriatal dopamine system. Prog Brain Res. 1993;99:209-226.
57. Freeman A, Ciliax B, Bakay R, et al. Nigrostriatal collaterals to thalamus degenerate in parkinsonian animal models. Ann Neurol. 2001;50:321-329.
58. He BJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME. Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc Natl Acad Sci U S A. 2008;105:16039-16044.
59. Zou Q, Wu CW, Stein EA, Zang Y, Yang Y. Static and dynamic characteristics of cerebral blood flow during the resting state. Neuroimage. 2009;48:515-524.
60. Garrett DD, Samanez-Larkin GR, MacDonald SW, Lindenberger U, McIntosh AR, Grady CL. Moment-tomoment brain signal variability: a next frontier in human brain mapping? Neurosci Biobehav Rev. 2013;37:610-624.
61. Yoon JH, Minzenberg MJ, Raouf S, D'Esposito M, Carter CS. Impaired prefrontal-basal ganglia functional connectivity and substantia nigra hyperactivity in schizophrenia. Biol Psychiatry. 2013;74:122-129.
62. Yoon JH, Westphal AJ, Minzenberg MJ, et al. Task-evoked substantia nigra hyperactivity associated with prefrontal hypofunction, prefrontonigral disconnectivity and nigrostriatal connectivity predicting psychosis severity in medication naïve first episode schizophrenia. Schizophr Res. 2014;159:521-526.
63. Wichmann T, DeLong M. The basal ganglia. In: Kandel E, Schwartz J, Jessel T, eds. Principles of Neural Sciences-Fifth edition. Ch 43. New York, NY: McGraw Hill; 2013:982-998.
64. Woodward ND, Karbasforoushan H, Heckers S. Thalamocortical dysconnectivity in schizophrenia. Am J Psychiatry. 2012;169:1092-1099.
65. Anticevic A, Cole MW, Repovs G, et al. Characterizing thalamo-cortical disturbances in schizophrenia and bipolar illness. Cereb Cortex. 2014;24:3116-3130.
66. Welsh RC, Chen AC, Taylor SF. Low-frequency BOLD fluctuations demonstrate altered thalamocortical connectivity in schizophrenia. Schizophr Bull. 2010;36:713-722.
67. Klingner CM, Langbein K, Dietzek M, et al. Thalamocortical connectivity during resting state in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2014;264:111-119.
68. Tu PC, Lee YC, Chen YS, Hsu JW, Li CT, Su TP. Networkspecific cortico-thalamic dysconnection in schizophrenia revealed by intrinsic functional connectivity analyses. Schizophr Res. 2015;166:137-143.
69. Lerman-Sinkoff DB, Barch DM. Network community structure alterations in adult schizophrenia: identification and localization of alterations. Neuroimage Clin. 2016;10:96-106.
70. Atluri G, Steinbach M, Lim KO, Kumar V, MacDonald A III. Connectivity cluster analysis for discovering discriminative subnetworks in schizophrenia. Hum Brain Mapp. 2015;36:756-767.
71. Wang HL, Rau CL, Li YM, Chen YP, Yu R. Disrupted thalamic resting-state functional networks in schizophrenia. Front Behav Neurosci. 2015;9:45.
72. Woodward ND, Heckers S. Mapping thalamocortical functional connectivity in chronic and early stages of psychotic disorders. Biol Psychiatry. 2016;79:1016-1025.
73. Giraldo-Chica M, Woodward ND. Review of thalamocortical resting-state fMRI studies in schizophrenia. Schizophr Res. 2017;180:58-63.
74. 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.
75. Bentivoglio M, Morelli M. The organization and circuits of mesencephalic dopaminergic neurons and the distribution of dopamine receptors in the brain. In: Dunnett SB, ed. Handbook of Chemical Neuroanatomy. Vol. 21. Amsterdam, Netherlands: Elsevier; 2005:1-107.
76. Glahn DC, Laird AR, Ellison-Wright I, et al. Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol Psychiatry. 2008;64:774-781.
77. Schröder J, Wenz F, Schad LR, Baudendistel K, Knopp MV. Sensorimotor cortex and supplementary motor area changes in schizophrenia. A study with functional magnetic resonance imaging. Br J Psychiatry. 1995;167:197-201.
78. Northoff G, Duncan NW. How do abnormalities in the brain's spontaneous activity translate into symptoms in schizophrenia? From an overview of resting state activity findings to a proposed spatiotemporal psychopathology. Progress in Neurobiology In press 2016;145-146:26-45.
79. Northoff G. Spatiotemporal Psychopathology II: how does a psychopathology of the brain's resting state look like? Spatiotemporal approach and the history of psychopathology. J Affect Disord. 2016;190:867-879.
80. Cole DM, Beckmann CF, Searle GE, et al. Orbitofrontal connectivity with resting-state networks is associated with midbrain dopamine D3 receptor availability. Cereb Cortex. 2012;22:2784-2793.
81. Rieckmann A, Karlsson S, Fischer H, Bäckman L. Caudate dopamine D1 receptor density is associated with individual differences in frontoparietal connectivity during working memory. J Neurosci. 2011;31:14284-14290.
82. Horga G, Cassidy CM, Xu X, et al. Dopamine-related disruption of functional topography of striatal connections in unmedicated patients with schizophrenia. JAMA Psychiatry. 2016;73:862-870.
83. De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM. fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage. 2006;29:1359-1367.
84. Damoiseaux JS, Rombouts SA, Barkhof F, et al. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A. 2006;103:13848-13853.
85. Dosenbach NU, Fair DA, Miezin FM, et al. Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci U S A. 2007;104:11073-11078.