Contrasting variability patterns in the default mode and sensorimotor networks balance in bipolar depression and mania

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 17, 2016, Pages 4824-4829

  Martino, Matteo ^a   Magioncalda, Paola ^a   Huang, Zirui ^b   Conio, Benedetta ^a   Piaggio, Niccolò ^a   Duncan, Niall W ^c,d,e   Rocchi, Giulio ^a   Escelsior, Andrea ^a   Marozzi, Valentina ^a   Wolff, Annemarie ^b   Inglese, Matilde ^a,f   Amore, Mario ^a   Northoff, Georg ^{b,c,d,e,g,h,i}  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF OTTAWA   (Canada)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e Hangzhou Normal College   (China)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^g NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

^h ZHEJIANG UNIVERSITY   (China)

ⁱ UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Bipolar disorder; Default mode network; Neuronal variability; Sensorimotor network

Indexed keywords

ANTERIOR CINGULATE; BIPOLAR DEPRESSION; BOLD SIGNAL; CINGULATE GYRUS; CLINICAL ARTICLE; CONFERENCE PAPER; CONTROLLED STUDY; DEFAULT MODE NETWORK; ELECTROENCEPHALOGRAM; FOLLOW UP; HAMILTON DEPRESSION RATING SCALE; HUMAN; INFERIOR PARIETAL LOBULE; MANIA; MEDIAL PREFRONTAL CORTEX; MIDDLE FRONTAL GYRUS; MIDDLE TEMPORAL GYRUS; NERVE CELL NETWORK; NEUROIMAGING; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; POTENTIAL DIFFERENCE; PRIORITY JOURNAL; REPLICATION STUDY; RESTING STATE NETWORK; SENSORIMOTOR FUNCTION; YOUNG MANIA RATING SCALE; ADOLESCENT; ADULT; AFFECT; BIPOLAR DISORDER; BLOOD; BRAIN MAPPING; COMPARATIVE STUDY; FEMALE; MALE; MIDDLE AGED; MOVEMENT (PHYSIOLOGY); NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; REST; RESTLESSNESS; SENSATION; THINKING; YOUNG ADULT;

OXYGEN;

ADOLESCENT; ADULT; AFFECT; BIPOLAR DISORDER; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOVEMENT; NERVE NET; OXYGEN; PSYCHOMOTOR AGITATION; REST; SENSATION; THINKING; YOUNG ADULT;

EID: 84964703131     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1517558113     Document Type: Article

References (93)

1. American Psychiatrich Association (2013) Diagnostic and Statistical Manual for Mental Disorders. 5th ed. (DSM-5). (American Psychiatrich Association, Washington, DC).
2. Kraepelin E (1902) Clinical Psychiatry (Macmillan, New York).
3. Northoff G (2016) Spatiotemporal psychopathology I: No rest for the brain's resting state activity in depression? Spatiotemporal psychopathology of depressive symptoms. J Affect Disord 190:854-866.
4. Northoff G (2016) 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 190:867-879.
5. Minassian A, et al. (2010) The quantitative assessment of motor activity in mania and schizophrenia. J Affect Disord 120(1-3):200-206.
6. Souery D, et al. (2012) Depression across mood disorders: Review and analysis in a clinical sample. Compr Psychiatry 53(1):24-38.
7. Northoff G, Sibille E (2014) Why are cortical GABA neurons relevant to internal focus in depression? A cross-level model linking cellular, biochemical and neural network findings. Mol Psychiatry 19(9):966-977.
8. Raichle ME, et al. (2001) A default mode of brain function. Proc Natl Acad Sci USA 98(2):676-682.
9. Raichle ME (2015) The brain's default mode network. Annu Rev Neurosci 38:433-447.
10. Huang S, et al. (2015) Multisensory competition is modulated by sensory pathway interactions with fronto-sensorimotor and default-mode network regions. J Neurosci 35(24):9064-9077.
11. Jilka SR, et al. (2014) Damage to the salience network and interactions with the default node network. J Neurosci 34(33):10798-10807.
12. Goulden N, et al. (2014) The salience network is responsible for switching between the default mode network and the central executive network: Replication from DCM. Neuroimage 99:180-190.
13. Fox MD, et al. (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102(27):9673-9678.
14. Davidson RJ (2000) Affective style, psychopathology, and resilience: Brain mechanisms and plasticity. Am Psychol 55(11):1196-1214.
15. Mason MF, et al. (2007) Wandering minds: The default network and stimulusindependent thought. Science 315(5810):393-395.
16. Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW (2009) Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proc Natl Acad Sci USA 106(21):8719-8724.
17. Magioncalda P, et al. (2015) Functional connectivity and neuronal variability of resting state activity in bipolar disorder-Reduction and decoupling in anterior cortical midline structures. Hum Brain Mapp 36(2):666-682.
18. Anand A, Li Y, Wang Y, Lowe MJ, Dzemidzic M (2009) Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression. Psychiatry Res 171(3):189-198.
19. Ongür D, et al. (2010) Default mode network abnormalities in bipolar disorder and schizophrenia. Psychiatry Res 183(1):59-68.
20. Anticevic A, et al. (2015) Ventral anterior cingulate connectivity distinguished nonpsychotic bipolar illness from psychotic bipolar disorder and schizophrenia. Schizophr Bull 41(1):133-143.
21. Meda SA, et al. (2014) Multivariate analysis reveals genetic associations of the resting default mode network in psychotic bipolar disorder and schizophrenia. Proc Natl Acad Sci USA 111(19):E2066-E2075.
22. Sheline YI, et al. (2009) The default mode network and self-referential processes in depression. Proc Natl Acad Sci USA 106(6):1942-1947.
23. Grimm S, et al. (2009) Altered negative BOLD responses in the default-mode network during emotion processing in depressed subjects. Neuropsychopharmacology 34(4): 932-943.
24. Alcaro A, Panksepp J, Witczak J, Hayes DJ, Northoff G (2010) Is subcortical-cortical midline activity in depression mediated by glutamate and GABA? A cross-species translational approach. Neurosci Biobehav Rev 34(4):592-605.
25. Angst J, et al. (2013) Evidence-based definitions of bipolar-I and bipolar-II disorders among 5,635 patients with major depressive episodes in the Bridge Study: Validity and comorbidity. Eur Arch Psychiatry Clin Neurosci 263(8):663-673.
26. Cassano GB, et al. (2012) The role of psychomotor activation in discriminating unipolar from bipolar disorders: A classification-tree analysis. J Clin Psychiatry 73(1): 22-28.
27. Kaiser RH, Andrews-Hanna JR, Wager TD, Pizzagalli DA (2015) Large-scale network dysfunction in major depressive disorder: A meta-analysis of resting-state functional connectivity. JAMA Psychiatry 72(6):603-611.
28. Northoff G (2015) Is schizophrenia a spatiotemporal disorder of the brain's resting state? World Psychiatry 14(1):34-35.
29. Karbasforoushan H, Woodward ND (2012) Resting-state networks in schizophrenia. Curr Top Med Chem 12(21):2404-2414.
30. Deco G, Kringelbach ML (2014) Great expectations: Using whole-brain computational connectomics for understanding neuropsychiatric disorders. Neuron 84(5):892-905.
31. Yang GJ, et al. (2014) Altered global brain signal in schizophrenia. Proc Natl Acad Sci USA 111(20):7438-7443.
32. Uddin LQ, Kelly AM, Biswal BB, Castellanos FX, Milham MP (2009) Functional connectivity of default mode network components: Correlation, anticorrelation, and causality. Hum Brain Mapp 30(2):625-637.
33. Seeley WW, et al. (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349-2356.
34. Carhart-Harris RL, et al. (2013) Functional connectivity measures after psilocybin inform a novel hypothesis of early psychosis. Schizophr Bull 39(6):1343-1351.
35. Zuo XN, et al. (2010) The oscillating brain: Complex and reliable. Neuroimage 49(2): 1432-1445.
36. Zang YF, et al. (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 29(2):83-91.
37. Garrett DD, Kovacevic N, McIntosh AR, Grady CL (2010) Blood oxygen level-dependent signal variability is more than just noise. J Neurosci 30(14):4914-4921.
38. Garrett DD, Kovacevic N, McIntosh AR, Grady CL (2011) The importance of being variable. J Neurosci 31(12):4496-4503.
39. Garrett DD, McIntosh AR, Grady CL (2014) Brain signal variability is parametrically modifiable. Cereb Cortex 24(11):2931-2940.
40. Garrett DD, et al. (2013) Moment-to-moment brain signal variability: A next frontier in human brain mapping? Neurosci Biobehav Rev 37(4):610-624.
41. Zou QH, et al. (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF. J Neurosci Methods 172(1): 137-141.
42. Basalyga G, Salinas E (2006) When response variability increases neural network robustness to synaptic noise. Neural Comput 18(6):1349-1379.
43. Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9(4):292-303.
44. Lugo E, Doti R, Faubert J (2008) Ubiquitous crossmodal stochastic resonance in humans: Auditory noise facilitates tactile, visual and proprioceptive sensations. PLoS One 3(8):e2860.
45. Ward LM (2003) Synchronous neural oscillations and cognitive processes. Trends Cogn Sci 7(12):553-559.
46. Han Y, et al. (2011) Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: A resting-state fMRI study. Neuroimage 55(1):287-295.
47. Xi Q, et al. (2012) Spontaneous brain activity in mild cognitive impairment revealed by amplitude of low-frequency fluctuation analysis: A resting-state fMRI study. Radiol Med (Torino) 117(5):865-871.
48. Raja Beharelle A, Kovacevi-c N, McIntosh AR, Levine B (2012) Brain signal variability relates to stability of behavior after recovery from diffuse brain injury. Neuroimage 60(2):1528-1537.
49. Huang Z, et al. (2014) The self and its resting state in consciousness: An investigation of the vegetative state. Hum Brain Mapp 35(5):1997-2008.
50. Huang Z, et al. (2014) Altered temporal variance and neural synchronization of spontaneous brain activity in anesthesia. Hum Brain Mapp 35(11):5368-5378.
51. Hoptman MJ, et al. (2010) Amplitude of low-frequency oscillations in schizophrenia: A resting state fMRI study. Schizophr Res 117(1):13-20.
52. Fernández A, Gómez C, Hornero R, López-Ibor JJ (2013) Complexity and schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 45:267-276.
53. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926-1929.
54. Balduzzi D, Riedner BA, Tononi G (2008) A BOLD window into brain waves. Proc Natl Acad Sci USA 105(41):15641-15642.
55. Zou Q, Wu CW, Stein EA, Zang Y, Yang Y (2009) Static and dynamic characteristics of cerebral blood flow during the resting state. Neuroimage 48(3):515-524.
56. Lee TW, Northoff G, Wu YT (2014) Resting network is composed of more than one neural pattern: An fMRI study. Neuroscience 274:198-208.
57. Xue SW, Li D, Weng XC, Northoff G, Li DW (2014) 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 4(4): 242-255.
58. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700-711.
59. Zhang D, Raichle ME (2010) Disease and the brain's dark energy. Nat Rev Neurol 6(1): 15-28.
60. Northoff G, et al. (2006) Self-referential processing in our brain-A meta-analysis of imaging studies on the self. Neuroimage 31(1):440-457.
61. Northoff G (2014) Unlocking the Brain (Oxford Univ Press, New York).
62. Northoff G (2014) How is our self altered in psychiatric disorders? A neurophenomenal approach to psychopathological symptoms. Psychopathology 47(6): 365-376.
63. Liu CH, et al. (2012) Regional homogeneity within the default mode network in bipolar depression: A resting-state functional magnetic resonance imaging study. PLoS One 7(11):e48181.
64. Fountoulakis KN, Giannakopoulos P, Kövari E, Bouras C (2008) Assessing the role of cingulate cortex in bipolar disorder: Neuropathological, structural and functional imaging data. Brain Res Brain Res Rev 59(1):9-21.
65. Savitz JB, Rauch SL, Drevets WC (2013) Clinical application of brain imaging for the diagnosis of mood disorders: The current state of play. Mol Psychiatry 18(5):528-539.
66. Chai XJ, et al. (2011) Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia. Neuropsychopharmacology 36(10):2009-2017.
67. Baker JT, et al. (2014) Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. JAMA Psychiatry 71(2):109-118.
68. Wu M, et al. (2013) Altered affective, executive and sensorimotor resting state networks in patients with pediatric mania. J Psychiatry Neurosci 38(4):232-240.
69. Knyazev GG (2007) Motivation, emotion, and their inhibitory control mirrored in brain oscillations. Neurosci Biobehav Rev 31(3):377-395.
70. He BJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME (2008) Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc Natl Acad Sci USA 105(41):16039-16044.
71. Duff EP, et al. (2008) The power of spectral density analysis for mapping endogenous BOLD signal fluctuations. Hum Brain Mapp 29(7):778-790.
72. Fransson P (2006) How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations. Neuropsychologia 44(14):2836-2845.
73. Cordes D, et al. (2001) Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am J Neuroradiol 22(7):1326-1333.
74. Gotts SJ, et al. (2013) The perils of global signal regression for group comparisons: A case study of autism spectrum disorders. Front Hum Neurosci 7:356.
75. Saad ZS, et al. (2012) Trouble at rest: How correlation patterns and group differences become distorted after global signal regression. Brain Connect 2(1):25-32.
76. Sheehan DV, et al. (1998) 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 59(Suppl 20):22-33, quiz 34-57.
77. Ventura J, Liberman RP, Green MF, Shaner A, Mintz J (1998) Training and quality assurance with the Structured Clinical Interview for DSM-IV (SCID-I/P). Psychiatry Res 79(2):163-173.
78. First MB, et al. (1994) Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II). Version 2.0 (Biometrics Research Deprtment, New York State Psychiatric Institute, New York).
79. Cassano GB, et al. (1989) Psychopathology, temperament, and past course in primary major depressions. 2. Toward a redefinition of bipolarity with a new semistructured interview for depression. Psychopathology 22(5):278-288.
80. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23: 56-62.
81. Young RC, Biggs JT, Ziegler VE, Meyer DA (1978) A rating scale for mania: Reliability, validity and sensitivity. Br J Psychiatry 133:429-435.
82. Cox RW (1996) AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162-173.
83. Talairach J, Tournoux P (1988) Co-Planar Stereotaxic Atlas of the Human Brain (Thieme Medical Publishers, New York).
84. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4): 537-541.
85. Laird AR, et al. (2009) Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J Neurosci 29(46):14496-14505.
86. Göttlich M, et al. (2013) Altered resting state brain networks in Parkinson's disease. PLoS One 8(10):e77336.
87. Qin P, Northoff G (2011) How is our self related to midline regions and the defaultmode network? Neuroimage 57(3):1221-1233.
88. Shafer AB (2006) Meta-analysis of the factor structures of four depression questionnaires: Beck, CES-D, Hamilton, and Zung. J Clin Psychol 62(1):123-146.
89. Hanwella R, de Silva VA (2011) Signs and symptoms of acute mania: A factor analysis. BMC Psychiatry 11:137.
90. Phillips ML, Travis MJ, Fagiolini A, Kupfer DJ (2008) Medication effects in neuroimaging studies of bipolar disorder. Am J Psychiatry 165(3):313-320.
91. Baldessarini RJ (2013) Chemotherapy in Psychiatry. Pharmacologic Basis of Treatments of Major Mental Illness (Springer, New York), 3rd Ed.
92. Arana GW, Rosenbaum JF (2000) Handbook of Psychiatric Drug Therapy, 4th Ed (Lippincott, Williams and Wilkins, Philadelphia, PA).
93. Davis JM, Chen N (2004) Dose response and dose equivalence of antipsychotics. J Clin Psychopharmacol 24(2):192-208.