Scale-free functional connectivity of the brain is maintained in anesthetized healthy participants but not in patients with unresponsive wakefulness syndrome

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Liu, Xiaolin ^a   Ward, B Douglas ^a   Binder, Jeffrey R ^a   Li, Shi Jiang ^a   Hudetz, Anthony G ^b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Department of Neurology Medical College of Wisconsin ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROPOFOL;

ADAPTATION; ADULT; ANESTHESIA; ANESTHETIC RECOVERY; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN SCALE FREE FUNCTIONAL CONNECTIVITY; CLINICAL ARTICLE; COMPUTER MODEL; CONNECTOME; CONSCIOUSNESS DISORDER; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; MALE; MIDDLE AGED; NERVE CELL NETWORK; NEUROANATOMY; TIME SERIES ANALYSIS; UNRESPONSIVE WAKEFULNESS SYNDROME; VOXEL BASED MORPHOMETRY; WAKEFULNESS; YOUNG ADULT; ALGORITHM; BRAIN; CLINICAL TRIAL; CONSCIOUSNESS; DEEP SEDATION; NORMAL HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT; ALGORITHMS; ANESTHESIA; BRAIN; CONSCIOUSNESS; DEEP SEDATION; FEMALE; HEALTHY VOLUNTEERS; HUMANS; MALE; MIDDLE AGED; NERVE NET; WAKEFULNESS; YOUNG ADULT;

EID: 84898623268     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092182     Document Type: Article

References (68)

1. Boveroux P, Vanhaudenhuyse A, Bruno MA, Noirhomme Q, Lauwick S, et al. (2010) Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113: 1038-1053.
2. Laureys S, Faymonville ME, Luxen A, Lamy M, Franck G, et al. (2000) Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet 355: 1790-1791. (Pubitemid 30265088)
3. Laureys S, Owen AM, Schiff ND (2004) Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3: 537-546. (Pubitemid 39485860)
4. White NS, Alkire MT (2003) Impaired thalamocortical connectivity in humans during general-anesthetic-induced unconsciousness. Neuroimage 19: 402-411. (Pubitemid 39665690)
5. Zhou J, Liu X, Song W, Yang Y, Zhao Z, et al. (2011) Specific and nonspecific thalamocortical functional connectivity in normal and vegetative states. Conscious Cogn 20: 257-268.
6. Liu X, Lauer KK, Ward BD, Li SJ, Hudetz AG (2013) Differential effects of deep sedation with propofol on the specific and nonspecific thalamocortical systems: a functional magnetic resonance imaging study. Anesthesiology 118: 59-69.
7. Tononi G, Laureys S (2008) The neurology of consciousness: An overview. In: Laureys S, Tononi G, editors. The Neurology of Consciousness: Cognitive Neuroscience and Neuropathology: Elsevier Ltd.
8. Hudetz AG (2012) General anesthesia and human brain connectivity. Brain Connect 2: 291-302.
9. Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322: 876-880.
10. Bak P, Tang C, Wiesenfeld K (1987) Self-organized criticality: An explanation of the 1/f noise. Phys Rev Lett 59: 381-384.
11. Bak P, Paczuski M (1995) Complexity, contingency, and criticality. Proc Natl Acad Sci U S A 92: 6689-6696.
12. Gisiger T (2001) Scale invariance in biology: coincidence or footprint of a universal mechanism? Biol Rev Camb Philos Soc 76: 161-209.
13. Werner G (2010) Fractals in the nervous system: conceptual implications for theoretical neuroscience. Front Physiol 1: 15.
14. Kello CT, Brown GD, Ferrer ICR, Holden JG, Linkenkaer-Hansen K, et al. (2010) Scaling laws in cognitive sciences. Trends Cogn Sci 14: 223-232.
15. Chialvo DR (2004) Critical brain networks. Physica a-Statistical Mechanics and Its Applications 340: 756-765.
16. Beggs JM (2008) The criticality hypothesis: how local cortical networks might optimize information processing. Philos Transact A Math Phys Eng Sci 366: 329-343.
17. Stam CJ, van Straaten EC (2012) The organization of physiological brain networks. Clin Neurophysiol 123: 1067-1087.
18. Werner G (2007) Brain dynamics across levels of organization. J Physiol Paris 101: 273-279.
19. Beggs JM, Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23: 11167-11177. (Pubitemid 37548953)
20. Fraiman D, Chialvo DR (2012) What kind of noise is brain noise: anomalous scaling behavior of the resting brain activity fluctuations. Front Physiol 3: 307.
21. Kitzbichler MG, Smith ML, Christensen SR, Bullmore E (2009) Broadband criticality of human brain network synchronization. PLoS Comput Biol 5: e1000314.
22. Ribeiro TL, Copelli M, Caixeta F, Belchior H, Chialvo DR, et al. (2010) Spike avalanches exhibit universal dynamics across the sleep-wake cycle. PLoS One 5: e14129.
23. Boonstra TW, He BJ, Daffertshofer A (2013) Scale-free dynamics and critical phenomena in cortical activity. Front Physiol 4: 79.
24. Bassett DS, Meyer-Lindenberg A, Achard S, Duke T, Bullmore E (2006) Adaptive reconfiguration of fractal small-world human brain functional networks. Proc Natl Acad Sci U S A 103: 19518-19523. (Pubitemid 46026063)
25. Stam CJ, de Bruin EA (2004) Scale-free dynamics of global functional connectivity in the human brain. Hum Brain Mapp 22: 97-109. (Pubitemid 38738032)
26. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26: 63-72. (Pubitemid 43090914)
27. Eguiluz VM, Chialvo DR, Cecchi GA, Baliki M, Apkarian AV (2005) Scale-free brain functional networks. Phys Rev Lett 94: 018102.
28. van den Heuvel MP, Stam CJ, Boersma M, Hulshoff Pol HE (2008) Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain. Neuroimage 43: 528-539.
29. Lee U, Oh G, Kim S, Noh G, Choi B, et al. (2010) Brain networks maintain a scale-free organization across consciousness, anesthesia, and recovery: evidence for adaptive reconfiguration. Anesthesiology 113: 1081-1091.
30. Achard S, Delon-Martin C, Vertes PE, Renard F, Schenck M, et al. (2012) Hubs of brain functional networks are radically reorganized in comatose patients. Proc Natl Acad Sci U S A 109: 20608-20613.
31. Tagliazucchi E, Balenzuela P, Fraiman D, Chialvo DR (2012) Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis. Front Physiol 3: 15.
32. Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3: e17.
33. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, 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. (Pubitemid 34852226)
34. Liu X, Lauer KK, Ward BD, Rao SM, Li SJ, et al. (2012) Propofol disrupts functional interactions between sensory and high-order processing of auditory verbal memory. Hum Brain Mapp 33: 2487-2498.
35. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10: 186-198.
36. Meunier D, Lambiotte R, Fornito A, Ersche KD, Bullmore ET (2009) Hierarchical modularity in human brain functional networks. Front Neuroinform 3: 37.
37. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8: 418-425. (Pubitemid 39179905)
38. Kaiser M (2007) Brain architecture: a design for natural computation. Philos Transact A Math Phys Eng Sci 365: 3033-3045.
39. Werner G (2007) Metastability, criticality and phase transitions in brain and its models. Biosystems 90: 496-508.
40. Fiset P, Paus T, Daloze T, Plourde G, Meuret P, et al. (1999) Brain mechanisms of propofol-induced loss of consciousness in humans: a positron emission tomographic study. J Neurosci 19: 5506-5513. (Pubitemid 29300215)
41. Alkire MT, Haier RJ, Shah NK, Anderson CT (1997) Positron emission tomography study of regional cerebral metabolism in humans during isoflurane anesthesia. Anesthesiology 86: 549-557. (Pubitemid 27118337)
42. Laureys S, Lemaire C, Maquet P, Phillips C, Franck G (1999) Cerebral metabolism during vegetative state and after recovery to consciousness. J Neurol Neurosurg Psychiatry 67: 121. (Pubitemid 29278345)
43. Alkire MT, Miller J (2005) General anesthesia and the neural correlates of consciousness. Prog Brain Res 150: 229-244. (Pubitemid 41381556)
44. Laureys S, Goldman S, Phillips C, Van Bogaert P, Aerts J, et al. (1999) Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET. Neuroimage 9: 377-382. (Pubitemid 29369857)
45. Plourde G, Belin P, Chartrand D, Fiset P, Backman SB, et al. (2006) Cortical processing of complex auditory stimuli during alterations of consciousness with the general anesthetic propofol. Anesthesiology 104: 448-457.
46. Laureys S, Faymonville ME, Peigneux P, Damas P, Lambermont B, et al. (2002) Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. Neuroimage 17: 732-741. (Pubitemid 35317007)
47. Davis MH, Coleman MR, Absalom AR, Rodd JM, Johnsrude IS, et al. (2007) Dissociating speech perception and comprehension at reduced levels of awareness. Proc Natl Acad Sci U S A 104: 16032-16037. (Pubitemid 350099355)
48. Perlin K (2002) Improving noise. Acm Transactions on Graphics 21: 681-682.
49. Steyn-Ross ML, Steyn-Ross DA, Sleigh JW (2004) Modelling general anaesthesia as a first-order phase transition in the cortex. Prog Biophys Mol Biol 85: 369-385. (Pubitemid 38629918)
50. Steyn-Ross DA, Steyn-Ross ML (2010) Modeling phase transitions in the brain: Springers New York Dordrecht Heidelberg London.
51. de Reus MA, van den Heuvel MP (2013) The parcellation-based connectome: Limitations and extensions. Neuroimage 80: 397-404.
52. Agnati LF, Santarossa L, Genedani S, Canela EI, Leo G, et al. (2004) On the nested hierarchical organization of CNS: basic characteristics of neuronal molecular organization. In: Erdi P., editor. Cortical Dynamics LNCS 3146: Springer, Berlin. pp. 24-54.
53. Sporns O, Honey CJ, Kotter R (2007) Identification and classification of hubs in brain networks. PLoS One 2: e1049.
54. Zeki S (1978) Functional specialization in the visual cortex of the monkey. Nature 274: 423-428.
55. Schroter MS, Spoormaker VI, Schorer A, Wohlschlager A, Czisch M, et al. (2012) Spatiotemporal reconfiguration of large-scale brain functional networks during propofol-induced loss of consciousness. J Neurosci 32: 12832-12840.
56. Lee H, Mashour GA, Noh GJ, Kim S, Lee U (2013) Reconfiguration of Network Hub Structure after Propofol-induced Unconsciousness. Anesthesiology 119: 1347-1359.
57. Liang Z, King J, Zhang N (2012) Intrinsic organization of the anesthetized brain. J Neurosci 32: 10183-10191.
58. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P (2007) Small-world networks and functional connectivity in Alzheimer's disease. Cereb Cortex 17: 92-99. (Pubitemid 44973898)
59. Sanz-Arigita EJ, Schoonheim MM, Damoiseaux JS, Rombouts SA, Maris E, et al. (2010) Loss of 'small-world' networks in Alzheimer's disease: graph analysis of FMRI resting-state functional connectivity. PLoS One 5: e13788.
60. Boubela RN, Kalcher K, Huf W, Kronnerwetter C, Filzmoser P, et al. (2013) Beyond Noise: Using Temporal ICA to Extract Meaningful Information from High-Frequency fMRI Signal Fluctuations during Rest. Front Hum Neurosci 7: 168.
61. Niazy RK, Xie J, Miller K, Beckmann CF, Smith SM (2011) Spectral characteristics of resting state networks. Prog Brain Res 193: 259-276.
62. Isono M, Wakabayashi Y, Fujiki MM, Kamida T, Kobayashi H (2002) Sleep cycle in patients in a state of permanent unconsciousness. Brain Inj 16: 705-712.
63. Baars BJ (2005) Global workspace theory of consciousness: toward a cognitive neuroscience of human experience. Prog Brain Res 150: 45-53.
64. Tononi G (2004) An information integration theory of consciousness. BMC Neurosci 5: 42.
65. Logothetis NK (2008) What we can do and what we cannot do with fMRI. Nature 453: 869-878.
66. Touboul J, Destexhe A (2010) Can power-law scaling and neuronal avalanches arise from stochastic dynamics? PLoS One 5: e8982.
67. Klaus A, Yu S, Plenz D (2011) Statistical analyses support power law distributions found in neuronal avalanches. PLoS One 6: e19779.
68. Clauset A, Shalizi CR, Newman MEJ (2009) Power-Law Distributions in Empirical Data. Siam Review 51: 661-703.