Specific and Evolving Resting-State Network Alterations in Post-Concussion Syndrome Following Mild Traumatic Brain Injury

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Messé, Arnaud ^a,b   Caplain, Sophie ^c   Pélégrini Issac, Mélanie ^a,b   Blancho, Sophie ^d   Lévy, Richard ^a,e   Aghakhani, Nozar ^f   Montreuil, Michèle ^c   Benali, Habib ^a,b,g   Lehéricy, Stéphane ^a,b,h  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c EA 2027   (France)

^d Institut Pour La Recherche Sur La Moelle Epinière Et L Encéphale IRME   (France)

^e HÔPITAL SAINT ANTOINE   (France)

^f BICÊTRE HOSPITAL   (France)

^g UNIVERSITÉ DE MONTRÉAL   (Canada)

^h SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANALYTIC METHOD; ARTICLE; BRAIN FUNCTION; BRAIN REGION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAPH THEORY ANALYSIS; HUMAN; MAJOR CLINICAL STUDY; MALE; POSTCONCUSSION SYNDROME; RESTING STATE NETWORK; TEMPORAL CORTEX; THALAMUS; TRAUMATIC BRAIN INJURY; BRAIN; BRAIN INJURY; COMPLICATION; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; POST-CONCUSSION SYNDROME;

ADULT; BRAIN; BRAIN INJURIES; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; POST-CONCUSSION SYNDROME;

EID: 84878805217     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065470     Document Type: Article

References (69)

1. Dikmen S, McLean A, Temkin N, (1986) Neuropsychological and psychosocial consequences of minor head injury. Journal of Neurology, Neurosurgery, and Psychiatry 46: 1227-32.
2. Levin HS, Mattis S, Ruff RM, Eisenberg HM, Marshall LF, et al. (1987) Neurobehavioral outcome following minor head injury: a three-center study. Journal of Neurosurgery 66: 234-43.
3. Iverson GL, (2005) Outcome from mild traumatic brain injury. Current Opinion in Psychiatry 18: 301-17.
4. Stålnacke BM, Björnstig U, Karlsson K, Sojka P, (2005) One-year follow-up of mild traumatic brain injury: post-concussion symptoms, disabilities and life satisfaction in relation to serum levels of S-100B and neurone-specific enolase in acute phase. Journal of Rehabilitation Medicine 37: 300-5.
5. Willer B, Leddy JJ, (2006) Management of concussion and post-concussion syndrome. Current Treatment Options in Neurology 8: 415-26.
6. von Wild KR, (2008) Posttraumatic rehabilitation and one year outcome following acute traumatic brain injury (TBI): data from the well defined population based German Prospective Study 2000-2002. Acta Neurochirurgica 101: 55-60.
7. Bazarian J, Zhong J, Blyth B, Zhu T, Kavcic V, et al. (2007) Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. Journal of Neurotrauma 24: 1447-59.
8. Smits M, Houston GC, Dippel DW, Wielopolski PA, Vernooij MW, et al. (2011) Microstructural brain injury in post-concussion syndrome after minor head injury. Neuroradiology 53: 553-63.
9. Messé A, Caplain S, Paradot G, Garrigue D, Mineo JF, et al. (2011) Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Human Brain Mapping 32: 999-1011.
10. Messé A, Caplain S, Pélégrini-Issac M, Blancho S, Montreuil M, et al. (2012) Structural integrity and post-concussion syndrome in mild traumatic brain injury patients. Brain Imaging and Behavior 6: 283-92.
11. Varela F, Lachaux JP, Rodriguez E, Martinerie J, (2001) The brainweb: Phase synchronization and large-scale integration. Nature Review Neurosciences 2: 229-39.
12. Bressler SL, Tognoli E, (2006) Operational principles of neurocognitive networks. International Journal of Psychophysiology 60: 139-48.
13. Logothetis NK, Wandell BA, (2004) Interpreting the BOLD signal. Annual Review of Neurophysiology 66: 735-69.
14. Fox M, Raichle ME, (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Review Neurosciences 8: 700-11.
15. Biswal B, Mennes M, Zuo XN, Gohel S, Kelly C, et al. (2010) Toward discovery science of human brain function. Proceedings of the National Academy of Sciences of the United States of America 107: 4734-9.
16. Raichle ME, (2011) The restless brain. Brain Connectivity 1: 1-12.
17. Sporns O (2011) Networks of the Brain. Cambridge, Massachusetts, United States: MIT Press.
18. Bullmore E, Sporns O, (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Review Neurosciences 10: 186-98.
19. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey C, et al. (2008) Mapping the structural core of human cerebral cortex. PLoS Biology 6: e159.
20. Reijneveld JC, Ponten SC, Berendse HW, Stam CJ, (2007) The application of graph theoretical analysis to complex networks in the brain. Clinical Neurophysiology 118: 2317-31.
21. Sporns O, Honey C, (2006) Small worlds inside big brains. Proceedings of the National Academy of Sciences of the United States of America 103: 19219-20.
22. van den Heuvel M, Sporns O, (2011) Rich-club organization of the human connectome. The Journal of Neuroscience 31: 15775-86.
23. Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Computational Biology 1: e42+.
24. Kaiser M, Hilgetag C, (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Computational Biology 2: e95.
25. Johnson B, Zhang K, Gay M, Horovitz S, Hallett M, et al. (2012) Alteration of brain default network in subacute phase of injury in concussed individuals: Resting-state fMRI study. Neuroimage 59: 511-8.
26. Slobounov S, Gay M, Zhang K, Johnson B, Pennell D, et al. (2011) Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study. Neuroimage 55: 1716-27.
27. Marquez de la Plata CD, Garces J, Shokri Kojori E, Grinnan J, Krishnan K, et al. (2011) Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury. Archives of Neurology 68: 74-84.
28. Sharp DJ, Beckmann CF, Greenwood R, Kinnunen KM, Bonnelle V, et al. (2011) Default mode network functional and structural connectivity after traumatic brain injury. Brain 134: 2233-47.
29. Vanhaudenhuyse A, Noirhomme Q, Tshibanda L, Bruno MA, Boveroux P, et al. (2010) Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133: 161-71.
30. Nakamura T, Hillary F, Biswal B, (2009) Resting network plasticity following brain injury. PLoS ONE 4: e8220.
31. Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA, (2011) Functional connectivity in mild traumatic brain injury. Human Brain Mapping 32: 1825-35.
32. Kay T, Harrington DE, Adams R, Anderson T, Berrol S, et al. (1993) Definition of mild traumatic brain injury. Journal of Head Trauma Rehabilitation 8: 86-87 (Head Injury Interdisciplinary Special Interest Group of the American Congress of Rehabilitation Medicine).
33. GREFEX (2001) [Groupe de réflexion sur l'évaluation des fonctions exécutives]. Revue de Neuropsychologie 11: 383-434 (in French).
34. DSM-IV (1994) Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR Fourth Edition (Text Revision) Washington, DC: American Psychiatric Association (APA).
35. Legome E (2006) Post-concussion syndrome. Retrieved from eMedicine.com.
36. King NS, Crawford S, Wenden FJ, Moss NEG, Wade DT, (1995) The Rivermead Post Concussion Symptoms Questionnaire: a measure of symptoms commonly experienced after head injury and its reliability. Journal of Neurology 242: 587-92.
37. 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: 273-89.
38. Fox M, Zhang D, Snyder A, Raichle M, (2009) The global signal and observed anticorrelated resting state brain networks. Journal of Neurophysiology 101: 3270-83.
39. van Dijk K, Hedden T, Venkataraman A, Evans K, Lazar S, et al. (2010) Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization. Journal of Neurophysiology 103: 297-321.
40. Benjamini Y, Yekutieli D, (2001) The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics 29: 1165-88.
41. Rubinov M, Sporns O, (2010) Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 52: 1059-69.
42. Bassett DS, Brown JA, Deshpande V, Carlson JM, Grafton ST, (2011) Conserved and variable architecture of human white matter connectivity. Neuroimage 54: 1262-79.
43. Lynall ME, Bassett D, Kerwin R, McKenna P, Kitzbichler M, et al. (2010) Functional connectivity and brain networks in schizophrenia. The Journal of Neuroscience 30: 9477-87.
44. Humphries M, Gurney K, (2008) Network 'small-world-ness': A quantitative method for determining canonical network equivalence. PLoS ONE 3: e0002051.
45. Latora V, Marchiori M, (2001) Efficient behavior of small-world networks. Physical Review Letters 87: 198701-4.
46. Newman MEJ, (2006) Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America 103: 8577-82.
47. Ravasz E, Barabási AL, (2003) Hierarchical organization in complex networks. Physical Review E 67: 026112.
48. Freeman L, (1977) A set of measures of centrality based on betweenness. Sociometry 40: 35-41.
49. 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. The Journal of Neuroscience 26: 63-72.
50. Watts DJ, Strogatz SH, (1998) Collective dynamics of 'small-world' networks. Nature 393: 440-2.
51. Bassett D, Greenfield D, Meyer Lindenberg A, Weinberger D, Moore S, Bullmore E, (2010) Efficient physical embedding of topologically complex information processing networks in brains and computer circuits. PLoS Computational Biology 6: e1000748.
52. Ginestet CE, Nichols TE, Bullmore ET, Simmons A, (2011) Brain network analysis: separating cost from topology using cost-integration. PLoS ONE 6: e21570.
53. Zalesky A, Cocchi L, Fornito A, Murray M, Bullmore E, (2012) Connectivity differences in brain networks. Neuroimage 60: 1055-62.
54. Irimia A, Chambers MC, Torgerson CM, van Horn JD, (2012) Circular representation of human cortical networks for subjects and population-level connectomic visualization. Neuroimage 60: 1340-51.
55. Xia M, Wang J, He YY (2011) Brainnet viewer: A graph-based brain network mapping tool. In Proceedings of the 17th international conference on functional mapping of the human brain. Québec, Canada.
56. Hou R, Moss-Morris R, Peveler R, Mogg K, Bradley B, et al. (2011) When a minor injury results in ending symptoms: a prospective investigation of risk factors for postconcussional syndrome after mild traumatic brain injury. Journal of Neurology, Neurosurgery, and Psychiatry 83: 217-23.
57. Shumskaya E, Andriessen TM, Norris DG, Vos PE, (2012) Abnormal whole-brain functional networks in homogeneous acute mild traumatic brain injury. Neurology 79: 175-82.
58. Tang L, Sodickson DK, Zhou Y, Reaume J, Grossman RI, (2011) Thalamic resting-state functional networks: disruption in patients with mild traumatic brain injury. Radiology 260: 831-40.
59. Evans RW, (1992) The post-concussion syndrome and the sequelae of mild head injury. Clinical Neurology 10: 815-47.
60. Hall RCW, Hall RCW, Chapman MJ, (2005) Definition, diagnosis, and forensic implications of post-concussional syndrome. Psychosomatics 46: 195-202.
61. Bigler ED, Bazarian J, (2010) Diffusion tensor imaging: A biomarker for mild traumatic brain injury? Neurology 74: 626-7.
62. Niogi S, Mukherjee P, (2010) Diffusion tensor imaging of mild traumatic brain injury. The Journal of Head Trauma Rehabilitation 25: 241-55.
63. Fitzgerald DB, Crosson BA, (2011) Diffusion weighted imaging and neuropsychological correlates in adults with mild traumatic brain injury. International Journal of Psychophysiology 82: 79-85.
64. Schwartz AJ, McGonigle J, (2011) Negative edges and soft thresholding in complex network analysis of resting state functional connectivity data. Neuroimage 55: 1132-46.
65. Bassett DS, Nelson BG, Mueller BA, Camchong J, Lim KO, (2012) Altered resting state complexity in schizophrenia. Neuroimage 59: 2196-207.
66. Wilde EA, Whiteneck GG, Bogner J, Bushnik T, Cifu DX, et al. (2010) Recommendations for the use of common outcome measures in traumatic brain injury research. Archives of Physical Medicine and Rehabilitation 91: 1650-60.
67. Boake C, McCauley SR, Levin HS, Pedroza C, Contant CF, et al. (2005) Diagnostic criteria for post-concussional syndrome after mild to moderate traumatic brain injury. Journal of Neuropsychiatry and Clinical Neurosciences 17: 350-6.
68. Sandrone S, Bacigaluppi M, (2012) Learning from default mode network: The predictive value of resting state in traumatic brain injury. The Journal of Neuroscience 32: 1915-7.
69. Sandrone S, (2012) The brain as a crystal ball: the predictive potential of default mode network. Frontiers in Human Neuroscience 6: 261.