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Detection of Functional Homotopy in Traumatic Axonal Injury

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objective

This study aimed to explore the interhemispheric intrinsic connectivity in traumatic axonal injury (TAI) patients.

Methods

Twenty-one patients with TAI (14 males, seven females; mean age, 38.71 ± 15.25 years) and 22 well-matched healthy controls (16 males, six females; mean age, 38.50 ± 13.82 years) were recruited, and from them we obtained resting-state fMRI data. Interhemispheric coordination was examined using voxel-mirrored homotopic connectivity (VMHC) and seed-based functional connectivity analysis was performed.

Results

We observed significantly decreased VMHC in a number of regions in TAI patients, including the prefrontal, temporal, occipital, parietal, and posterior cingulate cortices, thalami and cerebellar posterior lobes. Subsequent seed-based functional connectivity analysis revealed widely disrupted functional connectivity between the regions of local homotopic connectivity deficits and other areas of the brain, particularly the areas subserving the default, salience, integrative, and executive systems. The lower VMHC of the inferior frontal gyrus and basal ganglia, thalamus, and caudate were significant correlated with the Beck Depression Inventory score, Clinical Dementia Rating score, and Mini-Mental State Examination score, respectively.

Conclusion

TAI is associated with regionally decreased interhemispheric interactions and extensively disrupted seed-based functional connectivity, generating further evidence of diffuse disconnection being associated with clinical symptoms in TAI patients.

Key Points

Traumatic axonal injury is associated with decreased interhemispheric connectivity

Traumatic axonal injury couples with widely disrupted functional connectivity

These alterations support the default, salience, integrative, and executive functions

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Abbreviations

TAI:

Traumatic axonal injury

TBI:

Traumatic brain injury

VMHC:

Voxel-mirrored homotopic connectivity

FMRI:

Functional magnetic resonance imaging

FC:

Functional connectivity

MMSE:

Mini-Mental State Examination

DRS:

Disability Rating Scale

BDI:

Beck Depression Inventory

MAS:

Motor Assessment Scale

ABS:

Adaptive Behavior Scale

HAMA:

Hamilton Anxiety Scale

CDR:

Clinical Dementia Rating

ADL:

Activity of Daily Living Scale

References

  1. Roozenbeek B, Maas AI, Menon DK (2013) Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol 9:231–236

    Article  PubMed  Google Scholar 

  2. Faul MX, Wald L, Coronado MM. VG (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002-2006. Atlanta Centers for Disease Control and Prevention. National Center for Injury Prevention and Control:1-71.

  3. Chen AJ, D’Esposito M (2010) Traumatic brain injury: from bench to bedside to society. Neuron 66:11–14

    Article  CAS  PubMed  Google Scholar 

  4. Scheid R, Walther K, Guthke T et al (2006) Cognitive sequelae of diffuse axonal injury. Arch Neurol 63:418–424

    Article  PubMed  Google Scholar 

  5. Niogi SN, Mukherjee P, Ghajar J et al (2008) Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am J Neuroradiol 29:967–973

    Article  CAS  PubMed  Google Scholar 

  6. Rutgers DR, Fillard P, Paradot G et al (2008) Diffusion tensor imaging characteristics of the corpus callosum in mild, moderate, and severe traumatic brain injury. Am J Neuroradiol 29:1730–1735

    Article  CAS  PubMed  Google Scholar 

  7. Bendlin BB, Ries ML, Lazar M et al (2008) Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage 42:503–514

    Article  PubMed  PubMed Central  Google Scholar 

  8. Palacios EM, Sala-Llonch R, Junque C et al (2013) Long-term declarative memory deficits in diffuse TBI: correlations with cortical thickness, white matter integrity and hippocampal volume. Cortex 49:646–657

    Article  PubMed  Google Scholar 

  9. Biswal B, Yetkin FZ, Haughton VM et al (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541

    Article  CAS  PubMed  Google Scholar 

  10. Stevens MC, Lovejoy D, Kim J et al (2012) Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury. Brain Imaging Behav 6:293–318

    Article  PubMed  Google Scholar 

  11. Pandit AS, Expert P, Lambiotte R et al (2013) Traumatic brain injury impairs small-world topology. Neurology 80:1826–1833

    Article  PubMed  PubMed Central  Google Scholar 

  12. Palacios EM, Sala-Llonch R, Junque C et al (2013) Resting-state functional magnetic resonance imaging activity and connectivity and cognitive outcome in traumatic brain injury. JAMA Neurol 70:845–851

    Article  PubMed  Google Scholar 

  13. Tyszka JM, Kennedy DP, Adolphs R et al (2011) Intact bilateral resting-state networks in the absence of the corpus callosum. J Neurosci 31:15154–15162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zuo XN, Kelly C, Di Martino A et al (2010) Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci 30:15034–15043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Adams JH, Doyle D, Ford I et al (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15:49–59

    Article  CAS  PubMed  Google Scholar 

  16. Teasdale G, Murray G, Parker L et al (1979) Adding up the Glasgow Coma Score. Acta Neurochir Suppl (Wien) 28:13–16

    CAS  Google Scholar 

  17. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  18. Rappaport M, Hall KM, Hopkins K et al (1982) Disability rating scale for severe head trauma: coma to community. Arch Phys Med Rehabil 63:118–123

    CAS  PubMed  Google Scholar 

  19. Beck AT, Steer RA, Carbin MG (1988) Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clin Psychol Rev 8:77–100

    Article  Google Scholar 

  20. Carr JH, Shepherd RB, Nordholm L et al (1985) Investigation of a new motor assessment scale for stroke patients. Phys Ther 65:175–180

    CAS  PubMed  Google Scholar 

  21. Sparrow SS, Cicchetti DV (1985) Diagnostic uses of the Vineland Adaptive Behavior Scales. J Pediatr Psychol 10:215–225

    Article  CAS  PubMed  Google Scholar 

  22. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43:2412–2414

    Article  CAS  PubMed  Google Scholar 

  24. Nouri FM, Lincoln NB (1987) An extended activities of daily living scale for stroke patients. Clin Rehabil 1:301–305

    Article  Google Scholar 

  25. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839–851

    Article  PubMed  Google Scholar 

  26. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113

    Article  PubMed  Google Scholar 

  27. Yan CG, Cheung B, Kelly C et al (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76:183–201

    Article  PubMed  PubMed Central  Google Scholar 

  28. Friston KJ, Williams S, Howard R et al (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346–355

    Article  CAS  PubMed  Google Scholar 

  29. Satterthwaite TD, Elliott MA, Gerraty RT et al (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240–256

    Article  PubMed  Google Scholar 

  30. Jenkinson M, Bannister P, Brady M et al (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841

    Article  PubMed  Google Scholar 

  31. Stark DE, Margulies DS, Shehzad ZE, et al (2008) Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. In: 13754-64

  32. Werner C, Engelhard K (2007) Pathophysiology of traumatic brain injury. Br J Anaesth 99:4–9

    Article  CAS  PubMed  Google Scholar 

  33. Seeley WW, Crawford RK, Zhou J et al (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kinnunen KM, Greenwood R, Powell JH et al (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134:449–463

    Article  PubMed  Google Scholar 

  35. Caeyenberghs K, Leemans A, Leunissen I et al (2014) Altered structural networks and executive deficits in traumatic brain injury patients. Brain Struct Funct 219:193–209

    Article  CAS  PubMed  Google Scholar 

  36. Christodoulou C, DeLuca J, Ricker JH et al (2001) Functional magnetic resonance imaging of working memory impairment after traumatic brain injury. J Neurol Neurosurg Psychiatry 71:161–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nakayama N, Okumura A, Shinoda J et al (2006) Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. J Neurol Neurosurg Psychiatry 77:850–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kurth F, Zilles K, Fox PT et al (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534

    Article  PubMed  PubMed Central  Google Scholar 

  39. Tollard E, Galanaud D, Perlbarg V et al (2009) Experience of diffusion tensor imaging and 1H spectroscopy for outcome prediction in severe traumatic brain injury: preliminary results. Crit Care Med 37:1448–1455

    Article  PubMed  Google Scholar 

  40. Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bonnelle V, Ham TE, Leech R et al (2012) Salience network integrity predicts default mode network function after traumatic brain injury. Proc Natl Acad Sci U S A 109:4690–4695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci U S A 105:12569–12574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Arenivas A, Diaz-Arrastia R, Spence J et al (2014) Three approaches to investigating functional compromise to the default mode network after traumatic axonal injury. Brain Imaging Behav 8:407–419

    Article  PubMed  Google Scholar 

  44. Bonnelle V, Leech R, Kinnunen KM et al (2011) Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci 31:13442–13451

    Article  CAS  PubMed  Google Scholar 

  45. Ariza M, Serra-Grabulosa JM, Junque C et al (2006) Hippocampal head atrophy after traumatic brain injury. Neuropsychologia 44:1956–1961

    Article  PubMed  Google Scholar 

  46. de la Plata CDM, Garces J, Kojori ES et al (2011) Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury. Arch Neurol 68:74–84

    Google Scholar 

  47. Slobounov SM, Gay M, Zhang K et al (2011) Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study. Neuroimage 55:1716–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Dal Monte O, Schintu S, Pardini M et al (2014) The left inferior frontal gyrus is crucial for reading the mind in the eyes: brain lesion evidence. Cortex 58:9–17

    Article  PubMed  Google Scholar 

  49. McDonald S, Flanagan S (2004) Social perception deficits after traumatic brain injury: interaction between emotion recognition, mentalizing ability, and social communication. Neuropsychology 18:572–579

    Article  PubMed  Google Scholar 

  50. Witt ST, Lovejoy DW, Pearlson GD et al (2010) Decreased prefrontal cortex activity in mild traumatic brain injury during performance of an auditory oddball task. Brain Imaging Behav 4:232–247

    Article  PubMed  Google Scholar 

  51. Little DM, Kraus MF, Joseph J et al (2010) Thalamic integrity underlies executive dysfunction in traumatic brain injury. Neurology 74:558–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Garcia-Panach J, Lull N, Lull JJ et al (2011) A voxel-based analysis of FDG-PET in traumatic brain injury: regional metabolism and relationship between the thalamus and cortical areas. J Neurotrauma 28:1707–1717

    Article  PubMed  Google Scholar 

  53. Gale SD, Baxter L, Roundy N et al (2005) Traumatic brain injury and grey matter concentration: a preliminary voxel based morphometry study. J Neurol Neurosurg Psychiatry 76:984–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Jones DT, Mateen FJ, Lucchinetti CF et al (2011) Default mode network disruption secondary to a lesion in the anterior thalamus. Arch Neurol 68:242–247

    Article  PubMed  Google Scholar 

  55. Tang L, Ge Y, Sodickson DK et al (2011) Thalamic resting-state functional networks: disruption in patients with mild traumatic brain injury. Radiology 260:831–840

    Article  PubMed  PubMed Central  Google Scholar 

  56. Grossman EJ, Inglese M (2016) The Role of Thalamic Damage in Mild Traumatic Brain Injury. J Neurotrauma 33:163–167

    Article  PubMed  Google Scholar 

  57. Marchand WR, Lee JN, Suchy Y et al (2012) Aberrant functional connectivity of cortico-basal ganglia circuits in major depression. Neurosci Lett 514:86–90

    Article  CAS  PubMed  Google Scholar 

  58. Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication. Brain 123:1293–1326

    Article  PubMed  Google Scholar 

  59. Quigley M, Cordes D, Turski P et al (2003) Role of the corpus callosum in functional connectivity. Am J Neuroradiol 24:208–212

    PubMed  Google Scholar 

  60. Treble A, Hasan KM, Iftikhar A et al (2013) Working memory and corpus callosum microstructural integrity after pediatric traumatic brain injury: a diffusion tensor tractography study. J Neurotrauma 30:1609–1619

    Article  PubMed  PubMed Central  Google Scholar 

  61. Arenth PM, Russell KC, Scanlon JM et al (2014) Corpus callosum integrity and neuropsychological performance after traumatic brain injury: a diffusion tensor imaging study. J Head Trauma Rehabil 29:E1–E10

    Article  PubMed  PubMed Central  Google Scholar 

  62. Uddin LQ, Mooshagian E, Zaidel E et al (2008) Residual functional connectivity in the split-brain revealed with resting-state functional MRI. Neuroreport 19:703–709

    Article  PubMed  PubMed Central  Google Scholar 

  63. Saindane AM, Law M, Ge Y et al (2007) Correlation of diffusion tensor and dynamic perfusion MR imaging metrics in normal-appearing corpus callosum: support for primary hypoperfusion in multiple sclerosis. AJNR Am J Neuroradiol 28:767–772

    CAS  PubMed  Google Scholar 

  64. Hubbard NA, Turner M, Hutchison JL et al (2015) Multiple sclerosis-related white matter microstructural change alters the BOLD hemodynamic response. J Cereb Blood Flow Metab

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Acknowledgments

The scientific guarantor of this publication is Honghan Gong. The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article. This study has received funding by the National Natural Science Foundations of China (81260217 and 81460263). One of the authors (Lei Gao) has significant statistical expertise. Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Methodology: retrospective, cross sectional study, performed at one institution.

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Correspondence to Lei Gao.

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Jian Li and Lei Gao contributed equally to this work.

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Li, J., Gao, L., Xie, K. et al. Detection of Functional Homotopy in Traumatic Axonal Injury. Eur Radiol 27, 325–335 (2017). https://doi.org/10.1007/s00330-016-4302-x

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  • DOI: https://doi.org/10.1007/s00330-016-4302-x

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