Skip to main content
Top
Published in: European Radiology 1/2017

01-01-2017 | Magnetic Resonance

Detection of Functional Homotopy in Traumatic Axonal Injury

Authors: Jian Li, Lei Gao, Kai Xie, Jie Zhan, Xiaoping Luo, Huifang Wang, Huifang Zhang, Jing Zhao, Fuqing Zhou, Xianjun Zeng, Laichang He, Yulin He, Honghan Gong

Published in: European Radiology | Issue 1/2017

Login to get access

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
Literature
1.
go back to reference Roozenbeek B, Maas AI, Menon DK (2013) Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol 9:231–236CrossRefPubMed Roozenbeek B, Maas AI, Menon DK (2013) Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol 9:231–236CrossRefPubMed
2.
go back to reference 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. 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.
go back to reference Chen AJ, D’Esposito M (2010) Traumatic brain injury: from bench to bedside to society. Neuron 66:11–14CrossRefPubMed Chen AJ, D’Esposito M (2010) Traumatic brain injury: from bench to bedside to society. Neuron 66:11–14CrossRefPubMed
4.
go back to reference Scheid R, Walther K, Guthke T et al (2006) Cognitive sequelae of diffuse axonal injury. Arch Neurol 63:418–424CrossRefPubMed Scheid R, Walther K, Guthke T et al (2006) Cognitive sequelae of diffuse axonal injury. Arch Neurol 63:418–424CrossRefPubMed
5.
go back to reference 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 29:967–973CrossRefPubMed 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 29:967–973CrossRefPubMed
6.
go back to reference 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 29:1730–1735CrossRefPubMed 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 29:1730–1735CrossRefPubMed
7.
go back to reference 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 42:503–514CrossRefPubMedPubMedCentral 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 42:503–514CrossRefPubMedPubMedCentral
8.
go back to reference 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 49:646–657CrossRefPubMed 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 49:646–657CrossRefPubMed
9.
go back to reference 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 34:537–541CrossRefPubMed 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 34:537–541CrossRefPubMed
10.
go back to reference Stevens MC, Lovejoy D, Kim J et al (2012) Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury. Brain Imaging Behav 6:293–318CrossRefPubMed Stevens MC, Lovejoy D, Kim J et al (2012) Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury. Brain Imaging Behav 6:293–318CrossRefPubMed
12.
go back to reference 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 70:845–851CrossRefPubMed 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 70:845–851CrossRefPubMed
13.
go back to reference Tyszka JM, Kennedy DP, Adolphs R et al (2011) Intact bilateral resting-state networks in the absence of the corpus callosum. J Neurosci 31:15154–15162CrossRefPubMedPubMedCentral Tyszka JM, Kennedy DP, Adolphs R et al (2011) Intact bilateral resting-state networks in the absence of the corpus callosum. J Neurosci 31:15154–15162CrossRefPubMedPubMedCentral
14.
go back to reference 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 30:15034–15043CrossRefPubMedPubMedCentral 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 30:15034–15043CrossRefPubMedPubMedCentral
15.
go back to reference Adams JH, Doyle D, Ford I et al (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15:49–59CrossRefPubMed Adams JH, Doyle D, Ford I et al (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15:49–59CrossRefPubMed
16.
go back to reference Teasdale G, Murray G, Parker L et al (1979) Adding up the Glasgow Coma Score. Acta Neurochir Suppl (Wien) 28:13–16 Teasdale G, Murray G, Parker L et al (1979) Adding up the Glasgow Coma Score. Acta Neurochir Suppl (Wien) 28:13–16
17.
go back to reference 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 12:189–198CrossRefPubMed 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 12:189–198CrossRefPubMed
18.
go back to reference Rappaport M, Hall KM, Hopkins K et al (1982) Disability rating scale for severe head trauma: coma to community. Arch Phys Med Rehabil 63:118–123PubMed Rappaport M, Hall KM, Hopkins K et al (1982) Disability rating scale for severe head trauma: coma to community. Arch Phys Med Rehabil 63:118–123PubMed
19.
go back to reference Beck AT, Steer RA, Carbin MG (1988) Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clin Psychol Rev 8:77–100CrossRef Beck AT, Steer RA, Carbin MG (1988) Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clin Psychol Rev 8:77–100CrossRef
20.
go back to reference Carr JH, Shepherd RB, Nordholm L et al (1985) Investigation of a new motor assessment scale for stroke patients. Phys Ther 65:175–180PubMed Carr JH, Shepherd RB, Nordholm L et al (1985) Investigation of a new motor assessment scale for stroke patients. Phys Ther 65:175–180PubMed
21.
go back to reference Sparrow SS, Cicchetti DV (1985) Diagnostic uses of the Vineland Adaptive Behavior Scales. J Pediatr Psychol 10:215–225CrossRefPubMed Sparrow SS, Cicchetti DV (1985) Diagnostic uses of the Vineland Adaptive Behavior Scales. J Pediatr Psychol 10:215–225CrossRefPubMed
23.
go back to reference Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43:2412–2414CrossRefPubMed Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43:2412–2414CrossRefPubMed
24.
go back to reference Nouri FM, Lincoln NB (1987) An extended activities of daily living scale for stroke patients. Clin Rehabil 1:301–305CrossRef Nouri FM, Lincoln NB (1987) An extended activities of daily living scale for stroke patients. Clin Rehabil 1:301–305CrossRef
26.
27.
go back to reference 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 76:183–201CrossRefPubMedPubMedCentral 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 76:183–201CrossRefPubMedPubMedCentral
28.
go back to reference Friston KJ, Williams S, Howard R et al (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346–355CrossRefPubMed Friston KJ, Williams S, Howard R et al (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346–355CrossRefPubMed
29.
go back to reference 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 64:240–256CrossRefPubMed 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 64:240–256CrossRefPubMed
30.
go back to reference 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 17:825–841CrossRefPubMed 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 17:825–841CrossRefPubMed
31.
go back to reference Stark DE, Margulies DS, Shehzad ZE, et al (2008) Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. In: 13754-64 Stark DE, Margulies DS, Shehzad ZE, et al (2008) Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. In: 13754-64
32.
34.
go back to reference Kinnunen KM, Greenwood R, Powell JH et al (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134:449–463CrossRefPubMed Kinnunen KM, Greenwood R, Powell JH et al (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134:449–463CrossRefPubMed
35.
go back to reference Caeyenberghs K, Leemans A, Leunissen I et al (2014) Altered structural networks and executive deficits in traumatic brain injury patients. Brain Struct Funct 219:193–209CrossRefPubMed Caeyenberghs K, Leemans A, Leunissen I et al (2014) Altered structural networks and executive deficits in traumatic brain injury patients. Brain Struct Funct 219:193–209CrossRefPubMed
36.
go back to reference 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 71:161–168CrossRefPubMedPubMedCentral 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 71:161–168CrossRefPubMedPubMedCentral
37.
go back to reference 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 77:850–855CrossRefPubMedPubMedCentral 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 77:850–855CrossRefPubMedPubMedCentral
38.
go back to reference 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 214:519–534CrossRefPubMedPubMedCentral 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 214:519–534CrossRefPubMedPubMedCentral
39.
go back to reference 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 37:1448–1455CrossRefPubMed 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 37:1448–1455CrossRefPubMed
40.
go back to reference Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356CrossRefPubMedPubMedCentral Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356CrossRefPubMedPubMedCentral
41.
go back to reference 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 109:4690–4695CrossRefPubMedPubMedCentral 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 109:4690–4695CrossRefPubMedPubMedCentral
42.
go back to reference 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 105:12569–12574CrossRefPubMedPubMedCentral 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 105:12569–12574CrossRefPubMedPubMedCentral
43.
go back to reference 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 8:407–419CrossRefPubMed 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 8:407–419CrossRefPubMed
44.
go back to reference Bonnelle V, Leech R, Kinnunen KM et al (2011) Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci 31:13442–13451CrossRefPubMed Bonnelle V, Leech R, Kinnunen KM et al (2011) Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci 31:13442–13451CrossRefPubMed
45.
go back to reference Ariza M, Serra-Grabulosa JM, Junque C et al (2006) Hippocampal head atrophy after traumatic brain injury. Neuropsychologia 44:1956–1961CrossRefPubMed Ariza M, Serra-Grabulosa JM, Junque C et al (2006) Hippocampal head atrophy after traumatic brain injury. Neuropsychologia 44:1956–1961CrossRefPubMed
46.
go back to reference 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 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
47.
go back to reference 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 55:1716–1727CrossRefPubMedPubMedCentral 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 55:1716–1727CrossRefPubMedPubMedCentral
48.
go back to reference 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 58:9–17CrossRefPubMed 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 58:9–17CrossRefPubMed
49.
go back to reference McDonald S, Flanagan S (2004) Social perception deficits after traumatic brain injury: interaction between emotion recognition, mentalizing ability, and social communication. Neuropsychology 18:572–579CrossRefPubMed McDonald S, Flanagan S (2004) Social perception deficits after traumatic brain injury: interaction between emotion recognition, mentalizing ability, and social communication. Neuropsychology 18:572–579CrossRefPubMed
50.
go back to reference 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 4:232–247CrossRefPubMed 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 4:232–247CrossRefPubMed
51.
52.
go back to reference 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 28:1707–1717CrossRefPubMed 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 28:1707–1717CrossRefPubMed
53.
go back to reference 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 76:984–988CrossRefPubMedPubMedCentral 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 76:984–988CrossRefPubMedPubMedCentral
54.
go back to reference Jones DT, Mateen FJ, Lucchinetti CF et al (2011) Default mode network disruption secondary to a lesion in the anterior thalamus. Arch Neurol 68:242–247CrossRefPubMed Jones DT, Mateen FJ, Lucchinetti CF et al (2011) Default mode network disruption secondary to a lesion in the anterior thalamus. Arch Neurol 68:242–247CrossRefPubMed
55.
go back to reference Tang L, Ge Y, Sodickson DK et al (2011) Thalamic resting-state functional networks: disruption in patients with mild traumatic brain injury. Radiology 260:831–840CrossRefPubMedPubMedCentral Tang L, Ge Y, Sodickson DK et al (2011) Thalamic resting-state functional networks: disruption in patients with mild traumatic brain injury. Radiology 260:831–840CrossRefPubMedPubMedCentral
56.
go back to reference Grossman EJ, Inglese M (2016) The Role of Thalamic Damage in Mild Traumatic Brain Injury. J Neurotrauma 33:163–167CrossRefPubMed Grossman EJ, Inglese M (2016) The Role of Thalamic Damage in Mild Traumatic Brain Injury. J Neurotrauma 33:163–167CrossRefPubMed
57.
go back to reference Marchand WR, Lee JN, Suchy Y et al (2012) Aberrant functional connectivity of cortico-basal ganglia circuits in major depression. Neurosci Lett 514:86–90CrossRefPubMed Marchand WR, Lee JN, Suchy Y et al (2012) Aberrant functional connectivity of cortico-basal ganglia circuits in major depression. Neurosci Lett 514:86–90CrossRefPubMed
58.
go back to reference Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication. Brain 123:1293–1326CrossRefPubMed Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication. Brain 123:1293–1326CrossRefPubMed
59.
go back to reference Quigley M, Cordes D, Turski P et al (2003) Role of the corpus callosum in functional connectivity. Am J Neuroradiol 24:208–212PubMed Quigley M, Cordes D, Turski P et al (2003) Role of the corpus callosum in functional connectivity. Am J Neuroradiol 24:208–212PubMed
60.
go back to reference 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 30:1609–1619CrossRefPubMedPubMedCentral 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 30:1609–1619CrossRefPubMedPubMedCentral
61.
go back to reference 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–E10CrossRefPubMedPubMedCentral 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–E10CrossRefPubMedPubMedCentral
62.
go back to reference Uddin LQ, Mooshagian E, Zaidel E et al (2008) Residual functional connectivity in the split-brain revealed with resting-state functional MRI. Neuroreport 19:703–709CrossRefPubMedPubMedCentral Uddin LQ, Mooshagian E, Zaidel E et al (2008) Residual functional connectivity in the split-brain revealed with resting-state functional MRI. Neuroreport 19:703–709CrossRefPubMedPubMedCentral
63.
go back to reference 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 28:767–772PubMed 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 28:767–772PubMed
64.
go back to reference 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 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
Metadata
Title
Detection of Functional Homotopy in Traumatic Axonal Injury
Authors
Jian Li
Lei Gao
Kai Xie
Jie Zhan
Xiaoping Luo
Huifang Wang
Huifang Zhang
Jing Zhao
Fuqing Zhou
Xianjun Zeng
Laichang He
Yulin He
Honghan Gong
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 1/2017
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-016-4302-x

Other articles of this Issue 1/2017

European Radiology 1/2017 Go to the issue