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Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete Virtual 'In vivo' tractography dissection

Michel Thiebaut de Schotten, Francesco Tomaiuolo, Marilena Aiello, Sheila Merola, Massimo Silvetti UGent, Francesca Lecce, Paolo Bartolomeo and Fabrizio Doricchi (2014) CEREBRAL CORTEX. 24(3). p.691-706
abstract
The exact anatomical localization of right hemisphere lesions that lead to left spatial neglect is still debated. The effect of confounding factors such as acute diaschisis and hypoperfusion, visual field defects, and lesion size may account for conflicting results that have been reported in the literature. Here, we present a comprehensive anatomical investigation of the gray- and white matter lesion correlates of left spatial neglect, which was run in a sample 58 patients with subacute or chronic vascular strokes in the territory of the right middle cerebral artery. Standard voxel-based correlates confirmed the role played by lesions in the posterior parietal cortex (supramarginal gyrus, angular gyrus, and temporalparietal junction), in the frontal cortex (frontal eye field, middle and inferior frontal gyrus), and in the underlying parietalfrontal white matter. Using a new diffusion tensor imaging-based atlas of the human brain, we were able to run, for the first time, a detailed analysis of the lesion involvement of subcortical white matter pathways. The results of this analysis revealed that, among the different pathways linking parietal with frontal areas, damage to the second branch of the superior longitudinal fasciculus (SLF II) was the best predictor of left spatial neglect. The group study also revealed a subsample of patients with neglect due to focal lesion in the lateraldorsal portion of the thalamus, which connects the premotor cortex with the inferior parietal lobule. The relevance of fronto-parietal disconnection was further supported by complete in vivo tractography dissection of white matter pathways in 2 patients, one with and the other without signs of neglect. These 2 patients were studied both in the acute phase and 1 year after stroke and were perfectly matched for age, handedness, stroke onset, lesion size, and for cortical lesion involvement. Taken together, the results of the present study support the hypothesis that anatomical disconnections leading to a functional breakdown of parietalfrontal networks are an important pathophysiological factor leading to chronic left spatial neglect. Here, we propose that different loci of SLF disconnection on the rostro-caudal axis can also be associated with disconnection of short-range white matter pathways within the frontal or parietal areas. Such different local disconnection patterns can play a role in the important clinical variability of the neglect syndrome.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
stroke, spatial neglect, CEREBRAL-ARTERY INFARCTION, DIFFUSION-TENSOR MRI, STIMULUS-DRIVEN ATTENTION, FRONTAL-LOBE INFARCTION, LEFT UNILATERAL NEGLECT, HUMAN BRAIN-LESIONS, RIGHT-HEMISPHERE STROKE, OF-THE-LITERATURE, VISUAL NEGLECT, anatomy, THALAMIC HEMORRHAGE, diffusion tensor imaging, human
journal title
CEREBRAL CORTEX
volume
24
issue
3
pages
691 - 706
Web of Science type
Article
Web of Science id
000331845700012
JCR category
NEUROSCIENCES
JCR impact factor
8.665 (2014)
JCR rank
16/252 (2014)
JCR quartile
1 (2014)
ISSN
1047-3211
DOI
10.1093/cercor/bhs351
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
5701346
handle
http://hdl.handle.net/1854/LU-5701346
date created
2014-09-11 20:43:42
date last changed
2016-12-19 15:46:45
@article{5701346,
  abstract     = {The exact anatomical localization of right hemisphere lesions that lead to left spatial neglect is still debated. The effect of confounding factors such as acute diaschisis and hypoperfusion, visual field defects, and lesion size may account for conflicting results that have been reported in the literature. Here, we present a comprehensive anatomical investigation of the gray- and white matter lesion correlates of left spatial neglect, which was run in a sample 58 patients with subacute or chronic vascular strokes in the territory of the right middle cerebral artery. Standard voxel-based correlates confirmed the role played by lesions in the posterior parietal cortex (supramarginal gyrus, angular gyrus, and temporalparietal junction), in the frontal cortex (frontal eye field, middle and inferior frontal gyrus), and in the underlying parietalfrontal white matter. Using a new diffusion tensor imaging-based atlas of the human brain, we were able to run, for the first time, a detailed analysis of the lesion involvement of subcortical white matter pathways. The results of this analysis revealed that, among the different pathways linking parietal with frontal areas, damage to the second branch of the superior longitudinal fasciculus (SLF II) was the best predictor of left spatial neglect. The group study also revealed a subsample of patients with neglect due to focal lesion in the lateraldorsal portion of the thalamus, which connects the premotor cortex with the inferior parietal lobule. The relevance of fronto-parietal disconnection was further supported by complete in vivo tractography dissection of white matter pathways in 2 patients, one with and the other without signs of neglect. These 2 patients were studied both in the acute phase and 1 year after stroke and were perfectly matched for age, handedness, stroke onset, lesion size, and for cortical lesion involvement. Taken together, the results of the present study support the hypothesis that anatomical disconnections leading to a functional breakdown of parietalfrontal networks are an important pathophysiological factor leading to chronic left spatial neglect. Here, we propose that different loci of SLF disconnection on the rostro-caudal axis can also be associated with disconnection of short-range white matter pathways within the frontal or parietal areas. Such different local disconnection patterns can play a role in the important clinical variability of the neglect syndrome.},
  author       = {Thiebaut de Schotten, Michel and Tomaiuolo, Francesco and Aiello, Marilena and Merola, Sheila and Silvetti, Massimo and Lecce, Francesca and Bartolomeo, Paolo and Doricchi, Fabrizio},
  issn         = {1047-3211},
  journal      = {CEREBRAL CORTEX},
  keyword      = {stroke,spatial neglect,CEREBRAL-ARTERY INFARCTION,DIFFUSION-TENSOR MRI,STIMULUS-DRIVEN ATTENTION,FRONTAL-LOBE INFARCTION,LEFT UNILATERAL NEGLECT,HUMAN BRAIN-LESIONS,RIGHT-HEMISPHERE STROKE,OF-THE-LITERATURE,VISUAL NEGLECT,anatomy,THALAMIC HEMORRHAGE,diffusion tensor imaging,human},
  language     = {eng},
  number       = {3},
  pages        = {691--706},
  title        = {Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete Virtual 'In vivo' tractography dissection},
  url          = {http://dx.doi.org/10.1093/cercor/bhs351},
  volume       = {24},
  year         = {2014},
}

Chicago
Thiebaut de Schotten, Michel, Francesco Tomaiuolo, Marilena Aiello, Sheila Merola, Massimo Silvetti, Francesca Lecce, Paolo Bartolomeo, and Fabrizio Doricchi. 2014. “Damage to White Matter Pathways in Subacute and Chronic Spatial Neglect: a Group Study and 2 Single-case Studies with Complete Virtual ‘In Vivo’ Tractography Dissection.” Cerebral Cortex 24 (3): 691–706.
APA
Thiebaut de Schotten, M., Tomaiuolo, F., Aiello, M., Merola, S., Silvetti, M., Lecce, F., Bartolomeo, P., et al. (2014). Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete Virtual “In vivo” tractography dissection. CEREBRAL CORTEX, 24(3), 691–706.
Vancouver
1.
Thiebaut de Schotten M, Tomaiuolo F, Aiello M, Merola S, Silvetti M, Lecce F, et al. Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete Virtual “In vivo” tractography dissection. CEREBRAL CORTEX. 2014;24(3):691–706.
MLA
Thiebaut de Schotten, Michel, Francesco Tomaiuolo, Marilena Aiello, et al. “Damage to White Matter Pathways in Subacute and Chronic Spatial Neglect: a Group Study and 2 Single-case Studies with Complete Virtual ‘In Vivo’ Tractography Dissection.” CEREBRAL CORTEX 24.3 (2014): 691–706. Print.