Association Between Subcortical Vascular Lesion Location and Cognition: a Voxel-based and Tract-based Lesion-symptom Mapping Study. The SMART-MR Study

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Apr 18

PMID 23593238

Citations 60

Authors

J Matthijs Biesbroek

Hugo J Kuijf

Yolanda van der Graaf

Koen L Vincken

Albert Postma

Willem P T M Mali

Geert J Biessels

Mirjam I Geerlings

Affiliations

Soon will be listed here.

Abstract

Introduction: Lacunar lesions (LLs) and white matter lesions (WMLs) affect cognition. We assessed whether lesions located in specific white matter tracts were associated with cognitive performance taking into account total lesion burden.

Methods: Within the Second Manifestations of ARTerial disease Magnetic Resonance (SMART-MR) study, cross-sectional analyses were performed on 516 patients with manifest arterial disease. We applied an assumption-free voxel-based lesion-symptom mapping approach to investigate the relation between LL and WML locations on 1.5 Tesla brain MRI and compound scores of executive functioning, memory and processing speed. Secondly, a multivariable linear regression model was used to relate the regional volume of LLs and WMLs within specific white matter tracts to cognitive functioning.

Results: Voxel-based lesion-symptom mapping identified several clusters of voxels with a significant correlation between WMLs and executive functioning, mostly located within the superior longitudinal fasciculus and anterior thalamic radiation. In the multivariable linear regression model, a statistically significant association was found between regional LL volume within the superior longitudinal fasciculus and anterior thalamic radiation and executive functioning after adjustment for total LL and WML burden.

Conclusion: These findings identify the superior longitudinal fasciculus and anterior thalamic radiation as key anatomical structures in executive functioning and emphasize the role of strategically located vascular lesions in vascular cognitive impairment.

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References

Duering M, Zieren N, Herve D, Jouvent E, Reyes S, Peters N . Strategic role of frontal white matter tracts in vascular cognitive impairment: a voxel-based lesion-symptom mapping study in CADASIL. Brain. 2011; 134(Pt 8):2366-75. DOI: 10.1093/brain/awr169. View

Pohjasvaara T, Erkinjuntti T, Ylikoski R, Hietanen M, Vataja R, Kaste M . Clinical determinants of poststroke dementia. Stroke. 1998; 29(1):75-81. DOI: 10.1161/01.str.29.1.75. View

Rorden C, Karnath H, Bonilha L . Improving lesion-symptom mapping. J Cogn Neurosci. 2007; 19(7):1081-8. DOI: 10.1162/jocn.2007.19.7.1081. View

Brett M, Leff A, Rorden C, Ashburner J . Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage. 2001; 14(2):486-500. DOI: 10.1006/nimg.2001.0845. View

Robertson I, Ward T, Ridgeway V, Nimmo-Smith I . The structure of normal human attention: The Test of Everyday Attention. J Int Neuropsychol Soc. 1996; 2(6):525-34. DOI: 10.1017/s1355617700001697. View

Brand N, Jolles J . Learning and retrieval rate of words presented auditorily and visually. J Gen Psychol. 1985; 112(2):201-10. DOI: 10.1080/00221309.1985.9711004. View

Mungas D, Harvey D, Reed B, Jagust W, DeCarli C, Beckett L . Longitudinal volumetric MRI change and rate of cognitive decline. Neurology. 2005; 65(4):565-71. PMC: 1820871. DOI: 10.1212/01.wnl.0000172913.88973.0d. View

OBrien J, Wiseman R, Burton E, Barber B, Wesnes K, Saxby B . Cognitive associations of subcortical white matter lesions in older people. Ann N Y Acad Sci. 2002; 977:436-44. DOI: 10.1111/j.1749-6632.2002.tb04849.x. View

Grool A, van der Graaf Y, Mali W, Geerlings M . Location of cerebrovascular and degenerative changes, depressive symptoms and cognitive functioning in later life: the SMART-Medea study. J Neurol Neurosurg Psychiatry. 2011; 82(10):1093-100. DOI: 10.1136/jnnp.2010.232413. View

10.

Prins N, van Dijk E, den Heijer T, Vermeer S, Jolles J, Koudstaal P . Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain. 2005; 128(Pt 9):2034-41. DOI: 10.1093/brain/awh553. View

11.

Muller M, van der Graaf Y, Algra A, Hendrikse J, Mali W, Geerlings M . Carotid atherosclerosis and progression of brain atrophy: the SMART-MR study. Ann Neurol. 2011; 70(2):237-44. DOI: 10.1002/ana.22392. View

12.

Smith E, Salat D, Jeng J, McCreary C, Fischl B, Schmahmann J . Correlations between MRI white matter lesion location and executive function and episodic memory. Neurology. 2011; 76(17):1492-9. PMC: 3087468. DOI: 10.1212/WNL.0b013e318217e7c8. View

13.

Anbeek P, Vincken K, van Bochove G, van Osch M, van der Grond J . Probabilistic segmentation of brain tissue in MR imaging. Neuroimage. 2005; 27(4):795-804. DOI: 10.1016/j.neuroimage.2005.05.046. View

14.

Klein S, Staring M, Murphy K, Viergever M, Pluim J . elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging. 2009; 29(1):196-205. DOI: 10.1109/TMI.2009.2035616. View

15.

Gorelick P, Scuteri A, Black S, DeCarli C, Greenberg S, Iadecola C . Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the american heart association/american stroke association. Stroke. 2011; 42(9):2672-713. PMC: 3778669. DOI: 10.1161/STR.0b013e3182299496. View

16.

Bolandzadeh N, Davis J, Tam R, Handy T, Liu-Ambrose T . The association between cognitive function and white matter lesion location in older adults: a systematic review. BMC Neurol. 2012; 12:126. PMC: 3522005. DOI: 10.1186/1471-2377-12-126. View

17.

Anbeek P, Vincken K, van Osch M, Bisschops R, van der Grond J . Probabilistic segmentation of white matter lesions in MR imaging. Neuroimage. 2004; 21(3):1037-44. DOI: 10.1016/j.neuroimage.2003.10.012. View

18.

Fonov V, Evans A, Botteron K, Almli C, McKinstry R, Collins D . Unbiased average age-appropriate atlases for pediatric studies. Neuroimage. 2010; 54(1):313-27. PMC: 2962759. DOI: 10.1016/j.neuroimage.2010.07.033. View

19.

Kimberg D, Coslett H, Schwartz M . Power in Voxel-based lesion-symptom mapping. J Cogn Neurosci. 2007; 19(7):1067-80. DOI: 10.1162/jocn.2007.19.7.1067. View

20.

Chabriat H, Joutel A, Dichgans M, Tournier-Lasserve E, Bousser M . Cadasil. Lancet Neurol. 2009; 8(7):643-53. DOI: 10.1016/S1474-4422(09)70127-9. View