White matter structural connectivity underlying semantic processing: evidence from brain damaged patients

• Published in: Brain (London, England : 1878) Vol. 136; no. 10; pp. 2952 - 2965
• Main Authors: Han, Zaizhu, Ma, Yujun, Gong, Gaolang, He, Yong, Caramazza, Alfonso, Bi, Yanchao
• Format: Journal Article
• Language: English
• Published: Oxford Oxford University Press 01.10.2013
• Subjects: Adult; Aged; Anisotropy; Biological and medical sciences; Brain; Brain Damage; Brain Injuries - pathology; Brain Injuries - physiopathology; Brain Mapping - methods; Diffusion Tensor Imaging - methods; Female; Humans; Image Processing, Computer-Assisted - methods; Male; Medical sciences; Middle Aged; Multiple sclerosis and variants. Guillain barré syndrome and other inflammatory polyneuropathies. Leukoencephalitis; Nerve Fibers - pathology; Nerve Net - pathology; Neural Pathways - pathology; Neurology; Neuropsychological Tests; Semantic Processing; Young Adult; DTI; connectome; brain-damaged patient; semantic network; Human; Nervous system diseases; Semantics; Central nervous system disease; White matter; Cerebral disorder
• ISSN: 0006-8950; 1460-2156; 1460-2156
• DOI: 10.1093/brain/awt205

Widely distributed brain regions in temporal, parietal and frontal cortex have been found to be involved in semantic processing, but the anatomical connections supporting the semantic system are not well understood. In a group of 76 right-handed brain-damaged patients, we tested the relationship between the integrity of major white matter tracts and the presence of semantic deficits. The integrity of white matter tracts was measured by percentage of lesion voxels obtained in structural imaging and mean fractional anisotropy values obtained in diffusion tensor imaging. Semantic deficits were assessed by jointly considering the performance on three semantic tasks that vary in the modalities of input (visual and auditory stimuli) and output (oral naming and associative judgement). We found that the lesion volume and fractional anisotropy value of the left inferior fronto-occipital fasciculus, left anterior thalamic radiation, and left uncinate fasciculus significantly correlated with severity of impairment in all three semantic tasks. These associations remained significant even when we controlled for a wide range of potential confounding variables, including overall cognitive state, whole lesion volume, or type of brain damage. The effects of these three white matter tracts could not be explained by potential involvement of relevant grey matter, and were (relatively) specific to object semantic processing, as no correlation with performance on non-object semantic control tasks (oral repetition and number processing tasks) was observed. These results underscore the causal role of left inferior fronto-occipital fasciculus, left anterior thalamic radiation, and left uncinate fasciculus in semantic processing, providing direct evidence for (part of) the anatomical skeleton of the semantic network.