Failure to Identify the Left Arcuate Fasciculus at Diffusion Tractography Is a Specific Marker of Language Dysfunction in Pediatric Patients with Polymicrogyria
Abstract:Background. Polymicrogyric cortex demonstrates interindividual variation with regard to both extent of dyslamination and functional capacity. Given the relationship between laminar structure and white matter fibers, we sought to define the relationship between polymicrogyria (PMG), intrahemispheric association pathways, and network function. Methods. Each arcuate fasciculus (AF) was categorized as present or absent. Language was characterized by a pediatric neurologist. The presence of dysplastic cortex in the… Show more
“…These methods are commonly used to delineate ROI's for manual tractography (e.g. Cabeen et al, 2018 ; Coad et al, 2017 ; Filbey et al, 2014 ; Paldino et al, 2015 ). Fig.…”
Previous studies of white matter organization in sensorimotor tracts in developmental coordination disorder (DCD) have adopted diffusion tensor imaging (DTI), a method unable to reconcile pathways with ‘crossing fibres’. In response to limitations of the commonly adopted DTI approach, the present study employed a framework that can reconcile the ‘crossing fibre’ problem (i.e., constrained spherical deconvolution- CSD) to characterize white matter tissue organization of sensorimotor tracts in young adults with DCD. Participants were 19 healthy adults aged 18–46: 7 met diagnostic criteria for DCD (4 females) and 12 were controls (3 females). All underwent high angular diffusion MRI. After preprocessing, the left and right corticospinal tracts (CST) and superior longitudinal fasciculi (SLF) were delineated and all tracts were then generated using both CSD and DTI tractography respectively. Based on the CSD model, individuals with DCD demonstrated significantly decreased mean apparent fibre density (AFD) in the left SLF relative to controls (with large effect size, Cohen's d = 1.32) and a trend for decreased tract volume of the right SLF (with medium-large effect size, Cohen's d = 0.73). No differences in SLF microstructure were found between groups using DTI, nor were differences in CST microstructure observed across groups regardless of hemisphere or diffusion model. Our data are consistent with the view that motor impairment characteristic of DCD may be subserved by white matter abnormalities in sensorimotor tracts, specifically the left and right SLF. Our data further highlight the benefits of higher order diffusion MRI (e.g. CSD) relative to DTI for clarifying earlier inconsistencies in reports speaking to white matter organization in DCD, and its contribution to poor motor skill in DCD.
“…These methods are commonly used to delineate ROI's for manual tractography (e.g. Cabeen et al, 2018 ; Coad et al, 2017 ; Filbey et al, 2014 ; Paldino et al, 2015 ). Fig.…”
Previous studies of white matter organization in sensorimotor tracts in developmental coordination disorder (DCD) have adopted diffusion tensor imaging (DTI), a method unable to reconcile pathways with ‘crossing fibres’. In response to limitations of the commonly adopted DTI approach, the present study employed a framework that can reconcile the ‘crossing fibre’ problem (i.e., constrained spherical deconvolution- CSD) to characterize white matter tissue organization of sensorimotor tracts in young adults with DCD. Participants were 19 healthy adults aged 18–46: 7 met diagnostic criteria for DCD (4 females) and 12 were controls (3 females). All underwent high angular diffusion MRI. After preprocessing, the left and right corticospinal tracts (CST) and superior longitudinal fasciculi (SLF) were delineated and all tracts were then generated using both CSD and DTI tractography respectively. Based on the CSD model, individuals with DCD demonstrated significantly decreased mean apparent fibre density (AFD) in the left SLF relative to controls (with large effect size, Cohen's d = 1.32) and a trend for decreased tract volume of the right SLF (with medium-large effect size, Cohen's d = 0.73). No differences in SLF microstructure were found between groups using DTI, nor were differences in CST microstructure observed across groups regardless of hemisphere or diffusion model. Our data are consistent with the view that motor impairment characteristic of DCD may be subserved by white matter abnormalities in sensorimotor tracts, specifically the left and right SLF. Our data further highlight the benefits of higher order diffusion MRI (e.g. CSD) relative to DTI for clarifying earlier inconsistencies in reports speaking to white matter organization in DCD, and its contribution to poor motor skill in DCD.
“…This method is particularly relevant in pediatric populations such as extremely premature infants, or children with cortical malformations. Results have suggested a link between the microstructural properties of the arcuate fasciculus and language abilities (Salvan et al, 2017;Paldino et al, 2015). However, to our knowledge, only a few studies have gathered structural MRI together with behavioural and neuropsychological data in children with PAIS (François et al, 2016(François et al, , 2019Northam et al, 2018, see Figure 3 for a summary of the main results of the two last studies).…”
Section: Neuroimaging Markers Of Language Recovery After Perinatal Armentioning
Brain imaging methods such as functional Magnetic Resonance Imaging (fMRI) and Diffusion Tensor Imaging (DTI) have already been used to decipher the functional and structural brain changes occurring during normal language development. However, little is known about the differentiation of the language network after an early lesion. While in adults, stroke over the left hemisphere generally induces post-stroke aphasia, it is not always the case when a stroke occurs in the perinatal period, thus revealing a remarkable plastic power of the language network during early development. In particular, the role of perilesional tissues, as opposed to undamaged brain areas in the functional recovery of language functions after an early insult, remains unclear. In this review article, we provide an overview of the extant literature using functional and structural neuroimaging data revealing the signatures of brain plasticity underlying near-normal language development.
“…This finding may have prognostic implications, predicting a higher likelihood of language deficits in the more diffuse form of peri-Sylvian PMG. 15 In the 5 patients with PMG with diffuse malformations relating to congenital CMV infection, we observed less severe patterns of SLF abnormalities, compared with the remaining PMG cases without CMV infection. While this finding is contrary to our previously stated observation, this preliminary finding implies that the CMV infection affects cortical development in MCD via a distinct mechanism.…”
Section: Discussionmentioning
confidence: 53%
“…36,37 Abnormal SLF morphology was frequently identified in our PMG cohort, consistent with findings from other studies. 13,15,17 In our peri-Sylvian PMG cohort, the severity of SLF abnormalities (ie, from normal to irregular to absent) was found to be associated with the severity and extent of MCD. Related volumetric analysis (On-line Fig 4) highlighted that the volume of malformed cortices in the patients with peri-Sylvian PMG with absent or irregular SLF was significantly higher than that in patients with normal SLFs.…”
BACKGROUND AND PURPOSE: Polymicrogyria and lissencephaly may be associated with abnormal organization of the undelying white matter tracts that have been rarely investigated so far. Our aim was to characterize white matter tract organization in polymicrogyria and lissencephaly using constrained spherical deconvolution, a multifiber diffusion MR imaging modeling technique for white matter tractography reconstruction.
MATERIALS AND METHODS:We retrospectively reviewed 50 patients (mean age, 8.3 6 5.4 years; range, 1.4-21.2 years; 27 males) with different polymicrogyria (n ¼ 42) and lissencephaly (n ¼ 8) subtypes. The fiber direction-encoded color maps and 6 different white matter tracts reconstructed from each patient were visually compared with corresponding images reconstructed from 7 agematched, healthy control WM templates. Each white matter tract was assessed by 2 experienced pediatric neuroradiologists and scored in consensus on the basis of the severity of the structural abnormality, ranging from the white matter tracts being absent to thickened. The results were summarized by different polymicrogyria and lissencephaly subgroups.RESULTS: More abnormal-appearing white matter tracts were identified in patients with lissencephaly compared with those with polymicrogyria (79.2% versus 37.3%). In lissencephaly, structural abnormalities were identified in all studied white matter tracts. In polymicrogyria, the more frequently affected white matter tracts were the cingulum, superior longitudinal fasciculus, inferior longitudinal fasciculus, and optic radiation-posterior corona radiata. The severity of superior longitudinal fasciculus and cingulum abnormalities was associated with the polymicrogyria distribution and extent. A thickened superior fronto-occipital fasciculus was demonstrated in 3 patients.
CONCLUSIONS:We demonstrated a range of white matter tract structural abnormalities in patients with polymicrogyria and lissencephaly. The patterns of white matter tract involvement are related to polymicrogyria and lissencephaly subgroups, distribution, and, possibly, their underlying etiologies. ABBREVIATIONS: CG ¼ cingulum; CMV ¼ cytomegalovirus; CSD ¼ constrained spherical deconvolution; DEC ¼ direction-encoded color; dMRI ¼ diffusion MRI; FOD ¼ fiber orientation distribution; HARDI ¼ high angular resolution diffusion imaging; IFOF ¼ inferior fronto-occipital fasciculus; ILF ¼ inferior longitudinal fasciculus; LIS ¼ lissencephaly; MCD ¼ malformation of cortical development; OR-PCR ¼ optic radiation-posterior corona radiata; PMG ¼ polymicrogyria; SBH ¼ subcortical band heterotopia; SFOF ¼ superior fronto-occipital fasciculus/Muratoff bundle; SLF ¼ superior longitudinal fasciculus; WMT ¼ white matter tract
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