Diffusion tensor imaging reveals white matter reorganization in early blind humans

Abstract

Multiple functional methods including functional magnetic resonance imaging, transcranial magnetic stimulation, and positron emission tomography have shown cortical reorganization in response to blindness. We investigated microanatomical correlates of this reorganization using diffusion tensor imaging and diffusion tensor tractography (DTT). Five early blind (EB) were compared with 7 normally sighted (NS) persons. DTT showed marked geniculocalcarine tract differences between EB and NS participants. All EB participants showed evidence of atrophy of the geniculocortical tracts. Connections between visual cortex and the orbital frontal and temporal cortices were relatively preserved in the EB group. Importantly, no additional tracts were found in any EB participant. Significant alterations of average diffusivity and relative anisotropy were found in the white matter (WM) of the occipital lobe in the EB group. These observations suggest that blindness leads to a reorganization of cerebral WM and plausibly support the hypothesis that visual cortex functionality in blindness is primarily mediated by corticocortical as opposed to thalamocortical connections.

Figure 1

Demonstration, in a normally sighted individual, of achieved multimodal registration accuracy. (A) High-resolution T₁W (MP-RAGE) structural image. (B) Automatic (fuzzy class means based) segmentation of T₁W and T₂W structural data into cerebrospinal fluid (CSF) (dark gray), GM (light gray), and WM (white). (C) Unsensitized (averaged I₀) component of the diffusion data set. (D) Diffusion anisotropy (A_σ). All views show the same parasagittal plane. The red and green outlines indicate the outer brain edge and the GM–WM boundary, respectively; these were traced (Analyze ROI tool) on the MP-RAGE image and duplicated on the other volumes. The asterisk indicates a region illustrating diverse contrast mechanisms: In the I₀ image (C), bright CSF is outside the outer boundary of the brain. The corresponding locus in (A) and (B) shows GM bounded by the red and green traces. In the anisotropy image (D), both GM and CSF are dark and only WM is bright.

Figure 2

Illustration of the V1/V2 ROI obtained in 1 sighted (NS1) and 1 EB (EB7) participant. Sagittal and coronal sections are shown with and without the ROI overlay (red). The arrows indicate the calcarine sulcus. Note confinement, to within 2.5-mm³ voxel resolution, of these ROIs to subcortical WM. These ROIs were used for tract selection (Figs. 3 and 4, Tables 3 and 4) and diffusion parameter measurements (Table 5).

Figure 3

GCT tractography results obtained in 2 sighted and 2 EB participants. Tracks were selected as intersecting both individually defined V1/V2 ROI (Fig. 2) and the consensus LGN region (yellow) established in sighted participants. Selected tracks are shown overlaid on axial slices. Quantitative results for all participants are given in Table 4. NS2 is a typical NS participant, and NS7 is the most abnormal of the NS group. EB4 and EB11 are the 2 blind participants with a detectable GCT.

Figure 4

Tractography results obtained by selection of tracks intersecting individually defined V1/V2 ROI (Fig. 2). Tracks traced to several locations are shown color coded as follows: LGN (dark blue), pulvinar/SC (light blue), anterior temporal lobe (green), orbitofrontal (yellow), commissural (red). All images show individual DTT results overlaid on the participant's MP-RAGE. Sagittal, axial, and double oblique (inset key) views are shown on successive rows. One NS and 4/5 EB participants are included; EB1 was omitted because of a paucity of DTT fibers. Inspection results for all participants are given in Table 3.

Figure 5

Selected ROI used for regional measurement of ADC and A_σ (Table 5). A, B, and C: anterior, middle, and posterior thirds of the consensus GCT obtained in the NS group. The background slice shows the Talairach atlas representative image at axial plane Z = −4. D: inferior half of the splenium. E: other segments of the CC. The background slice is that of a representative NS individual through the midsagittal plane.