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Comparative Study
. 2014 Sep 25;55(10):6976-86.
doi: 10.1167/iovs.14-14737.

White matter consequences of retinal receptor and ganglion cell damage

Shumpei Ogawa  1 , Hiromasa Takemura  2 , Hiroshi Horiguchi  3 , Masahiko Terao  4 , Tomoki Haji  5 , Franco Pestilli  6 , Jason D Yeatman  6 , Hiroshi Tsuneoka  3 , Brian A Wandell  6 , Yoichiro Masuda  7
Affiliations
Comparative Study

White matter consequences of retinal receptor and ganglion cell damage

Shumpei Ogawa et al. Invest Ophthalmol Vis Sci. .

Abstract

Purpose: Patients with Leber hereditary optic neuropathy (LHON) and cone-rod dystrophy (CRD) have central vision loss; but CRD damages the retinal photoreceptor layer, and LHON damages the retinal ganglion cell (RGC) layer. Using diffusion MRI, we measured how these two types of retinal damage affect the optic tract (ganglion cell axons) and optic radiation (geniculo-striate axons).

Methods: Adult onset CRD (n = 5), LHON (n = 6), and healthy controls (n = 14) participated in the study. We used probabilistic fiber tractography to identify the optic tract and the optic radiation. We compared axial and radial diffusivity at many positions along the optic tract and the optic radiation.

Results: In both types of patients, diffusion measures within the optic tract and the optic radiation differ from controls. The optic tract change is principally a decrease in axial diffusivity; the optic radiation change is principally an increase in radial diffusivity.

Conclusions: Both photoreceptor layer (CRD) and retinal ganglion cell (LHON) retinal disease causes substantial change in the visual white matter. These changes can be measured using diffusion MRI. The diffusion changes measured in the optic tract and the optic radiation differ, suggesting that they are caused by different biological mechanisms.

Keywords: Leber hereditary optic neuropathy; cone-rod dystrophy; diffusion-MRI; white matter.

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Figures

Figure 1
Figure 1
Left panel: OCT image of a retina in a control, LHON, and CRD subject. In each panel, the inset image in the lower left shows the position of the scan line. The main image shows the cross-section. The blue lines outline the RNFL. The red line shows the borderline between inner segment/outer segment (IS/OS) photoreceptors. (A) Control. (B) LHON. The retinal nerve fiber layer is very thin whereas the IS/OS lines are similar to the control. (C) CRD. The IS/OS line is missing, but the RNFL thickness is similar to controls. Right panel: Visual fields measured by Goldmann perimetry. Black depicts visual field regions with no sensitivity to the target.
Figure 2
Figure 2
Circumpapillary retinal nerve layer thickness measured by OCT in three groups (blue: LHON; red: CRD; gray: controls). Control data are from Sung et al.
Figure 3
Figure 3
Visual white matter pathways determined by fiber tractography in a representative subject. The regions of interest (red) and tracts are shown above an axial slice of the T1-weighted image. Purple: optic tract. Yellow: optic radiation. The optic chiasm, LGN, and V1 ROIs are denoted as red volumes. Inserted cross lines are 2 cm.
Figure 4
Figure 4
Identification of tract profiles. (A) Optic tract (purple) and optic radiation (yellow) identified in a representative subject. (B) Values of FA in optic tract and optic radiation voxels (red, high FA; blue, low FA). (C) Values of FA averaged along optic tract and optic radiation. Averaged FA values along the pathway based on weighted-linear sum of voxel-wise FA values based on the distance from the core of the pathway.
Figure 5
Figure 5
Fractional anisotropy along the core of the optic tract and the optic radiation. The two panels show the FA measures in (A) the optic tract and (B) the optic radiation. Individual LHON (blue) and CRD (red) patients are compared with the distribution of measurements from the controls (gray shaded). Thick curves show the mean of each group (LHON: blue; CRD: red; control: black). The lighter gray shades show range of ±2 SD from the control mean, and the darker gray band shows ±1 SD from the control mean. x-axis describes normalized position along the tract. Shaded yellow region indicates the portion of the tract showing a significant main effect of subject groups in FA value (one-way ANOVA, P < 0.01).
Figure 6
Figure 6
Axial diffusivity and RD along the optic tract and the optic radiation. The left two panels show the average AD measures in (A) the optic tract and (C) the optic radiation. The right two panels show the average RD measures in (B) the optic tract and (D) the optic radiation. Other conventions are identical to those in Figure 5. Unit of diffusivity is μm2/ms.
Figure 7
Figure 7
Fractional anisotropy along optic radiation fibers grouped by length. In each subject, we grouped individual optic radiation fibers into five categories based on fiber length. The categories were the percentile of the fiber: (A) 0–20, (B) 20–40, (C) 40–60, (D) 60–80, and (E) 80–100 percentile from short to long. The separate panels compare the fractional anisotropy across groups in the five fiber-length categories. Other conventions are identical to those of Figures 5 and 6.
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