Age-related macular degeneration affects the optic radiation white matter projecting to locations of retinal damage

Abstract

We investigated the impact of age-related macular degeneration (AMD) on visual acuity and the visual white matter. We combined an adaptive cortical atlas and diffusion-weighted magnetic resonance imaging (dMRI) and tractography to separate optic radiation (OR) projections to different retinal eccentricities in human primary visual cortex. We exploited the known anatomical organization of the OR and clinically relevant data to segment the OR into three primary components projecting to fovea, mid-and far-periphery. We measured white matter tissue properties-fractional anisotropy, linearity, planarity, sphericity-along the aforementioned three components of the optic radiation to compare AMD patients and controls. We found differences in white matter properties specific to OR white matter fascicles projecting to primary visual cortex locations corresponding to the location of retinal damage (fovea). Additionally, we show that the magnitude of white matter properties in AMD patients' correlates with visual acuity. In sum, we demonstrate a specific relation between visual loss, anatomical location of retinal damage and white matter damage in AMD patients. Importantly, we demonstrate that these changes are so profound that can be detected using magnetic resonance imaging data with clinical resolution. The conserved mapping between retinal and white matter damage suggests that retinal neurodegeneration might be a primary cause of white matter degeneration in AMD patients. The results highlight the impact of eye disease on brain tissue, a process that may become an important target to monitor during the course of treatment.

The visual white matter connecting human area prostriata and the thalamus is retinotopically organized

“…In sum, given that the anterior and posterior parts of prostriata process the foveal and peripheral parts of the visual field respectively, our results suggest that whereas LGN-Pro-1 seems to transfer information from the foveal visual field, LGN-Pro-2 transfers information from the periphery. This is also consistent with the higher FA values within prostriata for LGN-Pro-1 ( Figure 4B), also observed in a previous report regarding the OR retinotopic segregation (Yoshimine et al 2018). Finally, to provide a quantification for the qualitative results reported above, we divided the prostriata ROI into two parts using the major (longer) axis of the ellipse illustrated in one representative subject in Figure 5B (this analysis is akin to that performed on 139 subjects for Figure 3).…”

“…This is not the first report of white matter tracts segmented into different subcomponent based on functional properties using in-vivo tractography. In fact, the division of a fiber bundle based on visual field representation has been carried out by Yoshimine et al(2018), (see their Figure 2) who separate the OR based on eccentricity with clear segregation of foveal and peripheral tracts (Yoshimine et al 2018;Parraga et al 2012). We note that the subdivision between LGN-Pro-1 and LGN-Pro-2 is somehow anatomically arbitrary.…”

“…LGN-Pro tract resembles (but only partially overlaps with) that of the optic radiations (OR). It has been shown that the OR can be subdivided into at least two sub-components defined by the termination of the fibers into V1 regions representing different eccentricities (Parraga et al 2012;Yoshimine et al 2018). The fibers of the OR projecting to V1 locations representing the visual periphery travel more ventrally and laterally within Meyer's loop.…”

“…The fibers of the OR projecting to V1 locations representing the visual periphery travel more ventrally and laterally within Meyer's loop. The fibers of the OR projecting to V1 locations representing the central visual field travel more dorsally and medially outside of Meyer's loop (Yoshimine et al 2018). Here, we used the anteriorposterior axis of prostriata described in the previous section ( Figure 2) and subdivided the…”

“…LGN-Pro-2 originates from prostriata that is clearly different from V1 and therefore we consider it as a separate entity. Finally, we used the diffusion-tensor model (Basser et al 1994;Pierpaoli et al 1996) and estimated fractional anisotropy (FA), mean diffusivity (MD) and radial diffusivity (RD) at 100 locations along the tracts' length using tract profiles (Rykhlevskaia et al 2009;Yeatman et al 2012;Yoshimine et al 2018). The two tracts differ substantially along their length in their microstructural properties (FA, MD, RD; Figure 3D), while the automatic subdivision of subcomponents reveals a similar number of fibers assigned to each of them ( Figure 3E).…”