Abstract

Retinal diseases like age-related macular degeneration (AMD) or hereditary juvenile macular dystrophies (JMD) lead to a loss of central vision. Many patients compensate for this loss with a pseudo fovea in the intact peripheral retina, the so-called “preferred retinal locus” (PRL). How extensive eccentric viewing associated with central vision loss (CVL) affects brain structures responsible for visual perception and visually guided eye movements remains unknown. CVL results in a reduction of cortical gray matter in the “lesion projection zone” (LPZ) in early visual cortex, but the thickness of primary visual cortex appears to be largely preserved for eccentric-field representations. Here we explore how eccentric viewing strategies are related to cortical thickness (CT) measures in early visual cortex and in brain areas involved in the control of eye movements (frontal eye fields, FEF, supplementary eye fields, SEF, and premotor eye fields, PEF). We determined the projection zones (regions of interest, ROIs) of the PRL and of an equally peripheral area in the opposite hemifield (OppPRL) in early visual cortex (V1 and V2) in 32 patients with MD and 32 age-matched controls (19–84 years) by functional magnetic resonance imaging. Subsequently, we calculated the CT in these ROIs and compared it between PRL and OppPRL as well as between groups. Additionally, we examined the CT of FEF, SEF, and PEF and correlated it with behavioral measures like reading speed and eccentric fixation stability at the PRL. We found a significant difference between PRL and OppPRL projection zones in V1 with increased CT at the PRL, that was more pronounced in the patients, but also visible in the controls. Although the mean CT of the eye fields did not differ significantly between patients and controls, we found a trend to a positive correlation between CT in the right FEF and SEF and fixation stability in the whole patient group and between CT in the right PEF and reading speed in the JMD subgroup. The results indicate a possible association between the compensatory strategies used by patients with CVL and structural brain properties in early visual cortex and cortical eye fields.

Highlights

  • In Western countries, macular degeneration is one of the most common causes for blindness, especially in elderly people (Ambati and Fowler, 2012)

  • Since reading speed was negatively correlated with age and with scotoma size in the juvenile macular dystrophies (JMD) group, the positive correlation with cortical thickness (CT) in left and right FEF into a medial (FEF-m) and right premotor eye field (PEF) may at least partially be confounded with those variables

  • The post hoc tests revealed no significant differences between preferred retinal locus” (PRL) and OppPRL CT values in the control group, where CT was measured in comparable regions of interest (ROIs), there was a trend to positive differences in CT between PRL and OppPRL ROIs in controls, which resulted in a significant main effect of ROI in primary visual cortex (V1)

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Summary

Introduction

In Western countries, macular degeneration is one of the most common causes for (partial) blindness, especially in elderly people (Ambati and Fowler, 2012). Juvenile forms of retinal dystrophies (JMD, e.g., Stargardt’s disease or conerod dystrophy) lead to central scotomas due to similar processes (Glazer and Dryja, 2002). Degenerative diseases, such as macular degeneration, physiologically lead to a structural and functional change in the associated areas of the brain (e.g., Xiao et al, 2007; Xie et al, 2007; Barnes et al, 2010; Hernowo et al, 2014). Since previous findings at the neuronal level indicate that despite disease, signals from the retina can still be transmitted to the visual cortex for subsequent processing, further investigation into the capacity of neural plasticity will inform future therapy methods and visual restoration (Prins et al, 2016a; McGregor et al, 2020)

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