Reorganization of visual processing in macular degeneration

Abstract

Macular degeneration (MD), the leading cause of visual impairment in the developed world, damages the central retina, often obliterating foveal vision and severely disrupting everyday tasks such as reading, driving, and face recognition. In such cases, the macular damage eliminates the normal retinal input to a large region of visual cortex, comprising tens of square centimeters of surface area in each hemisphere, which is normally responsive only to foveal stimuli. Using functional magnetic resonance imaging, we asked whether this deprived cortex simply becomes inactive in subjects with MD, or whether it takes on new functional properties. In two adult MD subjects with extensive bilateral central retinal lesions, we found that parts of visual cortex (including primary visual cortex) that normally respond only to central visual stimuli are strongly activated by peripheral stimuli. Such activation was not observed (1) with visual stimuli presented to the position of the former fovea and (2) in control subjects with visual stimuli presented to corresponding parts of peripheral retina. These results demonstrate large-scale reorganization of visual processing in MD and will likely prove important in any effort to develop new strategies for rehabilitation of MD subjects.

Figure 1.

Schematic diagram indicating visual fields in the left eyes of MD1 and MD2. Only the central 44 × 30° (deg) is shown. In MD1, all retina outside this region is functional; in MD2, some functional retina exists outside this region.

Figure 2.

Activation of visual cortex (stimuli greater than baseline) in MD and control subjects (experiment 1). a, Ventral and medial views of inflated right hemisphere of MD1. b, Flattened occipital cortex of MD1 showing activation at the foveal confluence. For a schematic diagram showing the typical organization of visual cortex on the flattened brain, see supplementary Figure 3 (available at www.jneurosci.org as supplemental material). c, Flattened occipital cortex of a control subject matched to MD1. Note the absence of positive activation at the foveal confluence for stimuli presented to peripheral retina (equivalent to MD1's PRL). d, Inflated right hemisphere of MD2. e, Flattened occipital cortex of the right hemisphere of MD2 showing activation in the foveal confluence. f, Flattened occipital cortex of a control subject matched to MD2. Note the absence of activation in the foveal confluence for stimuli presented to peripheral retina (equivalent to MD2's PRL). Arrows point to activations overlying cortex that would normally be responsive to peripheral stimuli presented at retinal locations corresponding to the PRLs. Scale bar, 20 mm.

Figure 3.

Visual activation in MD and control subjects to stimuli presented either at the fovea or at the PRL (experiment 2). a, Left hemisphere of MD1 and one control subject. Peripheral, but not foveal, stimuli elicited strong activation in foveal cortex in MD1. In contrast, foveal cortical activation was only observed with foveal presentation in the control subject. Scale bar, 10 mm. b, Time course of response in an anatomically defined ROI at the posterior end of the calcarine sulcus (dashed white outlines in a) in MD1 (top) and four control subjects (bottom). c, d, Average responses to peripheral stimuli in foveal cortical ROIs in MD and control subjects. For MD1 and controls, stimuli were presented at the midline, and data are shown from both hemispheres. For MD2 and controls, stimuli mainly landed in the left visual field, and data are shown for the right hemisphere only. Error bars indicate SE.