Reorganization of visual processing in macular degeneration: replication and clues about the role of foveal loss - PubMed (original) (raw)

Reorganization of visual processing in macular degeneration: replication and clues about the role of foveal loss

Chris I Baker et al. Vision Res. 2008 Aug.

Abstract

We previously reported large-scale reorganization of visual processing (i.e., activation of "foveal" cortex by peripheral stimuli) in two individuals with loss of foveal input from macular degeneration [Baker, C.I., Peli, E., Knouf, N., & Kanwisher, N. G. (2005). Reorganization of visual processing in macular degeneration. Journal of Neuroscience, 25(3), 614-618]. Here, we replicate this result in three new individuals. Further, we test the hypothesis that this reorganization is dependent on complete loss of foveal input. In two other individuals with extensive retinal lesions but some foveal sparing we found no evidence for reorganization. We conclude that large-scale reorganization of visual processing in MD occurs only in the complete absence of functional foveal vision.

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Figures

Figure 1

Figure 1

Samples of fixation stability measured with the Nidek MP-1. The blue dots represent 900 samples of the position of the fixation cross on the retina. A (Left). MD3's PRL fixation stability taken during an extended session of static perimetry (open squares represent invisible targets and filled square visible ones). Even during this extended and attention requiring task, fixation was stable (45% of the samples within 4 degrees), and the fixation cross was never closer than 10 degrees from the fovea. A (Right). MD3's PRL fixation stability during the fixation task (shown with the right eye to illustrate the correspondence of the PRLs between the eyes) was more stable (94% of the samples within 4 degrees). B (Left). MD7's central fixation stability with the residual left fovea demonstrating normal foveal fixation stability where 100% of the samples were within 4 degrees. B (Right). MD7's PRL fixation stability for the same subject was much less stable (26% of the samples within 4 degrees), yet it is obvious that the fixation cross was never closer than 10 degrees from the fovea.

Figure 2

Figure 2

Cortical flattening and the occipital cortical patch. Examples of cortical flattening in two control participants (top row, control for MD3; bottom row, control for MD5) showing the relationship between functional activation for foveal stimuli and the anatomically defined occipital pole ROI (white outline on flattened patch). The overlaid activation maps show areas with significantly greater activation for visual objects (top row, 3 × 3 degrees; bottom row, 3 × 4 degrees) presented at the fovea compared with a fixation baseline. The flattened representations of the occipital lobe were produced by first inflating the cortex, unfolding the sulci and gyri. A cut was then made along the fundus of the calcarine sulcus and the posterior cortex (including the occipital lobe) separated from the rest of the brain. Next, the occipital lobe patch was then flattened to produce the representations on which we displayed the activation data. The foveal confluence lies at the posterior end of the calcarine sulcus, near the occipital pole and is at the apex of the cut on the flattened cortical patch. The anatomically defined occipital pole ROI clearly overlaps the activation produced by foveal stimuli. The fundus of the calcarine sulcus separates the cortical representations of the upper and lower visual field. The representation of the lower visual field is dorsal to the fundus (above the foveal confluence on the patch), while the representation of the upper visual field is ventral to the fundus (below the foveal confluence on the patch). The eccentricity of the cortical representation increases as you move anteriorly from the posterior end of the calcarine sulcus (moving away from the foveal confluence on the patch in a direction parallel to the calcarine sulcus cut).

Figure 3

Figure 3

Large-scale reorganization of visual processing in three MD participants with extensive retinal lesions covering the fovea and matched control participants. Column 1. Schematic of visual fields in the left eye of each MD participant showing the large extent of the blind field (scotoma). MD3 and MD5 were tested with the right eye patched. MD4 was tested binocularly and the field loss in the right eye was very similar to that shown for the left eye. Column 2. Statistical parametric maps on the flattened cortex showing activation at the occipital pole (white outlines show the anatomically defined occipital pole ROI) for MD participants. The activation maps are displayed on the flattened cortex and show activation in response to visual objects presented at the PRL compared with the fixation baseline. In all three participants, the PRL was located in the left visual field, and data are shown for the right hemisphere only. In each case, activation was observed not only in parts of cortex corresponding to the retinal location of the PRL (white arrows), but also in the foveal confluence. Column 3. Bar charts showing percent signal change in the independently defined occipital pole ROI (white outlines). Stimuli presented at the PRL (red bars) elicited strong responses while stimuli presented at the fovea (blue bars) elicited little or no response. Column 4. Unlike the MD participants, in the control participants the flat maps show no activation at the occipital pole for stimuli presented to peripheral retina (corresponding to the matched MD participant's PRL). Column 5. Percent signal change in the occipital pole ROI for control participants shows a strong response to foveal stimuli but no response to peripheral stimuli.

Figure 4

Figure 4

Time course of activation at the occipital pole ROI for MD3, MD4, MD5, and matched controls. Average time course of visually active voxels in the occipital pole ROI for MD participants (left column) and matched controls (right column). In each participant, voxels within the occipital pole ROI responsive to either foveal or peripheral stimuli (relative to fixation baseline) were selected using half of the total data collected. Independent time courses were plotted by averaging data from those voxels using the other half of the data. In each MD participant, there is a strong increase in activation relative to the fixation baseline for stimuli presented at the PRL (red lines) over the course of the blocks. In contrast stimuli presented at the fovea (blue lines) elicited little or no change in the activation over time. The opposite pattern was observed in the matched control participants: large increases in activation over the course of the blocks for foveal stimuli but no or even small decreases in activation over time for stimuli presented in the periphery.

Figure 5

Figure 5

Lack of large-scale reorganization in two MD participants with foveal sparing and a matched control participant. Column 1. Schematic of visual fields in the left eye of MD6 and MD7. Visual fields in the other eye for both patients were similar, both showing some residual central foveal vision. The right eye of each participant was patched. Column 2. Statistical parametric maps on the flattened cortex showing activation in both hemispheres in response to visual objects presented at the PRL compared with the fixation baseline. In both participants, the PRL was located on the vertical mid-line and ROI data are shown for both hemispheres. In both participants, while activation was observed in parts of cortex corresponding to the PRL location (white arrows), no activation was observed at the occipital pole. Column 3. Bar charts showing percent signal change in the occipital pole ROI in the left (light bars) and right (dark bars) hemispheres. Stimuli presented at the fovea (blue bars) elicited small but significant responses while stimuli presented at the PRL (red bars) elicited little or no response. Column 4. Statistical parametric map showing activation elicited by peripheral stimuli compared with the fixation baseline for matched control participant. Similar to MD6 and MD7, the flat maps show no activation at the occipital pole for stimuli presented to peripheral retina. Column 5. Percent signal change in the occipital pole ROI shows a strong response to foveal stimuli but no response to peripheral stimuli. Color scale for statistical parametric maps is the same as in Figure 3.

Figure 6

Figure 6

Time course of activation at the occipital pole for MD6 and MD7 and matched control. In both MD participants (left column), stimuli presented at the fovea (blue lines) elicited weak increases in activation relative to the fixation baseline in both the right (solid lines) and left hemisphere (dotted lines). In contrast to MD3, MD4 and MD5, however, stimuli presented at the PRL (red lines) elicited weak decreases or little change in activation relative to fixation over the course of the blocks, and the activation for foveal stimuli was greater than for peripheral stimuli. In the matched control participant, while the change in activation for foveal stimuli was much stronger than in MD6 and MD7, since there was no damage to the fovea, the same qualitative pattern was observed.

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