Visual space and object space in the cerebral cortex of retinal disease patients

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Abstract

The lower areas of the hierarchically organized visual cortex are strongly retinotopically organized, with strong responses to specific retinotopic stimuli, and no response to other stimuli outside these preferred regions. Higher areas in the ventral occipitotemporal cortex show a weak eccentricity bias, and are mainly sensitive for object category (e.g., faces versus buildings). This study investigated how the mapping of eccentricity and category sensitivity using functional magnetic resonance imaging is affected by a retinal lesion in two very different low vision patients: a patient with a large central scotoma, affecting central input to the retina (juvenile macular degeneration), and a patient where input to the peripheral retina is lost (retinitis pigmentosa). From the retinal degeneration, we can predict specific losses of retinotopic activation. These predictions were confirmed when comparing stimulus activations with a no-stimulus fixation baseline. At the same time, however, seemingly contradictory patterns of activation, unexpected given the retinal degeneration, were observed when different stimulus conditions were directly compared. These unexpected activations were due to position-specific deactivations, indicating the importance of investigating absolute activation (relative to a no-stimulus baseline) rather than relative activation (comparing different stimulus conditions). Data from two controls, with simulated scotomas that matched the lesions in the two patients also showed that retinotopic mapping results could be explained by a combination of activations at the stimulated locations and deactivations at unstimulated locations. Category sensitivity was preserved in the two patients. In sum, when we take into account the full pattern of activations and deactivations elicited in retinotopic cortex and throughout the ventral object vision pathway in low vision patients, the pattern of (de)activation is consistent with the retinal loss. © 2014 Goesaert et al.

Figures

  • Figure 1. Stimulus set filtered with simulated retinal defects. (A) Example of the stimulus set under normal viewing conditions (B) Stimulus set for the JMD control study. Most conditions show a blank screen, with the five most eccentric stimuli showing part of the rings. (C) Stimulus set for the RP control study. The shift between the visible and not visible stimuli is more gradual, with input present in a large part of the stimulus sequence. Only the most eccentric stimuli are not visible any more. doi:10.1371/journal.pone.0088248.g001
  • Figure 2. Schematic view of the scanner screen for both patients in the eccentricity mapping paradigm. (A) schematics for the RP patient, with fixation point (blue square) in the centre of the screen. The grey circle represents the extent of the eccentric stimuli, and the blue lines mark the edges of the remaining visual field. Outside these borders the parts of the stimuli that fall outside the remaining visual field are marked in a lighter grey. (B) schematics for the JMD patient. The fixation point is located in the lower left corner, about 5u away from the lower edge of the scotoma. The scotoma (marked with blue lines) covers the centre of the screen, and is slightly larger at the left. The most eccentric stimuli are visible in the right part of the screen (shown in gray). doi:10.1371/journal.pone.0088248.g002
  • Figure 3. Relative preference for different eccentricities in lower visual areas without a simulated scotoma. The medial view of the posterior part of right and left hemisphere is shown on an inflated cortical surface for control 2. The approximate location of the calcarine sulcus is marked with a dotted line. The color legend is shown above (orange-red for central stimuli, green for paracentral stimuli, blue-purple for peripheral stimuli). doi:10.1371/journal.pone.0088248.g003
  • Figure 4. Preference and activity patterns for different eccentricities in lower visual areas for the JMD patient. (A) The medial view of the posterior part of right and left hemisphere is shown on an inflated cortical surface. The approximate location of the calcarine sulcus is marked with a dotted line. The color legend is shown above (orange-red for central stimuli, green for paracentral stimuli, blue-purple for peripheral stimuli) and reflects the relative preference to the different eccentricities. In black two regions are marked which are further characterized for illustration purposes. The data of one region (red arrow/box) are mostly dominated by a positive response, and for the other region (blue arrow/box) mostly by a negative response compared to a no-stimulus baseline (B) Activity patterns in both hemispheres compared to a fixation baseline, at p,0.05 uncorrected for one of three conditions: central (8 most central stimuli, contrasted against baseline), paracentral (8 paracentral stimuli, contrasted against baseline) and peripheral (8 most eccentric stimuli, contrasted against baseline). The selected ROIs now show the underlying positive and negative responses. (C) Time course averaged across runs and across stimulus sequences to represent the response in a selected ROI to different eccentricities. The red dotted lines represent the 95% confidence intervals (calculated using the variation across runs). (C, left panel) ROI with a small positive response to peripheral stimuli compared to a fixation baseline and negative responses to the other conditions (C, right panel) ROI with a close to zero response to central stimuli and negative responses to the other conditions.(D) Average beta values in each selected ROI. The left panel indicates activity of a ROI that shows a small positive response to the (visible) peripheral stimuli, while the right panel shows a ROI with negative responses to unstimulated parts of the visual field and the absence of activation in the central condition. doi:10.1371/journal.pone.0088248.g004
  • Figure 5. Preference and activity patterns for different eccentricities in lower visual areas for the JMD controls. (A) The medial view of the posterior part of right and left hemisphere is shown on an inflated cortical surface for the two controls (control 1: upper figure, control 2: lower figure). They were tested with the stimulus set simulating the JMD scotoma. The approximate location of the calcarine sulcus is marked with a dotted line. The color legend is shown above (orange-red for central stimuli, green for paracentral stimuli, blue-purple for peripheral stimuli) and reflects the relative preference to the different eccentricities. In black two regions are marked which are further characterized for illustration purposes. The data of one region (red arrow/box) are mostly dominated by a positive response, and for the other region (blue arrow/box) mostly by a negative response compared to a no-stimulus baseline. (B) Average beta values in each selected ROI. The red arrows and box indicate activity of a ROI that shows a positive response to the (visible) peripheral stimuli, while the blue arrows and box show a ROI where negative responses to unstimulated central parts of the visual field cause a phase preference in the absence of activation in the other conditions. doi:10.1371/journal.pone.0088248.g005
  • Figure 6. Preference and activity patterns for different eccentricities in lower visual areas for the RP patient. (A) The medial view of the posterior part of right and left hemisphere is shown on an inflated cortical surface. The approximate location of the calcarine sulcus is marked with a dotted line. The color legend is shown above (orange-red for central stimuli, green for paracentral stimuli, blue-purple for peripheral stimuli) and reflects the relative preference to the different eccentricities. In black two regions are marked which are further characterized for illustration purposes. The data of one region (red arrow/box) are mostly dominated by a positive response, and for the other region (blue arrow/box) mostly by a negative response compared to a no-stimulus baseline (B) Activity patterns in both hemispheres compared to a fixation baseline, at p,0.05 uncorrected for one of three conditions: central (8 most central stimuli, contrasted against baseline), paracentral (8 paracentral stimuli, contrasted against baseline) and peripheral (8 most eccentric stimuli, contrasted against baseline). The selected ROIs now show the underlying positive and negative responses. (C) Time course averaged across runs and across stimulus sequences to represent the response in a selected ROI to different eccentricities. The red dotted lines represent the 95% confidence intervals (calculated using the variation across runs). (C, left panel) A positive response to the most central stimuli, with a strong drop in activation to a near zero response when more eccentric stimuli are presented (C, right panel) Strong deactivations for the central and paracentral stimuli, and a response close to zero for the peripheral stimuli (D) Average beta values in each selected ROI. (D, left panel) Positive responses in the central and paracentral conditions, and a near zero response in the peripheral condition. (D, right panel) Negative responses (beta values) for the (para)central conditions and a near zero response to the peripheral condition. doi:10.1371/journal.pone.0088248.g006
  • Figure 7. Preference and activity patterns for different eccentricities in lower visual areas for the RP controls. (A) The medial view of the posterior part of right and left hemisphere is shown on an inflated cortical surface for the two controls (control 1: upper figure, control 2: lower figure). They were tested with the stimulus set simulating the RP scotoma. The approximate location of the calcarine sulcus is marked with a dotted line. The color legend is shown above (orange-red for central stimuli, green for paracentral stimuli, blue-purple for peripheral stimuli) and reflects the relative preference to the different eccentricities. In black two regions are marked which are further characterized for illustration purposes. The data of one region (red arrow/box) are mostly dominated by a positive response and for the other region (blue arrow/box) mostly by a negative response compared to a no-stimulus baseline (B) Average beta values in each selected ROI. The red arrows and box indicate activity of a ROI that shows a positive response to the (visible) central stimuli, while the blue arrows and box show a ROI where negative responses to unstimulated peripheral parts of the visual field cause a phase preference in the absence of activation in the other conditions. doi:10.1371/journal.pone.0088248.g007
  • Figure 8. Preference and activity patterns for different eccentricities in the ventral cortex with central (simulated) scotoma. (Left) Relative preference in the eccentricity mapping paradigm for the JMD patient (A), control 1 (C) and control 2 (E), shown on an inflated hemisphere. The color legend is shown above (orange-red for central stimuli, green for paracentral stimuli, blue-purple for peripheral stimuli). The black lines mark the face-sensitive areas (FA), the red lines mark the house (place)-sensitive areas (PA) defined by the blocked localizer design. (Right) average beta values of three conditions, when the eccentricity data are analyzed as a block design and compared to a fixation baseline, in both the FA and PA region for the JMD patient (B), control 1 (D) and control 2 (F). doi:10.1371/journal.pone.0088248.g008

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Goesaert, E., Van Baelen, M., Spileers, W., Wagemans, J., & Op De Beeck, H. P. (2014). Visual space and object space in the cerebral cortex of retinal disease patients. PLoS ONE, 9(2). https://doi.org/10.1371/journal.pone.0088248

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