Primary visual cortical remapping in patients with inherited peripheral retinal degeneration

Abstract

Human studies addressing the long-term effects of peripheral retinal degeneration on visual cortical function and structure are scarce. Here we investigated this question in patients with Retinitis Pigmentosa (RP), a genetic condition leading to peripheral visual degeneration. We acquired functional and anatomical magnetic resonance data from thirteen patients with different levels of visual loss and twenty-two healthy participants to study primary (V1) visual cortical retinotopic remapping and cortical thickness. We identified systematic visual field remapping in the absence of structural changes in the primary visual cortex of RP patients. Remapping consisted in a retinotopic eccentricity shift of central retinal inputs to more peripheral locations in V1. Importantly, this was associated with changes in visual experience, as assessed by the extent of the visual loss, with more constricted visual fields resulting in larger remapping. This pattern of remapping is consistent with expansion or shifting of neuronal receptive fields into the cortical regions with reduced retinal input. These data provide evidence for functional changes in V1 that are dependent on the magnitude of peripheral visual loss in RP, which may be explained by rapid cortical adaptation mechanisms or long-term cortical reorganization. This study highlights the importance of analyzing the retinal determinants of brain functional and structural alterations for future visual restoration approaches.

Keywords: FPZ, Function Projection Zone; Functional magnetic resonance imaging (fMRI); Human; LE, Left Eye; LH, Left Hemisphere; LPZ, Lesion Projection Zone; MRI, Magnetic Resonance Imaging; Plasticity; Primary visual cortex; RE, Right Eye; RH, Right Hemisphere; RNFL, Retinal Nerve Fiber Layer; RP, Retinitis Pigmentosa; Reorganization; Retinitis pigmentosa; Retinotopy; fMRI, functional Magnetic Resonance Imaging.

Fig. 1

Representation of the left eye lesions (scotomata) measured with static perimetry on the left side of the figure (vertical and horizontal axis represent visual field extent in degrees; the gray scale represents visual field sensitivity in dB), and right hemisphere retinotopic eccentricity maps on the right side of the figure (Linear Correlation Maps, r > 0.25; inflated hemisphere mesh; the color scale represents visual field eccentricity in degrees) for all patients and one control participant. Right eye scotomata and left hemisphere eccentricity maps were very similar to the ones presented, thus, their images were not displayed in this figure. RP = Retinitis Pigmentosa, LE = Left Eye.

Fig. 2

Representation of the eight eccentricity rings stimuli in the visual field and their respective cortical representation in the right hemisphere (multi-study General Linear Model, p < 0.050; average group mesh). Cortical responses for Retinitis Pigmentosa and control groups are shown for each eccentricity ring, as well as the response contrast between the two groups. The color bar represents the t-values from the General Linear Model. RP = Retinitis Pigmentosa; OP = Occipital Pole.

Fig. 3

Ratio between the cortical distance to the occipital pole of the eight eccentricity rings' representation along the calcarine sulcus and the length of calcarine sulcus for patients' and controls' groups in both hemispheres (in left side of the figure). The distances were higher for the Retinitis Pigmentosa group as compared to control participants (Linear Mixed Model, F_(1,32.09) = 5.63, p = 0.024). The right side of the figure represents the same distance for RP A (with < 15 deg of visual field diameter) and RP B (with > 15 deg of visual field diameter) patients' subgroups and the control group, with augmented distances for subgroup RP A (Linear Mixed Model, F_(2,31.01) = 5.33, p = 0.010) when compared to RP B patients and the control group. Error bars represent data standard error. RP = Retinitis Pigmentosa.

Fig. 4

Ratio between primary visual cortical thickness and the average hemisphere thickness for the Lesion Projection Zone (LPZ) and Function Projection Zone (FPZ) regions in the calcarine sulcus for patients' and controls' groups in both hemispheres. RP A patients (with < 15 deg of visual field diameter) presented augmented left cortical thickness in the FPZ in comparison to RP B patients (with > 15 deg of visual field diameter) [*statistical significance with t = 3.25 and p = 0.003]. RP = Retinitis Pigmentosa.