Visual callosal topography in the absence of retinal input

Abstract

Using probabilistic diffusion tractography, we examined the retinotopic organization of splenial callosal connections within early blind, anophthalmic, and control subjects. Early blind subjects experienced prenatal retinal "waves" of spontaneous activity similar to those of sighted subjects, and only lack postnatal visual experience. In anophthalmia, the eye is either absent or arrested at an early prenatal stage, depriving these subjects of both pre- and postnatal visual input. Therefore, comparing these two groups provides a way of separating the influence of pre- and postnatal retinal input on the organization of visual connections across hemispheres. We found that retinotopic mapping within the splenium was not measurably disrupted in early blind or anophthalmic subjects compared to visually normal controls. No significant differences in splenial volume were observed across groups. No significant differences in diffusivity were found between early blind subjects and sighted controls, though some differences in diffusivity were noted between anophthalmic subjects and controls. These results suggest that neither prenatal retinal activity nor postnatal visual experience plays a role in the large-scale topographic organization of visual callosal connections within the splenium.

Keywords: Anophthalmia; Blind; Development; Diffusion tensor imaging; Plasticity; Tractography.

Figure 1. Definition of occipital ROIs

Left hemisphere cortical surface of a sighted subject showing the (A) dorsal (blue) and ventral (green) ROIs, as well as (B) the anterior (yellow), middle (orange), and posterior (red) ROIs. The yellow line in (A) and (B) represents the border of V1, defined by Freesurfer (see methods). The V1 ROI included the following cortical labels: 2 – G_and_S_occipital_inf ; 11 – G_cuneus ; 19 – G_occipital_middle ; 20 – G_occipital_sup ; 21 – G_oc-temp_lat-fusifor ; 22 – G_oc-temp_med-Lingual ; 43 – Pole_occipital ; 45 – S_calcarine ; 52 – S_collat_transv_post ; 58 – S_oc_middle_and_Lunatus ; 59 – S_oc_sup_and_transversal ; 60 – S_occipital_ant ; 61 – S_oc-temp_lat ; 62 – S_oc-temp_med_and_Lingual ; 66 – S_parieto_occipital (see (Destrieux et al., 2010) for label details). Insets show V1 from a medial view of the entire brain to aid in orienting the reader.

Figure 2. Calculation of projection probabilities

Splenial probabilistic maps for a single sighted subject, showing the (A) dorsal/ventral and (B) anterior/posterior maps. Anatomical directions are shown in (A). We used color maps where dorsal = blue [0 0 1] and ventral = green [0 1 0] such that if a voxel had a connectivity value of 0.9 to the ventral region and 0.1 to the dorsal region then it was assigned a green color value of 0.9 * [0 1 0] + 0.1 * [0 0 1]. The anterior-to-posterior classification was likewise labeled using a yellow-red scale: anterior = yellow [1 1 0], middle = orange [1 0.5 0], and posterior = red [1 0 0]. A linear ramp was fit to each map, shown in (C) and (D), resulting in a vector that represents the orientation (vector angle) and gradient (vector line length) of the (C) dorsal-to-ventral and (D) anterior-to-posterior splenial maps. A polar plot summarizing the resulting vectors for each map is found in (E).

Figure 3. Splenial and Callosal Volume

Scatter plot of the occipital callosal fiber volume in relation to the volume of the corpus callosum. While blind subjects tended to have relatively small callosal volumes as compared to sighted subjects, all but one anophthalmic subject fell within the normal range, as represented by a 2 standard deviation covariance ellipsoid (dotted line).

Figure 4. Summary polar plots

Left column: data from the left hemisphere of two control, two early blind, and two anophthalmic subjects. Individual Vector Plots: vectors representing the dorsal/ventral (blue) and anterior/posterior (red) maps for subjects in the left column. Summary Vector Plots: vectors representing maps from all subjects (both hemispheres) for each group; dashed lines indicate the average slope and orientation; shaded regions represent the standard error of the mean. Summary Orthogonality Plots: difference between the two map vectors (purple) for each subject (both hemispheres); lengths of lines indicate the average slope of the dorsal/ventral and anterior/posterior maps. In all other vector plots, lengths of lines indicate the slope of the gradient for that map, numbers indicate the orientation angle in degrees, inner dotted circles indicate a slope of 0.005, and outer circles indicate a slope of 0.01.

Figure 5. Timeline of human visual development

Dates are based on human and laboratory animal data (Clancy et al., 2007b).