Organization of the visual cortex in human albinism

Abstract

In albinism there is an abnormal projection of part of the temporal retina to the visual cortex contralateral to the eye. This projection, together with the normally routed fibers from nasal retina, provides a cortical hemisphere with visual input from more than the normal hemifield of visual space. In many mammalian models of albinism, a possible sensory mismatch in the visual cortex is avoided either by reorganization of the thalamocortical connections to give the abnormal input an exclusive cortical representation, or by the abnormal input being substantially suppressed. In this study we examine, with fMRI, how the human visual cortex topographically maps its input in albinism. We find that the input from temporal retina is not substantially suppressed and forms a retinotopic mapping that is superimposed on the mapping of the nasal retina in striate and extrastriate areas. The abnormal routing of temporal fibers is not total, with the line of decussation shifting to between 6 and 14 degrees into temporal retina. Our results indicate that the abnormal input to visual cortex in human albinism does not undergo topographic reorganization between the thalamus and cortex. Furthermore, the abnormal input is not significantly suppressed in either striate or extrastriate areas. The topographic mapping that we report in human does not conform, therefore, to the commonly observed patterns in other mammals but takes the form of the "true albino" pattern that has been reported rarely in cat and in the only other individual primate studied.

Figure 2.

Schematic of the projection of the temporal and nasal retina of one eye in a normal control (left) and a subject with albinism (right). In the top row schematics of the stimuli are given; the corresponding false color map of the eccentricities in the visual field is shown underneath together with an indication of the position of the line of decussation (dotted lines). The projection of the optic nerves is indicated in the third row, with the inferred representation of the nasal and temporal retina in a model of V1 shown underneath. In modeling the albino cortical maps, it is assumed that cortical input from misrouted temporal retina is mirrored onto the normal input from nasal retina. This figure demonstrates that, in the albino condition, a shift of the line of decussation into the temporal retina results in a cortical pattern similar to that which has been demonstrated in albino A1 (bottom right).

Figure 3.

Mapping of the representation of the polar angles in the visual field on the occipital cortex contralateral to the stimulated eye in two control subjects (C1 and C2, bottom row) after stimulation of the nasal retina and in four albino subjects (A1-4) after stimulation of the nasal (top row) and temporal (middle row) retina. Cortical activity (c > 0.20 and c > 0.15) is plotted in false color on flattened representations of the right occipital lobes. The false color indicates the phase of the cortical response and therefore the polar angle to which that part of the cortex responds. A color key indicating polar angle and schematics of the stimuli is given at the bottom right. The positions of the reversals of the phase progressions on the flattened representations allow visual area boundaries to be identified. These boundaries were determined after stimulation of the nasal retina of the left eye (black lines). There is a correspondence of these boundaries, especially in V1, to those obtained after stimulation of the temporal retina of the albino subjects.

Figure 1.

Mapping of the representation of visual field eccentricities on the occipital cortex in two control (C1 and C2, to the left) and four albino (A1-4, to the right) subjects. Stimulation was through one eye; this and subsequent figures are drawn as if stimulation was through the left eye. For each subject, cortical activity (correlation coefficient >0.20) is plotted in false color on the flattened representations of the left and right occipital lobes. The false color indicates the phase of the cortical response and therefore the eccentricity to which that part of the cortex responds. A color key indicating eccentricity and schematics of the stimuli are given at the right. The first and third row represent the responses after stimulation of the nasal retina, whereas the second and forth row represent the responses after stimulation of the temporal retina. The upper and lower bank (white dashed lines) and the fundus (black dashed lines) of the calcarine sulcus are highlighted as cortical landmarks delimiting primary visual cortex. In the control subjects the activity is dominant on the hemisphere contralateral to the stimulated hemifield. In the albino, the activity is dominant on the hemisphere contralateral to the stimulated eye for stimulation of both nasal and temporal retina. Although this albino misrouting can be found for the central visual field, the projection reverts to the normal pattern for the eccentric representation (see Results for details).

Figure 4.

BOLD signal (mean of 2 × 6 cycles ± SEM) on the right hemisphere after stimulation of the nasal and temporal retina of the left eye. ROI for traces in left and right column cover lower and upper bank of calcarine sulcus, respectively. For details of ROI definition see Results. In albinos and controls, stimulation of the nasal retina results in a strong response (thin traces), which differs in phase for the lower and upper bank of the calcarine (top and bottom row, respectively). After stimulation of the temporal retina, this activity is strongly reduced in the control subjects, whereas it is still prominent in the subjects with albinism (thick traces in each panel).

Figure 5.

A, Frequency distributions of the separations of nasal and temporal retinal coordinates of voxel receptive field locations (see Results for details). Data are given for voxels in V1 for four albino subjects as indicated in the legend. A range for the control distributions is given (±1 SD, 4 hemispheres) for two different comparisons: one when stimulation was repeated in the same hemi-retina and the other for stimulation of different hemi-retinas. B, Cross-study comparison of the mirror-symmetrical superposition of the cortical representation of the normal input from nasal retina and of the abnormal input from temporal retina in humans (number of subjects, n = 4; number of units, m = 679), monkey (n = 1; m = 30), and cats with albinism (n = 2; m = 18). The proportion of units as a function of the eccentricity difference (receptive field separation) between the two maps is plotted according to Figure 5A.

Figure 6.

The mean fMRI signal amplitude after nasal (normal projection, filled bars) and temporal retinal stimulation (abnormal projection, open bars). The average response strength of the four albino subjects is depicted (mean ± 1 SD). Data are given for striate cortex and for extrastriate cortex that includes V2 and V3.