Hemifield columns co-opt ocular dominance column structure in human achiasma

Abstract

In the absence of an optic chiasm, visual input to the right eye is represented in primary visual cortex (V1) in the right hemisphere, while visual input to the left eye activates V1 in the left hemisphere. Retinotopic mapping In V1 reveals that in each hemisphere left and right visual hemifield representations are overlaid (Hoffmann et al., 2012). To explain how overlapping hemifield representations in V1 do not impair vision, we tested the hypothesis that visual projections from nasal and temporal retina create interdigitated left and right visual hemifield representations in V1, similar to the ocular dominance columns observed in neurotypical subjects (Victor et al., 2000). We used high-resolution fMRI at 7T to measure the spatial distribution of responses to left- and right-hemifield stimulation in one achiasmic subject. T₂-weighted 2D Spin Echo images were acquired at 0.8mm isotropic resolution. The left eye was occluded. To the right eye, a presentation of flickering checkerboards alternated between the left and right visual fields in a blocked stimulus design. The participant performed a demanding orientation-discrimination task at fixation. A general linear model was used to estimate the preference of voxels in V1 to left- and right-hemifield stimulation. The spatial distribution of voxels with significant preference for each hemifield showed interdigitated clusters which densely packed V1 in the right hemisphere. The spatial distribution of hemifield-preference voxels in the achiasmic subject was stable between two days of testing and comparable in scale to that of human ocular dominance columns. These results are the first in vivo evidence showing that visual hemifield representations interdigitate in achiasmic V1 following a similar developmental course to that of ocular dominance columns in V1 with intact optic chiasm.

Figure 1

Functional imaging slice placement, GLM results, and residual distortion. A) Coronal slices (gray overlay) covered a portion of occipital cortex, with 0.8 mm (isotropic) resolution. B) Cortical surfaces (thin lines) and results of GLM (stimulus on minus stimulus off, collapsing across left and right visual hemifield; orange indicates positive fMRI responses; blue, negative) are visualized on functional data after distortion compensation and registration to reference T1-weighted anatomy. In most places, there is excellent agreement between WM/GM/CSF contrast in EPI images and cortical surfaces. C) The crosshairs are centered on a region judged to have good alignment, and included in further analyses. However, large errors are also1 shown, where the GM surface (pink line) from the reference anatomy extends beyond the limit of the tissue seen in EPI data (indicated by *) and where WM surfaces (yellow line) fail to align to evident contrast in EPI data (+). Regions such as this were excluded from further analysis.

Figure 2

Coverage and activation maps for two scanning sessions. Average slice placement was slightly more posterior on Day 2, but functional responses in the posterior half of the calcarine were sampled on both days (left panel). Stringent inclusion criteria of individual voxel modulation with F_2,1199 > 4.609, p < 0.01 at all cortical depths for voxels with a volume of 0.5-mm³ resulted in exclusion of regions of the lower bank of the calcarine sulcus, where signal distortion was greatest, from further analysis (right panel). White box indicates regions where data are shown in subsequent figures.

Figure 3

Sensitivity and selectivity profiles for regions of V1 where responses were strong and EPI/T₁ (functional → anatomical) alignment was good. Sensitivity was computed as the average of the absolute values of the modulation in response to left and right hemifield checkerboard presentations (average magnitude of beta weights in GLM). Selectivity was defined as the difference in beta weights, divided by the sensitivity, with a positive number indicating a stronger response to stimuli in the left visual field. For this plot, the absolute value at each vertex/depth was taken before averaging. Data for the achiasmic participant (two different scanning sessions) are plotted in red; data for two control participants (two scanning sessions, each) are plotted in black.

Figure 4

Visualization of left and right hemifield responses at multiple depth samples in a patch of right V1 located on the dorsal side of the calcarine sulcus (white box, Fig. 2). Left column: data from Day 1; right column: data from Day 2. In each column, data are visualized on flattened surface patches spaced evenly between the white matter (WM, bottom row) and pial surface (pia, top row). Surface vertices at which functional responses were dominated by stimuli presented to the left visual hemifield are shown in green; right visual hemifield dominance is indicated by yellow; saturation indicates degree of dominance (fully saturated colors indicate responses that are 10% larger for one hemifield than the other).

Figure 5

Visualization of left- vs right-hemifield selectivity in the achiasmic participant. Surface vertices at which functional responses were dominated by stimuli presented to the left visual hemifield are shown in green; right visual hemifield dominance is indicated by yellow; saturation indicates degree of dominance (fully saturated colors indicate responses that are 10% larger for one hemifield than the other). Black fiducial lines mark identical locations on cortex in each panel. Top panel: data sampled at a single depth in the middle of the parenchyma. Bottom panels: composite images formed as weighted sums of the data from all depths, with strong weight given to regions with more power in a 2–3 cyc/mm frequency band.