Plasticity and stability of the visual system in human achiasma

Abstract

The absence of the optic chiasm is an extraordinary and extreme abnormality in the nervous system. The abnormality produces highly atypical functional responses in the cortex, including overlapping hemifield representations and bilateral population receptive fields in both striate and extrastriate visual cortex. Even in the presence of these large functional abnormalities, the effect on visual perception and daily life is not easily detected. Here, we demonstrate that in two achiasmic humans the gross topography of the geniculostriate and occipital callosal connections remains largely unaltered. We conclude that visual function is preserved by reorganization of intracortical connections instead of large-scale reorganizations of the visual cortex. Thus, developmental mechanisms of local wiring within cortical maps compensate for the improper gross wiring to preserve function in human achiasma.

Figure 1

Hemifield retinotopic mapping results. A) Schematic of the normal projection pattern of the optic nerve of the right eye together with the visual contracting ring stimulus for hemifield eccentricity and its color-coded lateralized representation in a schematic V1-flatmap. The nasal retina (blue) projects to the contralateral and the temporal retina (red) to the ipsilateral hemisphere, resulting in a representation of each hemifield on its respective contralateral hemisphere. B) Schematic of the achiasmic optic nerve projection and eccentricity maps in AC1’s flattened representation of the early visual areas upon separate monocular stimulation of the right eye in the left and right visual hemifield. Responses are dominant in the right hemisphere and organized as an orderly eccentricity map for both visual hemifields. The visual area boundaries are indicated as determined from polar angle mapping (supplementary Figure S1). C) Correlation of the respective hemifield mappings to quantify the cortical superposition of hemifield maps in right V1 (mean±SD across four controls and for AC1 across repetitive correlations). In the controls the two repetitions of contralateral hemifield mappings were correlated (p<0.01) and, to a lesser degree (p<0.04), also those of two repetitions of ipsilateral hemifield mappings, but, in contrast, not those of contra- and ipsilateral field mappings. For AC1 both contra- and ipsilateral field mappings were highly correlated (p<0.001). See also supplementary Figure S1.

Figure 2

Population receptive field modelling results. A) pRF model comparisons for AC1 and AC2 (left and right, respectively) and two control subjects at the respective measurement sites. The mean variance explained and 95% confidence intervals for fMRI responses in the right Calcarine sulcus are shown for four different pRF models. Only cortical locations where any model explains more than 50% of the variance are included the analysis. However the results are near-identical for any other or no threshold. Four different models were tested: the conventional pRF model containing 1 Gaussian, and three different pRF models with 2 Gaussians where the Gaussians are mirrored around the y-axis, fixation or x-axis. The pRF models are indicated by the x-axis’ cartoon representations. There is no difference in degrees of freedom in the models. In the right hemisphere of the achiasmic subjects, the model containing 2 pRFs mirrored around the y-axis explains most of the variance. In control subjects, the conventional model explains most of the variance in the data. Two example pRF model fits are shown in panels B and C. These panels show the fMRI data of AC2 (dotted line) fitted (solid line) with a conventional pRF using a single Gaussian (B) and a 2 Gaussian pRF model (C). The insets indicate the particular pRF model that is fitted to the data and the variance explained (r²). The conventional pRF model consistently misses certain time-series features that are captured by the 2 Gaussian pRF model (gray arrows). Next we compare the conventional pRF model to the pRF model consisting of 2 Gaussians mirrored on the y-axis by subtracting the variance explained of either model. The difference in percent variance explained of both models is shown on the cortical surfaces of AC2 (D) and a control subject (E). The data that is shown has at least a variance explained of 30% in any pRF model. The dashed white lines indicate the V1-V2 border (vertical meridian or Y-axis). In the subject without an optic chiasm the pRF model with two Gaussians mirrored on the Y-axis explains most of the variance within and beyond V1, whereas the in the control subject the conventional model explains most of the variance in the fMRI data. F) pRF size versus eccentricity in the right Calcarine sulcus of AC2 and 4 control subjects. In the control subjects pRF sizes increase with eccentricity (Dumoulin and Wandell, 2008). This relationship is also plotted for the subject without an optic chiasm for two pRF models (conventional model: open circles; pRF model consisting of two Gaussians mirrored on the Y-axis: closed circles). The pRF sizes of the conventional pRF model deviate from the known relationship between (p)RF size and eccentricity in humans and animals, but the pRF sizes of the novel two Gaussian pRF model are consistent with the known relationship as illustrated by control subjects. See also supplementary Figure S2.

Figure 3

Diffusion tensor imaging (DTI) and tractography results of AC2 and 30 controls. A) ROIs and estimated fiber bundles superimposed on the T1 weighted axial slice, viewed from below. Estimates of the right (red) and left (blue) optic tracts; the right (pink) and left (purple) optic radiations; the right (dark red) and left (dark blue) occipital callosal fibers. Yellow spheres represent the optic chiasm (large anterior) LGN’s (small in the middle) and Calcarine sulcus (posterior) regions of interest. (B) Scatter plot of the radial and longitudinal diffusivities of the optic tract, optic radiation and occipital callosal fiber groups (see color legend on the right). The 2 standard deviation covariance ellipsoid of 30 normally sighted subjects is drawn for each fiber group. The black stars represent the averaged right and left diffusivity values for each fiber group in the achiasmic subject which are within the range of control subjects. (C) The location of the occipital callosal fibers in the plane of the corpus callosum. (D) Scatter plot of the cross-sectional area of the occipital callosal fiber group in relation to the cross-sectional area of the entire corpus callosum. The cross-sectional area of achiasmic occipital callosal fiber group (purple star) is small compared to the controls (grey diamonds); however, the overall size of AC2’s corpus callosum is small too.