Cortical plasticity and preserved function in early blindness

Abstract

The "neural Darwinism" theory predicts that when one sensory modality is lacking, as in congenital blindness, the target structures are taken over by the afferent inputs from other senses that will promote and control their functional maturation (Edelman, 1993). This view receives support from both cross-modal plasticity experiments in animal models and functional imaging studies in man, which are presented here.

Keywords: Congenital blindness; Cortical reorganization; Cross-modal plasticity; Functional neuroimaging; Visual deprivation.

Figure 1

Expansion of whisker-barrel system in blind mice. The size of barrels in the somatosensory cortex was compared in mouse pups that were reared with normal vision or with eyes surgically removed immediately after birth. The graph displays the size distribution of all barrels in the two groups. In the blind littermates barrel size was enlarged by up to 20%. The largest barrels were even larger in the binocularly deprived animals, which causes their distribution to be shifted to the right (P< 0.0001; t test). Comparisons within and between litters of the same group did not show any significant differences (adapted from Rauschecker et al., 1992).

Figure 2

Sound localization in binocularly deprived (BD) and normal cats. The experimental setup is shown in (a) with azimuth positions 1 to 8 in clockwise fashion, with sham speakers in between. The bottom panel (b) displays the precision of sound localization at the eight positions in terms of mean variance (precision is related inversely to the width of the distribution of sound localization error). The results demonstrate that all cats were more precise in localizing straight ahead than rear positions, but blind cats were more precise than sighted cats at practically every position (p<0.002, two-way ANOVA) (adapted from Rauschecker, 1995 and Rauschecker and Kniepert, 1994). (c) Schematic display of crossmodal plasticity determined by electrophysiological mapping in binocularly deprived and normal cats. The extent of sensory cortical representations in the cat is shown after normal development (a, b) and after extended periods of binocular visual deprivation (c, « blind »). The schematic displays are based on track reconstructions from single-unit recordings in both normal and blind cats, in which the sensory modality of the neurons was determined (from Rauschecker and Korte; 1993). Significant expansion of auditory and somatosensory cortical regions is seen in visually deprived cats (adapted from Rauschecker, 1995).

Figure 3

Between-group comparison for the auditory modality. In orange-yellow the brain areas that were activated more in early blind subjects than in blindfolded sighted controls during auditory identification and localization tasks, whereas the blue-green zones are those that are more recruited in sighted subjects performing the same auditory processing tasks on the same stimuli. Activation maps are resulting from a random-effects (RFX) between-group comparison with a threshold of p < 0.05 corrected for multiple comparisons. The color-gradient scale codes the t value (adapted from Renier et al., 2010).

Figure 4

In subjects who are blind from birth, the brain adapts itself and « re-uses » cortical areas that are normally devoted to visual abilities, in order to develop auditory and tactile abilities. During fMRI, subjects were provided with sounds or vibrotactile stimuli and were requested to identify, to localize, or simply detect them. The task comparison shows that the occipital cortex of blind subjects, devoid of visual function from birth, does reorganize itself to process these stimuli and the cortical reorganization follows the same architecture as the one of sighted subjects. In particular, the right middle occipital gyrus (MOG) is recruited to localize the stimuli, whether auditory or tactile, in early blind subjects, whereas the same region is only recruited to localize visual stimuli in sighted subjects, as shown by the activity profiles (adapted from Renier et al., 2010).

Figure 5

PET imaging evidence in blind humans that auditory-triggered mental imagery of shape (IMAG) contrasted to a control auditory task (CONT) recruits the ventral “visual” pathway in these subjects. The statistical parametric map for this comparison is superimposed on an individual normalized MRI displaying the anterior, right and medial surfaces (first row), and the posterior, left and medial surfaces (second row). The results show bilateral activation of occipito-temporal brain areas in early blind subjects. The cursor lines indicate a voxel in the left fusiform gyrus with a Z-value of 5.0 (p<0.05 corrected for multiple comparisons, coordinates with reference to the Talairach system). (adapted from De Volder et al., 2001).