Cortical lateralization of cheirosensory processing in callosal dysgenesis

Abstract

The paradoxical absence of a split-brain syndrome in most cases of callosal dysgenesis has originated three main hypotheses, namely, (i) bilateral cortical representation of language, (ii) bilateral thalamocortical projections of somatosensory pathways conveyed by the spinothalamic-medial lemniscus system, and (iii) a variable combination of (i) and (ii). We used functional neuroimaging to investigate the cortical representation and lateralization of somatosensory information from the palm of each hand in six cases of callosal dysgenesis (hypothesis [ii]). Cortical regions of interest were contralateral and ipsilateral S1 (areas 3a and 3b, 1 and 2 in the central sulcus and postcentral gyrus) and S2 (parts of areas 40 and 43 in the parietal operculum). The degree of cortical asymmetry was expressed by a laterality index (LI), which may assume values from -1 (fully left-lateralized) to +1 (fully right-lateralized). In callosal dysgenesis, LI values for the right and the left hands were, respectively, -1 and + 1 for both S1 and S2, indicating absence of engagement of ipsilateral S1 and S2. In controls, LI values were - 0.70 (S1) and - 0.51 (S2) for right hand stimulation, and 0.82 (S1) and 0.36 (S2) for left hand stimulation, reflecting bilateral asymmetric activations, which were significantly higher in the hemisphere contralateral to the stimulated hand. Therefore, none of the main hypotheses so far entertained to account for the callosal dysgenesis-split-brain paradox have succeeded. We conclude that the preserved interhemispheric transfer of somatosensory tactile information in callosal dysgenesis must be mediated by a fourth alternative, such as aberrant interhemispheric bundles, reorganization of subcortical commissures, or both.

Keywords: Callosal dysgenesis; Somatosensory cortical lateralization; fMRI callosal agenesis.

Graphical abstract

Fig. 1

Sagittal slices showing the anatomical types of callosal dysgenesis that took part in this study: (A) agenesis (N = 2), (B) partial agenesis (N = 2), and (C) hypoplasia (N = 2).

Fig. 2

Somatosensory activation in patients with CD (top) and controls (bottom) in response to unilateral exteroceptive hand stimulation. Activations in (a) and (b) are significant at p < .05, familywise error, corrected. Coordinates and activations plotted on the Montreal Neurological Institute standard brain. Color bar represents t-values of activations. L: left; R: right.

Fig. 3

Increased brain activation in controls when compared to CD patients in response to unilateral exteroceptive hand stimulation. Activations in (a) and (b) are significant at p < .001, cluster size of 5 voxels. Coordinates and activations plotted on the Montreal Neurological Institute standard brain. Color bar represents t-values of activations. L: left; R: right.

Fig. 4

Laterality indexes based on number of activated voxels (p < .05, familywise error corrected for multiple comparisons at cluster level) may range from −1 (fully left-lateralized) to +1 (fully right-lateralized).

Fig. 5

MNI: Montreal Neurological Institute coordinates for significant activation maxima of clusters in group analyses (p < .05, familywise error corrected for multiple comparisons on the cluster level). Cheirosensory cortical engagement in patients with CD differed from that of controls in their overall lower level of activation and because they were exclusively contralateral

Fig. S1

Same as Fig. 2, except that p-values <.001.