Bilateral language representation in congenital callosal agenesis

Here, we report the results of fMRI during language comprehension in Congenital Callosal Agenesis (CCA), a very rare disconnection syndrome. In most humans, language is lateralized to the left side of the brain. Left-sided brain lesions acquired early in life may result in bilateral language representation. Therefore, bilateral development of usually distinct lateralized functions could be assumed as a compensatory mechanism. The presence of an intact and often hypertrophied anterior commissure in acallosal brains implicates that the increasing use of noncallosal commissures might be a further possible substitution.

Extensive neurological and neuropsychological examinations failed to exhibit pathological findings. Furthermore, an established test for cross-hemisphere transfer capabilities did not reveal the pattern of interferences seen in adults who have undergone callosotomy. In contrast to normal subjects fMRI revealed bilateral activity at perisylvian language areas, anterior insula and striatum. The findings of structural MRI and DTI are summarized in Figure 1. Assuming an increasing use of noncallosal commissures as a compensatory mechanism in acallosal brains could not be confirmed, whereas, bilateral development of usually distinct lateralized language functions as a possible compensatory mechanism in CCA could be corroborated by fMRI. The reason therefore might be that the developmental arrest occurs at an early stage of cortical growth, well before the association fibres from each cortical plate begin crossing the midline to connect contralateral hemispheric regions. One may speculate that the lack of interactions between the two hemispheres would deprive the developing cortical substrates of possible interhemispheric influences exerted, during ontogenesis, through the commissural fibres. As an adaptive response to CCA, each hemisphere might develop patterns of neural organisation that do not rely on interhemisperic communication for the functional outcome.

Therefore, our observations provide the first direct support that the compensatory mechanism for full realization of linguistic processing in compromised interhemispheric interaction is not a hemispheric specialization but a bilateral development and representation of language functions.

Figure 1

T1 images demonstrating ACC. T2 images reveal enlarged occipital horns of the lateral ventricles. Transversal slice indicated with * crossing the anterior commissure, transversal slice indicated with ** is located within a plane where normally the corpus callosum would reside. b. DTI did not show any increased numbers of fibres crossing the anterior commissure or other interhemispheric connections above pyramidal tract decussation. The transversal slice is crossing the anterior commissure. Red colour=fibre tracts running left – right; green colour fibre tracts running up – down; blue colour=fibre tracts running back – front. c. fMRI activity during speech production (word chains) superimposed on the individual MPRAGE. d. fMRI activity during speech perception (narrative story) superimposed on the individual MPRAGE. R=right hemisphere; z=distance to the intercommissural plane. Technical Data: 3.0 T Siemens Allegra head scanner, Functional EPIs: 36 parallel axial slices, thickness=3mm, gap=0.75mm, 64×64 matrix, field of view =192×192mm², TE=35 ms, TR=3s, flip angle=90 deg; T1 images: 208 sagittal slices, thickness=1.0mm, 256×256 matrix, field of view 256×256mm², TE=4.38 ms, TR=2.2s; T2 images: 24 parallel axial slices, thickness=3.0mm, 512×512 matrix, field of view 256×256mm², TE=97 ms, TR=5.5s. For further information concerning technical parameters of the DTI protocol see (Alexander & Barker, 2005). The height threshold of the present study at voxel level was set at p<0.001 (T >3.09) with an extension threshold of k=47 voxels (SPM2, n=1). The auditory stimuli (narrative story) were presented via specially converted high-fidelity stereo headphones and the speech production was recorded on a computer in digitized form using a microphone insensitive to the magnetic environment and positioned close to the mouth.