Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study

Reorganization after early brain injuries is not only determined by the maturational stage of the CNS at the time of the insult (timing), but also by the structural properties, location and extent of the lesion. This study addresses the impact of different lesion extents on the type of reorganization induced in a cohort of patients with lesions of uniform structure and location (unilateral periventricular defects) and similar timing (early third trimester of pregnancy). Twelve young adult patients with congenital hemiparesis and 10 age-matched controls were studied. The severity of structural damage to hand motor projections of the cortico-spinal tract was assessed on semi-coronal MRI reconstructions along anatomical landmarks of cortico-spinal tract somatotopy. The functional integrity of these crossed cortico-spinal projections in the affected hemisphere, as well as the presence of any abnormal ipsilateral projections to the paretic hand, was examined by transcranial magnetic stimulation (TMS). Cortical activation during simple voluntary hand movements was studied by functional MRI (fMRI). Patients with small lesions (SL; n = 4) and only mild hand motor impairment possessed intact crossed cortico-spinal projections to the paretic hand, whereas no motor response could be elicited by TMS of the affected hemisphere in those with large lesions (LL; n = 6) and more severe hand motor impairment. Evidence for compensatory recruitment of the unaffected hemisphere was found in both subgroups. In the SL group, fMRI demonstrated ipsilateral activation of premotor areas, without any abnormal projections to the paretic hand originating from these sites. In the LL group, such abnormal ipsilateral projections to the paretic hand were indeed found, and fMRI confirmed cortical activation of an abnormal ipsilateral hand motor representation in the primary sensorimotor region of the unaffected hemisphere. Two patients with intermediate-sized lesions presented combined features of both groups (SL, LL). In conclusion, this study provides evidence that the type of cortico-spinal reorganization depends on the extent of the brain lesion. We propose that involvement of the ipsilateral hemisphere can be (i) of the premotor type, i.e. without ipsilateral motor projections but with significant activation of ipsilateral premotor areas, or (ii) of the primary motor type, i.e. with abnormal ipsilateral cortico-spinal projections to the paretic hand.