Predicting hand function after hemidisconnection

Abstract

Hemidisconnections (i.e. hemispherectomies or hemispherotomies) invariably lead to contralateral hemiparesis. Many patients with a pre-existing hemiparesis, however, experience no deterioration in motor functions, and some can still grasp with their paretic hand after hemidisconnection. The scope of our study was to predict this phenomenon. Hypothesizing that preserved contralateral grasping ability after hemidisconnection can only occur in patients controlling their paretic hands via ipsilateral corticospinal projections already in the preoperative situation, we analysed the asymmetries of the brainstem (by manual magnetic resonance imaging volumetry) and of the structural connectivity of the corticospinal tracts within the brainstem (by magnetic resonance imaging diffusion tractography), assuming that marked hypoplasia or Wallerian degeneration on the lesioned side in patients who can grasp with their paretic hands indicate ipsilateral control. One hundred and two patients who underwent hemidisconnections between 0.8 and 36 years of age were included. Before the operation, contralateral hand function was normal in 3/102 patients, 47/102 patients showed hemiparetic grasping ability and 52/102 patients could not grasp with their paretic hands. After hemidisconnection, 20/102 patients showed a preserved grasping ability, and 5/102 patients began to grasp with their paretic hands only after the operation. All these 25 patients suffered from pre- or perinatal brain lesions. Thirty of 102 patients lost their grasping ability. This group included all seven patients with a post-neonatally acquired or progressive brain lesion who could grasp before the operation, and also all three patients with a preoperatively normal hand function. The remaining 52/102 patients were unable to grasp pre- and postoperatively. On magnetic resonance imaging, the patients with preserved grasping showed significantly more asymmetric brainstem volumes than the patients who lost their grasping ability. Similarly, these patients showed striking asymmetries in the structural connectivity of the corticospinal tracts. In summary, normal preoperative hand function and a post-neonatally acquired or progressive lesion predict a loss of grasping ability after hemidisconnection. A postoperatively preserved grasping ability is possible in hemiparetic patients with pre- or perinatal lesions, and this is highly likely when the brainstem is asymmetric and especially when the structural connectivity of the corticospinal tracts within the brainstem is asymmetric.

Preclinical and Clinical Evidence on Ipsilateral Corticospinal Projections: Implication for Motor Recovery

“…In a large trial of children undergoing HS, Kupper et al demonstrated that grasping ability in the ipsilesional hand is only preserved in patients with prenatal or perinatal unilateral brain injury (or CP) and is associated with asymmetric structural connectivity of CST projections. This data suggests the reinforcement of developmentally preserved iCST fibers in these patients [83]. …”

Pyramidal tract and alternate motor fibers complementarily mediate motor compensation in patients after hemispherotomy

“…Early lesions to the motor system lead to the preservation of these normally transient ipsilateral connections 28 . Several electrophysiological and imaging studies have implicated this pathway as mediator of motor recovery after hemispheric lesions 15,29 . The pyramidal system is believed to be an evolutionary prerequisite for dexterous hand function including grasping 16 , which is why their role as a mediator of distal arm motor function is particularly plausible.…”

Improvements in upper extremity function in children with unilateral spastic cerebral palsy after intensive training correlates with interhemispheric connectivity

“…While the exact mechanisms in the CC for unimanual and bimanual functions remain debatable, some noteworthy reviews have described the interaction between the two hemispheres and whether the regulation of the latter is done through inhibitory or excitatory signaling [34,35]. Evidence of the involvement of the CC on unilateral and bimanual skills was unequivocally found in patients with lesions to the CC [36,37], in individuals with stroke [38], callosotomized patients [39] and in animals studies [40].…”