Case 1
First patient was with no known perinatal history but with right hand spastic paresis, incompetency with fine motor movements and with a muscle strength of 4/5 in proximal part of right upper extremity, 3/5 in hand, and very mild paresis in right lower extremity. Patient’s seizures began when 8 years old as tonic contractions in right hand. Cranial MRI revealed wide atrophy and encephalomalacia in left hemisphere (Fig. 1a). EEG findings were consistent with diffuse suppression in the left hemisphere and epileptiform activity in the occipital region. According to fMRI speech and right upper extremity motor functions of the patient were represented at the right hemisphere (Fig. 1b), whereas the right lower extremity motor functions remained in the left hemisphere (Fig. 1d).
With Phase I investigations a functional hemispheretomy was indicated for intractable seizures. However, due to the preserved motor functions in the left hemisphere, a modification of left functional hemispherotomy that spares the motor cortex and its projection fibers was planned.
IONM and neuronavigation were both applied during the surgery. Tc MEP was not optimal due to wide surgical incision and inability to place stimulation electrodes on the scalp in the appropriate positions.
IONM findings: Suboptimal tc electrical stimulation of the left hemisphere elicited muscle MEP responses only in the right lower extremity before the beginning of the surgery (Fig. 2a,b). Phase reversal on SEP responses was not detected through a strip electrode perpendicular to the sulci by stimulation of the right median nerve. However, when the right tibial nerve stimulated, phase reversal was observed on SEP responses between two consecutive contacts. Afterwards, cortical motor mapping was initiated using anodal stimulation at 10mA over the exposed cortex. The right lower extremity motor representation was found to be localized within the precentral gyrus in close proximity to the midline at 20 mA (Fig. 2d,e). The stimulation amplitude was gradually increased to a maximum of 25 mA, at which point epileptic after-discharges were observed on EEG. However, the motor representation of the right upper extremity was not found within the exposed cortical area. Cortical motor thresholds for the muscles of the right lower extremity remained stable during the surgery. The right tibial SEP disappeared while the left did not (Fig. 2c). During white matter dissection, safe distance from the CST were regularly checked with cathodal stimulation. Even with stimulation of the CST with higher amplitude did not reveal any motor response from the right upper extremity which clearly proved total shift of the right upper extremity motor functions to the contralateral hemisphere.
Immediately after the operation, the patient’s hemiparesis was increased on the right extremities compared to the pre-operative condition. An early post-operative cranial MRI was taken for routine control. Motor muscle strength was 2/5 in right proximal upper extremity and 1/5 in right hand on postoperative first day, whereas left extremities were similar to pre-operative motor strength. Up to postoperative seventh day, muscle strength was gradually increased on the right, and the patient was discharged as ambulatory without assistance. On postoperative third month, patient’s motor functions were back to basal condition. The pathology sent from the temporal lobe reported as Focal Cortical Dysplasia Type 1b. In last follow-up in 2023, patient’s muscle strength of the right upper and lower extremities was exactly same as the pre-operative condition. Patient’s fMRI (Fig. 1c and 1e) and Diffusion Tensor Tractography (DTT) (Fig. 1f) results on postoperative fifth year has showed the right hand and foot representation remained at the same locations and seizure outcome was Engel Class IA and ILAE Class I at the sixth post-operative year.
Case 2
The second patient was with no known perinatal history. Seizures started at the age of 11 as focal to bilateral tonic-clonic seizures, and the patient was diagnosed to have Methylenetetrahydrofolate reductase (MTHFR) deficiency at that time. The patient had a motor muscle strength of 4/5 in the right upper extremity. Cranial MRI showed sequalae encephalomalacia areas in the left inferior frontal gyrus, insular cortex and superior temporal gyrus extending to external and internal capsule (Fig. 3a). EEG results showed diffuse suppression in the left hemisphere and neuronal hyperexcitability in the left frontocentral region. fMRI findings revealed that right hand presentation were on both hemispheres’ cortex (Fig. 3b) and right foot representation was in the left hemisphere (Fig. 3c). Due to possible perinatal damage in left hemisphere related to the hand area and the motor deficit of right upper extremity, no final decision could be made whether the right hand presentation was shifted to the right hemisphere or is represented by both hemispheres.
After the phase I investigations, a left sided functional hemispherotomy that spares the motor, especially the related hand region, cortex and its projection fibers was decided to be performed to the patient due to the preserved motor functions on the left hemisphere (Fig. 4c).
IONM findings: In this case, we were able to perform tc stimulation. MEP responses from the muscles on the right upper extremity with tc stimulation of the left hemisphere before the beginning of the surgery were obtained which showed that there was a representation of right upper extremity in the left hemiphere. Central sulcus localization was defined between the 2nd and 3rd contacts of the strip electrode (Fig. 4a) by phase reversal technique by median SEP after opening the dura (Fig. 4d). Cortical motor mapping showed the right upper extremity responses on the exposed cortical area in the left hemisphere. (Fig. 4b and 4e). The subcortical motor stimulus threshold from the resection cavity to the CST was 5 mA and it was obtained from right upper extremity muscles as well. At the end of the surgery, tc MEP responses of the right upper extremity muscles were lost, and amplitude decreased more than 50% while staying at the same threshold on dc MEP.
The patient woke up with a mild worsened paresis in right upper extremity (4/5) and right hand (3/5) than before. On postoperative first day, a cranial MRI was taken for routine control. Up to postoperative tenth day, muscle strength was gradually increased, and the patient was discharged with physical therapy recommendation. On postoperative third month, patient’s motor functions were back to basal values. The pathological diagnosis of the parenchyma with encephalomalacia was subpial gliosis compatible with chronic ischemia. In last follow-up in 2023, patient’s only deficit was in right upper extremity with a muscle strength of 4/5, and incompetency in fine motor movements. fMRI results postoperatively on fifth year showed right hand (Fig. 3d) and foot (Fig. 3e) representation stayed the same. Follow-up time was six years with Engel Class IA and ILAE Class I outcomes.
Case 3
The third patient was a patient with epilepsy with oral automatism seizures in sleep. There was no previous history of perinatal or postnatal injury recorded. The patient had right hemiparesis more prominently in hand and foot with a muscle strength of 4/5, 3/5 in foot, spasticity in hand and foot. Cranial MRI results had showed wide polymicrogyria and cortical dysplasia in left frontal and insular lobe extending to the central sulcus (Fig. 5a,b). fMRI showed right hand and foot motor activity was traced mostly in right hemisphere’s precentral gyrus and a little on the medial face of left hemisphere’s paracentral lobule (Fig. 5c,d,e ). Interictal Positron Emission Tomography (PET)-MR results had showed bilateral hypometabolism in mesial temporal lobes which was more prominent on the left. EEG results had showed continuous epileptiform activity in both frontocentral and frontotemporal areas which was more prominent on the left also. Due to inconsistencies between PET-MR and EEG and other cranial imaging during Phase I studies, the epilepsy team decided for Phase II to determine the following treatment. The patient underwent Stereoelectroencephalography (SEEG) of the left hemisphere (Fig. 5f,g,h). During SEEG monitorization, functional mapping with deep-brain electrodes was performed and no motor or speech functions were affected. After seven days with SEEG monitorization phase II studies showed that the seizures originated from the polymicrogyric precentral gyrus on the left hemisphere and the patient underwent left lesionectomy carried out with IONM and neuronavigation.
IONM findings: MEP responses on the right extremities were not obtained from tc stimulation of the left hemisphere. However, tc stimulation of the right hemisphere via C2/C1 and C4/Cz points at the low stimulus intensity (120 and 130V) elicited bilateral MEP responses with similar latency. When stimulus threshold was increased to 300V to the left hemisphere via C1/C2, MEP responses obtained from the right extremities. However, those responses were thought to be originated from the stimulation of deep CST. Following the dural opening, cortical motor mapping was negative, meaning that no MEP responses were obtained from the exposed cortical area. The surgery went without any complication. MEP and SEP monitoring remained stable during the surgery. At the immediate post-operative period, the motor examination was the same as pre-operative findings. A routine cranial MRI was taken on the postoperative first day (Fig. 6a, b).
The pathological diagnosis was polymicrogyria. Last follow-up revealed still seizure freedom (Engel IA and ILAE I) at post-operative third year. fMRI on the post-operative third year showed right hand (Fig. 6c) and foot (Fig. 6d) representation was still in the right hemisphere as before the surgery.
Case 4
The patient was presented with staring, jerking movements or focal to bilateral tonic-clonic seizures. Medical history was uneventful except for seizures which started when 2 months old. Patient had also no previous history of perinatal injury that was recorded, however had spastic right hemiparesis with a muscle strength of 4/5, more prominent in distal extremities. Cranial MRI was consistent with encephalomalacia as a sequelae of stroke in the left medial cerebral artery watershed area (Fig. 7a). fMRI showed that motor representation of right extremities was found on the right hemisphere (Fig. 7c and 7e). EEG revealed epileptiform activity related to the left hemisphere motor network and burn-out phenomena on the right hemisphere. After Phase I epilepsy studies, the patient underwent left periinsular functional hemispherotomy with the aid of IONM and neuronavigation.
IONM findings: MEP responses from the left upper extremity were obtained at 80V by tc stimulation of the right hemisphere, whereas responses from the right upper extremity (ipsilateral response) and bilateral lower extremities appeared at 100V and 150V, respectively. MEP responses of the right extremities were not obtained by tc electrical stimulation of the left hemisphere within normal limits of the stimulation. However, bilateral upper and lower extremity responses by stimulation of the left hemisphere were elicited at 250V which is higher than normal limits, can be explained by subcortical deep white matter stimulation of the right hemisphere. SEP responses of the left extremities were recorded on the right hemisphere whereas SEP responses of the right extremities were not elicited.
Following the dural opening, cortical motor mapping was negative on the exposed cortex of the left hemisphere. Resection was accompanied by intermittent subcortical stimulation. The subcortical deep white matter stimulation interestingly showed responses from the left extremities at 18 mA (Fig. 8a), while stimulation with 20 mA at the same location revealed bilateral motor responses from all extremities (Fig. 8b). This finding let us to conclude that, as a result of neuroplastical process the fibers of the shifted motor function were located lateral to the native corticospinal fibers on the right hemisphere. Tc MEP and SEP recordings were similar to the baseline recordings at the end of the surgery.
After the surgery, motor examination was the same as before the surgery. On the post-operative third day, a routine cranial MRI was taken (Fig. 7b). The pathological diagnosis was cortical lacunae formation in subpial areas and surrounding gliosis. fMRI on post-operative first year showed that right hand (Fig. 7d) and foot (Fig. 7f) presentation is on right hemisphere. Last follow-up was at the first year after the surgery with an Engel IA and ILAE I seizure outcome.