Surgical removal of lesions located around the rolandic cortex remains a challenge for neurosurgeons because of the high risk of neurological deficit [18]. Techniques, such as awake anesthesia, could help preserve the brain's functions during surgery but not enough. In our case series, 41 patients received surgical removal of the epileptogenic cortex involving the rolandic and peri-rolandic cortex and 39 patients without a persistent motor deficit in long-term follow-up. This result is achieved based on a good understanding of the cortex's cytoarchitectonic basis and detailed peri-surgical evaluation techniques. We introduced our experiences dealing with cases around the rolandic cortex and hope our experience could help motor function protection in clinical practice.
The precentral gyrus as a whole is not all indispensable for motor function. Traditionally, the precentral gyrus was thought to be responsible for movement, and the postcentral gyrus was responsible for sensory information processing[23–25]. However, this is not always the case in the real setting. According to the cytoarchitectonic organization of the brain, Brodmann divided the brain into different sub-areas. Based on Brodmann’s observation, BA4, characterized by giant pyramid neurons, is responsible for voluntary movement. BA6, situated anterior to the primary motor cortex, is responsible for planning complex movements[26]. Penfield performed direct cortical stimulation to confirm functional representation regions with awake craniotomy and found motor response areas mainly situated around the central sulcus, but not purely in the precentral gyrus[23], which is similar to Brodmann's findings. However, the boundary between BA4 and BA6 is not always consistent with anatomical landmarks. Ziles further studied the morphology and cytoarchitecture of the central sulcus with 32 human brains and found BA4 mainly located in the anterior bank of central sulcus [27]. That is, the anterior bank of the central sulcus might be the indispensable cortex for motor function. So, surgical removal of the precentral gyrus's anterior part might not lead to a persistent motor deficit.
The lower part of the precentral gyrus is also safe to remove, even located in the central sulcus's anterior bank. According to Penfield's early observations, stimulation in the face representation area of the precentral gyrus could induce a bilateral facial motor response, but no ipsilateral motor response was observed with stimulation in the representation area of limb[23, 28]. So, motor responses are not always controlled by the unilateral hemisphere. This could explain why surgical removal of the lower part of the precentral gyrus will not cause permanent disability. In addition to identifying the motor representation cortex with DCS, it is also crucial to bear in mind that we need to find the boundary between the hand representation area and face representation area because the motor cortex below this boundary is relatively safe to remove.
An epileptogenic lesion which is located within the central sulcus is not always a contra indicator for surgery. The epileptic lesion might destroy the brain's function locally or at a considerable distance away[7]. This is most probably because of the interictal discharges and seizure spreading effects[29, 30]. So the epileptogenic lesion, especially those benign lesions that occurred early during the lifespan, may not harbor any function, even if they are located in the center of the eloquent cortex. Much attention should be paid to the perioperative evaluation stage to delineate the boundary of the lesion and the eloquent cortex to achieve a better prognosis, which is the case with our case series.
Whether invasive exploration, such as subdural electrodes or SEEG, helps protect the brain's function for epilepsy surgeries involving the rolandic cortex is doubtful. In our early cases, subdural electrodes were applied to identify the potential epileptogenic zone and help us identify the eloquent cortex to avoid motor deficits. Surgical removal of the posterior part of the superior and middle frontal gyrus, together with the upper part of the precentral gyrus (the anterior bank of central sulcus was involved), was performed (supplemental figure ). Successful control of epilepsy was achieved after surgery. However, two patients (patient 6 & patient 24) experienced a persistent left hand movement deficit. This might be because the commercially available subdural strips/grid is not precise enough for functional mapping in the eloquent cortex. Currently, each contact's diameter is 2.5mm, and the distance between two adjacent subdural strips/grid contacts is 10mm, which is inexactitude for delineating the boundary of the eloquent cortex. We need a more precise method to delineate the epileptogenic zone boundary and eloquent zone, which is the core problem in epilepsy surgeries. High-density ECoG grid/strip might help this scenario, but lots more work needs to be done.
Intraoperative neuro-electrophysiological monitoring is crucial in identifying the boundaries of the eloquent cortex and preserving the intact functions of the brain[31]. From our perspective, SSEP and MEP monitoring is a must, while awake surgery with DCS is recommended but not essential for motor function protection. For seizure arising from the rolandic cortex, it is good to identify the motor representation cortex as described before. However, it is quite common to induce a seizure for DCS, especially in the motor cortex[32, 33]. We need to be quite careful with DCS in the motor cortex. SSEP helps identify the central sulcus location, and continuous MEP monitoring is essential in helping protect motor functions. In our case series, all of them have SSEP and MEP monitoring. Twelve surgeries were performed under awake anesthesia, and none of them experienced long-term motor deficits.
Neuro-navigation is also recommended in epilepsy surgery involving rolandic cortex surgery but not enough. Brain shift due to loss of CSF is a big problem for neuro-navigations[34]. We can not rely on neuro-navigations to identify surgical boundaries if we could not correct brain shift related problems. 'Surface navigation' based on relative anatomical structures, such as vessels, bones, and gyrus, could supplement the current navigation system[35].
En bloc resection of the lesion is recommended. This is because the seizure is believed orientated from grey matter and corticectomy is enough for seizure control. Destructions of extra white matter in the rolandic region may lead to a persistent motor deficit. We need to find the boundary between the grey matter and the white matter to remove the epileptic grey matter purely. Thus, we could start from the relatively safe areas where the interface between grey matter and white matter is straightforward. The resected grey matter thickness could serve as the reference for the remaining cortex to be removed. We could also follow the boundary from relative safe areas to highly eloquent areas.
Limitations
In this study, we only included epilepsy surgeries with benign lesions. Seizures due to malignant lesions, such as GBM, were not included. This is because, for benign lesions, we could only remove regions that are responsible for seizure generation. Thus, functional preservation is of vital importance with minimum resection. However, for malignant lesions, such as GBM, we need to balance between tumor recurrent and function preservation. Sometimes aggressive resection is needed, and we have to sacrifice some functions of the brain. So, our result might not be suitable for malignant tumor-induced epilepsies in the rolandic area. Secondly, a relatively short follow-up time is also a disadvantage of our study. We will still work on this topic and provide more cases with a longer follow-up time later.