• Users Online: 251
  • Print this page
  • Email this page

Table of Contents
Year : 2020  |  Volume : 3  |  Issue : 3  |  Page : 126-134

Maximal safe resection of diffuse low-grade gliomas within/near motor areas using awake craniotomy with intraoperative cortical/subcortical mapping via direct electrical stimulation: A narrative review

Department of Neurosurgery, General Hospital of Southern Theatre Command, Guangzhou, Guangdong Province, China

Date of Submission12-May-2020
Date of Decision26-May-2020
Date of Acceptance27-Jul-2020
Date of Web Publication17-Oct-2020

Correspondence Address:
Dr. Hongmin Bai
Department of Neurosurgery, General Hospital of Southern Theatre Command, 111 Liuhua Road, Guangzhou 510010
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/glioma.glioma_14_20

Rights and Permissions

Diffuse low-grade gliomas are a diverse category of neuroepithelial neoplasms, which are characterized by a low proliferation index and an indolent course with a long-term survival in comparison with high-grade gliomas. It is convinced that maximal safe resection can significantly increase survival. Multiple intraoperative techniques help neurosurgeons to maximize the resection with a safe range; however, the tumors involving motor areas are still intractable for many surgeons who believe that these tumors are unresectable. We searched on PubMed database and summarized studies and reviews about diffuse low-grade gliomas within/near motor areas. Moreover, studies about anatomy about motor area were also reviewed. In this article, we discussed the anatomy of the central lobe and supplementary motor area, including the cortex, subcortical fibers, and relevant vessels, as well as the technical details of awake craniotomy and direct electrical stimulation. At last, combined with some cases, we try to demonstrate that tumors within/near motor areas are resectable, which may cause only mild neurological deficits using awake craniotomy with intraoperative monitoring by cortical/subcortical mapping, and, furthermore, it provides a longer and better survival for those young patients.

Keywords: Awake craniotomy, diffuse low-grade glioma, direct electrical stimulation, maximal safe resection, motor area

How to cite this article:
Yang R, Bai H. Maximal safe resection of diffuse low-grade gliomas within/near motor areas using awake craniotomy with intraoperative cortical/subcortical mapping via direct electrical stimulation: A narrative review. Glioma 2020;3:126-34

How to cite this URL:
Yang R, Bai H. Maximal safe resection of diffuse low-grade gliomas within/near motor areas using awake craniotomy with intraoperative cortical/subcortical mapping via direct electrical stimulation: A narrative review. Glioma [serial online] 2020 [cited 2022 Nov 28];3:126-34. Available from: http://www.jglioma.com/text.asp?2020/3/3/126/298389

  Introduction Top

A variety of techniques can be used intraoperatively to optimize the extent of resection of diffuse low-grade gliomas (DLGGs), including awake craniotomy (AC) combined with cortical/subcortical brain mapping via direct electrical stimulation (DES), intraoperative electrophysiological monitoring, functional neuro-navigation, and intraoperative magnetic resonance imaging (MRI).[1] However, tumors in eloquent regions of the cortex, such as the central lobe and supplementary motor area (SMA), are considered intractable because of the functional significance of these regions. In this article, we have reviewed DLGGs within/near the motor area concerning anatomy, the extent of resection, and the technical nuance of AC.

  Database Search Strategy Top

We queried PubMed to identify relevant publications from inception until April 1, 2020. The search terms used were as follows: (low-grade gliomas OR diffuse low-grade gliomas OR WHO grade II gliomas) AND (awake craniotomy OR awake brain surgery OR awake neurosurgery) AND (motor area OR central lobe OR eloquent area OR rolandic OR supplementary motor area OR perirolandic) AND (direct electrical stimulation OR intraoperative cortical mapping OR subcortical mapping OR intraoperative mapping OR cortical stimulation OR subcortical stimulation) NOT (conference abstract OR letter OR note OR editorial) AND (English). The reference lists of previous reviews were also screened to include additional potentially relevant studies. Moreover, literatures which discussed anatomy were searched separately using the terms of motor area OR central lobe OR eloquent area OR rolandic OR supplementary motor area OR perirolandic AND anatomy OR microsurgery anatomy. All references were assessed for eligibility by abstract screening as well as full-text reading, and non-relevant studies were excluded from the study.

  Anatomy of the Motor Area Top

Motricity of the limbs is a complex process that involves several functional cortexes and subcortical fibers. The primary motor cortex and SMA are located in the posterior portion of the frontal lobe.[2]

Cortex anatomy

The primary motor cortex, also regarded as the precentral gyrus, is limited by the precentral sulcus anteriorly and central sulcus posteriorly on the lateral surface. It folds over the superior border of the hemisphere and together with the postcentral gyrus forms the paracentral lobule, which is limited by the paracentral sulcus anteriorly, the ascending ramus of the cingulate sulcus posteriorly, and the cingulate sulcus underneath.[3] The ascending ramus is a constant sulcus that is easily visible on the sagittal plane of MRI. Thus, it is a useful landmark for determining the position of the paracentral lobule, as well as the primary motor area [Figure 1].
Figure 1: The gyrus, sulci, and subcortical fibers of the motor area. (A) Lateral view. The (CS, yellow dotted line) commonly opens directly into the interhemispheric fissure, but it is separated from the sylvian fissure by the subcentral gyrus. The CS has a gently convex posterior upper curve and a gently convex anterior lower curve. (B) Superior view. The “hand knob” on the precentral gyrus is visible in both hemispheres. (C) Lateral medial view. The paracentral lobule is limited posteriorly by the ascending ramus of the cingulate sulcus and anteriorly by the paracentral ramus of the cingulate sulcus. (D) Coronal plane of MRI with diffusion tensor imaging reconstruction. PT: Pyramidal tract, FAT: Frontal aslant tract, FST: Frontostriatal tract, CC: Corpus callosum, CS: Central sulcus, MRI: Magnetic resonance imaging. Figure 1 is sourced from the authors' unpublished clinical work

Click here to view

The central sulcus is another constant sulcus on the lateral surface of the hemisphere. Its upper end opens directly into the interhemispheric fissure in most hemispheres, and its lower end is separated from the sylvian fissure by the subcentral gyrus between the pre- and post-central gyri.[4] The precentral gyrus has a parallel trajectory with the central sulcus, which forms an angle of approximately 20° with the coronal plane passing through its upper end.[3] There are two genua in the precentral gyrus. Its upper half is gently convex posteriorly, and its lower half is gently convex anteriorly.[5] The upper genu corresponds to the motor area of the hand, thus being named the hand knob. The somatotopic organization of the primary motor cortex is well known, featuring areas related to the lower limb, trunk, upper limbs, face, and tongue.[6] The postcentral gyrus is narrower than the precentral gyrus, and it follows the curvatures of the central sulcus. It is a useful characteristic for differentiating the gyri in the surgical field, as the pre- and post-central gyri and the central sulcus are three parallel lines with the sulcus directly opening to the interhemispheric fissure and the thinner gyrus posterior of the sulcus [Figure 1].

The SMA is positioned in the posterior portion of the superior frontal gyrus, and it is limited by the precentral sulcus posteriorly, the superior frontal sulcus inferolaterally, and the cingulate sulcus inferomedially.[7] The SMA is composed of two parts, namely the pre-SMA and SMA-proper. These two regions are distinguished by different functions and cortical–subcortical connections.[8] The SMA-proper participates in the activation, control, and generation of movement, whereas pre-SMA activation is more tightly coupled to cognitive nonmotor tasks.[9] The SMA-proper is organized somatotopically with areas related to the inferior and superior limbs and face. In addition, a contribution to language function has been demonstrated in the dominant hemisphere.[10]

Subcortical fibers

The corticospinal tract (CST, also called the pyramidal tract), frontal aslant tract (FAT), frontostriatal tract (FST), and superior longitudinal fasciculus (SLF) I are essential tracts that participate in motor control networks [Figure 1].[2],[10] Based on a postmortem tractography study, the SLF I, CST, FST, and FAT are positioned in order from medial to lateral.[10] The CST arises in the primary motor cortex and ends at motor neurons in the ventral horn of the spinal cord, and it dominates spontaneous movements. However, approximately 10% of the fibers of the CST arise in the SMA-proper and terminate in the spinal cord.[11] SLF I connects the superior parietal lobe to the SMA and anterior cingulate cortex along the medial side of the hemisphere, and this pathway is considered relevant to the higher-order control of body-centered action and the initiation of motor activity.[12],[13] The FAT connects the superior frontal gyrus with the inferior frontal gyrus (Broca's area), and this pathway participates in verbal fluency.[14] The FST has been described as a connection between the pre-SMA and striatum. It was suggested in an electrical stimulation study that this tract is particularly involved in the control of lower and upper limb movements.[2]


The SMA is supplied by the anterior cerebral artery, and the central lobe is supplied by both the middle and anterior cerebral arteries.[15] The pericallosal artery, arising from the anterior cerebral artery and running adjacent to the corpus callosum, gives rise to several cortical branches, including posterior internal frontal, paracentral, and superior parietal lobules, which supply the medial surface and upper part of the lateral surface of the cerebrum bordering the interhemispheric fissure.[5],[10] Coagulation of these branches may lead to motor weakness of the contralateral foot and leg, sensory loss, and urinary incontinence in the acute phase after bilateral occlusion.[3] The branches of the middle cerebral artery, including the precentral, central, and postcentral arteries from anterior to posterior, supply the lateral surface of the central lobe, and the central artery has the greatest contribution among these arteries.[15] When processing lesions near the sylvian fissure, care should be taken to avoid coagulating these branches, which may cause permanent severe neuro-functional impairment.

Drainage of the motor cortex is usually directed to at least one of the three sinuses, namely the superior sagittal, transverse, and sphenoparietal sinuses. The SMA, paracentral lobule, and upper two-thirds of the lateral surface of the central lobe frequently drain to the superior sagittal sinus through precentral, central, and paracentral veins. The lower third of the lateral surface most commonly drains to the superficial sylvian veins through the frontosylvian veins and from there to the transverse sinus via the vein of Labbé or anteriorly to the sphenoparietal sinus.[3],[5],[16]

  Awake Craniotomy and Intraoperative Stimulation Mapping Top

AC was first described by Victor Horsley more than 120 years ago and later popularized by Wilder Penfield, and the procedure was subsequently introduced into modern usage by several researchers.[17],[18] Based on the development of anesthesia, intraoperative seizure management, surgical techniques, and intraoperative testing methods and a better understanding of the neuro-functional anatomy, the AC technique has evolved over the last century.[19] With improvements in neuro-oncology, emerging evidence has suggested that a greater extent of resection positively affects overall survival, progression-free survival, and malignant transformation (low-grade gliomas) in adult patients with hemispheric gliomas.[20],[21],[22],[23],[24] Neurosurgeons noticed that AC can significantly increase the extent of glioma resection while simultaneously minimizing the risk of postoperative complications, especially neurological morbidity.[19],[25],[26],[27],[28] Because it preserves the quality of life of patients (and decreasing the risk of postoperative morbidity) with tumors in eloquent areas while increasing the extent of resection (and maximizing postoperative survival), AC has been increasingly used in neuro-oncology in the past two decades, especially in patients with low-grade gliomas, who have a long survival expectancy.[29]

Over the past two decades, studies of patients who underwent AC suggested failure rates of 2.3%–6.4%, and the reasons for failure included poor patient selection, inadequate anesthesia, and intraoperative stimulation-induced seizures.[19] The AC procedure varies by surgeon.[30],[31],[32] However, identical principles are needed to standardize the management of patients undergoing AC, which could help minimize failure rates. Based on our experience and the literature, we have identified four essential components of the AC procedure namely patient selection, preoperative evaluation, anesthesia management, and functional mapping.

Patient selection

Proper patient selection is critical for maximizing perioperative safety.[19],[33] Patients suitable for AC have intrinsic brain tumors located within or adjacent to eloquent areas on preoperative imaging. Patients with tumors presumed to be located within functional cortical or subcortical sites may benefit from intraoperative mapping to maximize the extent of tumor resection.[34],[35] The contraindications of AC include (1) age <14 years (relative contraindication) or incomplete development of cognition or self-control ability, (2) psychiatric history or emotional instability that was not corrected by preoperative antidepressant medication treatment, (3) uncontrolled coughing, (4) severe dysphasia (i.e., >25% naming errors despite a trial of preoperative corticosteroids and mannitol), (5) hemiplegia with less than antigravity motor function, and (6) other systemic diseases that preclude surgery.

In addition to these contraindications, some risk factors should be carefully considered and managed before or during surgery, including large tumors with mass effects exceeding 2 cm, obesity, a psychiatric history or severe anxiety, intraoperative seizures, chronic smoking, chronic coughing, reoperation and extensive dural scarring, and severely impaired preoperative function.[36]

Preoperative evaluation

The preoperative evaluation includes neuro-imaging (functional and anatomical), language and sensorimotor examination, and patient education. General MRI sequences include pre- and post-contrast T1 and T2-weighted fluid-attenuated inversion recovery, and diffusion tensor imaging for white-matter pathways. Blood oxygen level-dependent functional MRI is used for eloquent area positioning combined with language or sensorimotor tasks, which is an optional choice that can be replaced by magnetic source imaging with magnetoencephalography. Perfusion-weighted imaging and magnetic resonance spectroscopy are also beneficial for estimating the blood supply and grade of the tumor. Baseline language and sensorimotor examinations are performed 24–48 h prior to surgery, including naming (64-object panel), reading, spelling, calculations, visuospatial testing, and comprehension testing depending on the tumor location.[19],[37] Only pictures and words are used intraoperatively because such testing can be done individually and correct answers can be reliably verified on the basis of the preoperative evaluation. Preoperative neuro-psychological evaluation is selectively performed as judged necessary. Patient education to provide information on the surgical procedure, significance of cooperation, intraoperative tasks, and possible discomfort during the surgery is vital for successful AC. Furthermore, caring communication can also relieve patients' concerns.

Anesthesia protocol

Monitored anesthesia care and asleep-awake-asleep methods are two commonly used anesthetic strategies for AC. Monitored anesthesia care uses conscious sedation to manage patients' pain and agitation while maintaining their ability to follow commands and protect their own airways without invasive airway instrumentation.[38] The asleep-awake-asleep technique utilizes general anesthesia with a secured airway using an endotracheal tube or laryngeal mask airway before and after intraoperative cortical/subcortical mapping.[39] In addition to these two general anesthesia methods, complete scalp block of the supraorbital, supratrochlear, auriculotemporal, zygomaticotemporal, greater occipital, lesser occipital, and greater auricular nerves can be performed by the neurosurgeon or anesthesiologist using 0.33% ropivacaine with 1:200,000 adrenaline and 0.33% lidocaine, as well as local anesthesia at the site of pin insertion and scalp incision. This provides rapid-onset, long-lasting local anesthesia with reduced bleeding. The dura can be covered with 2% lidocaine-soaked cotton for 5 min or blocked between the two layers of dura with 1% lidocaine using a 1-mL injector around the middle meningeal artery before opening the dura. It is critical that clear communication is established between the surgeon and anesthesiologist to ensure ideal intraoperative mapping conditions. The patient should be positioned laterally or semi-laterally with his or her head positioned optimally for the surgical procedure while allowing access for potential laryngeal mask airway placement (for the asleep-awake-asleep method), if needed.[19]

Current techniques for awake craniotomy

Based on our experience and the literature, we have summarized the current intraoperative techniques and emergency treatment.

Craniotomy procedure

After the patient is well positioned, the central sulcus and sylvian fissures are marked on the scalp using Rhoton's method or neuro-navigation.[5] The focus exposure encompasses the lesion plus 2–4 cm depending on the location of the adjacent eloquent areas to be mapped.[19] Before the scalp is incised, an initial dose of mannitol (1–2 g/kg) may be administered to reduce cerebral edema (particularly for patients with >2 cm mass effects, high-grade tumors, or high body mass indices), and sodium valproate is administered intravenously (loading dose of 15 mg/kg and maintenance dose of 1 mg/kg/h) to prevent stimulation-induced seizures. During bone flap removal, all medications are discontinued, and the patient is awoken to prepare for the intraoperative tasks. The laryngeal mask airway or endotracheal tube must be removed before opening the dura in case cough or vomit is induced. Before opening the dura, the brain is assessed for brain relaxation. The patient may be asked to take multiple deep breaths for controlled hyperventilation, given additional mannitol, asked to raise his or her head, and subjected to opening of the arachnoid space to release cerebrospinal fluid and decrease brain tension. If severely increased intracranial pressure persists after these measures are taken as previously mentioned, internal debulking is performed through the assumed nonfunctional cortex (based on preoperational imaging) to prevent acute cerebral hernia.

Cortical and subcortical mapping via direct electrical stimulation

Before initiating DES-based mapping, intraoperative transcortical ultrasonography is performed to delineate the lesion. Importantly, cold normal saline is made available to rapidly terminate intraoperative stimulation-induced seizures.[40] Both cortical and subcortical stimulation is delivered using a 1-mm bipolar electrode separated by 5 mm between the tips to deliver a biphasic constant current (square waves; pulse frequency of 60 Hz; pulse phase duration of 1 ms; OSIRIS NeuroStimulator, inomed Medizintechnik GmbH, Germany), beginning at 1 mA and increased in 0.5–1-mA steps to a maximum of 6 mA until a functional response is elicited.[34],[41] The entire exposed brain is stimulated, and all responsive and nonresponsive sites are stimulated three times for confirmation. When the central region is exposed, sensorimotor mapping is first performed to confirm the current intensity. The patient is then asked to perform language tasks, namely counting (regular rhythm, from one to ten, repetitively) and picture naming tasks to identify the essential cortical sites known to be inhibited by stimulation. The patient is not informed when the brain was stimulated. The stimulation lasts approximately 1–4 s. No site is stimulated twice in succession because this can increase the risk of intraoperative DES-induced seizures. Functional responses include involuntary movement, paresthesia, speech arrest, anomia, phonetic/phonemic/semantic paraphasia, slowness with initiation disturbances, and movement inhibition. Each eloquent area is marked with a sterile numbered tag on the cerebral surface.[19] The glioma is then removed via alternating resection and electrostimulation for subcortical functional mapping. Using the same stimulation parameters, the functional pathways are followed progressively from the cortical eloquent areas through the depth of the resection. The patient is asked to continuously perform the required tasks throughout the glioma resection. All resections are continued until eloquent subcortical structures are encountered within the surgical cavity or until the patient feels too tired to work efficiently. Thus, resection is performed according to individual functional boundaries with no margin left around the eloquent areas [Figure 2]. When possible, the resection is extended beyond the tumor's limits visible on preoperative MRI and intraoperative ultrasonography (the so-called supratotal resection). Subpial resection of gliomas near eloquent areas is recommended, and care should be taken when processing lesions close to vessels, including the arteries and large drainage veins because it has been reported that neurological impairment following glioma resection was more frequently caused by ischemic lesions than by cortical or subcortical structural damage.[34]
Figure 2: Maximum safe resection of gliomas in the left central lobe under awake craniotomy. The precentral gyrus and pyramidal tract comprised the anterior resection boundary, and the sensory area of the thumb comprised the lateral resection boundary. (A–C) Preoperative axial T2-weighted magnetic resonance image revealing a left central lobe diffuse low-grade glioma in a 61-year-old right-handed woman who experienced seizures. The neurologic examination revealed mild inflexible movement of the right fingers. The yellow arrow indicates the position of the hand knob. (D) Intraoperative view before resection. Tumor borders were marked with letter tags (A, anteriorly, B, posteriorly; C, laterally; D, medially). Number tags denote the zones of positive direct electrical stimulation mapping (1, thumb movement; 2, mouth movement; 3, thumb numbness; 4, little finger numbness). (E) Intraoperative view after tumor resection in a conscious patient. The glioma was removed until direct electrical stimulation mapping detected eloquent neural structures at both cortical and subcortical levels excluding the area associated with little finger numbness (tag 4). Tag 5 is the pyramidal tract for the right foot, and the large upper draining vein was persevered after tumor resection. (F–H) Postoperative axial T2-weighted magnetic resonance imaging demonstrating incomplete resection with residual tumor tissue left in the precentral gyrus to avoid a permanent deficit (yellow arrow). The patient experienced short-term hemiplegia in the right limb after surgery with muscle strength of grade 0. Her condition returned to the preoperative state 3 months after surgery with mild inflexible movement of her right fingers. Figure 2 is sourced from the authors' unpublished clinical work

Click here to view

  Effects of Cortical and Subcortical Mapping Via Direct Electrical Stimulation on the Extent of Glioma Resection Near Motor Areas Top

To minimize the risk of damage to motor areas, intraoperative functional mapping is mandatory. Awake surgery, which permits maximally safe functional-based resection according to functional boundaries, has been demonstrated to improve the extent of resection and patient survival while decreasing the risk of postoperative morbidity and maintaining patient's quality of life. A large meta-analysis of patients undergoing resection of a supratentorial glioma with or without intraoperative electrostimulation functional mapping revealed that resection using intraoperative functional mapping was associated with fewer late severe neurological deficits and more extensive resection even though the gliomas were more frequently located in eloquent areas.[34] An increasing body of evidence suggests that a greater extent of resection and a lower residual tumor volume prolong both overall and progression-free survival.[26],[42],[43] A recent meta-analysis of patients with low-grade gliomas compared the extent of resection and prognosis,[42] confirming that extensive resection is associated with better overall and progression-free survival after 2, 5, and 10 years than subtotal resection. However, this finding was based on Class III and Class IV studies, and no prospective cohort studies have been reported. Another retrospective study by Smith et al.[44] indicated that the extent of resection remained a significant predictor of overall survival and malignant progression-free survival after adjusting for age, performance status, and tumor location; however, only a trend toward prolonged progression-free survival was observed.

In addition, recent evidence suggested that supratotal resection, when possible, offers an additional survival benefit.[45] It has been demonstrated that early and maximal safe surgical resection of DLGG using awake mapping significantly improves patient survival and quality of life. For patients with noneloquent area tumors, supramarginal removal of DLGG appears to minimize the risk of malignant transformation without decreasing patient's quality of life. Thus, supratotal resection provides longer survival for patients with DLGG than extensive resection. In fact, biopsy samples revealed that conventional MRI underestimated the actual spatial extent of DLGG because tumor cells were found up to 2 cm beyond the area of signal abnormalities, even for gliomas well defined on MRI.[46] The rate of permanent neurologic impairment was significantly decreased using AC and DES;[47] moreover, postoperative quality of life was improved after large DLGG excision.[48],[49],[50] All these findings support the promise of supratotal resection for prolonging the survival and improving the quality of life of patients with DLGG.

In a recent study, 34 patients with gliomas within or near motor areas underwent AC with DES for cortical and subcortical mapping of the eloquent area. The tumors were removed on the basis of their functional boundaries in 30 of 34 patients (88.2%). Postoperative MRI illustrated that total, subtotal, and partial resection were achieved in 22 (64.7%), nine (26.5%), and three patients (8.8%), respectively. In total, 29 patients (85.3%) presented with new early postoperative neurologic deficits or experienced worsening. Three patients experienced worsening of late postoperative neurologic deficits, including one mild, moderate, and severe case each (2.9%). Among 16 patients with preoperative neurological deficits or increased intracranial pressure, 13 (81.3%) experienced improvement 3 months after surgery. Conversely, two patients experienced no change, and one patient developed severe deficits [Figure 2] and [Figure 3]. Thus, maximal safe resection of gliomas near motor areas can be achieved under AC with intraoperative cortical and subcortical mapping via DES. Under this strategy, gliomas are removed on the basis of the functional boundary with few permanent postoperative deficits. Quality of life is improved in certain patients with preoperative deficits after surgery.[51]
Figure 3: Maximum safe resection of gliomas in the right supplementary motor area under awake craniotomy. The precentral gyrus, transverse gyrus of the precentral gyrus, and pyramidal tract comprise the posterior resection boundary. (A–C) Preoperative axial T2-weighted (A), fluid-attenuated inversion recovery-weighted (B), and coronal T2-weighted (C) magnetic resonance imaging revealing a right supplementary motor area diffuse low-grade glioma in a 34-year-old right-handed man who experienced seizures. The neurologic and neuro-cognitive examination was normal. The yellow arrow indicates the position of the hand knob. (D) Intraoperative view before resection. Tumor borders were marked with letter tags (A, anteriorly, B, laterally; C, posteriorly; D, medially). Number tags denote the zones of positive direct electrical stimulation mapping (1, primary motor cortex of the left hand generating involuntary movement of the left hand during DES; 2, primary sensory cortex of the left hand generating light numbness during DES). (E) Intraoperative view after tumor resection in a conscious patient. The glioma was removed until DES mapping detected eloquent neural structures at both cortical and subcortical levels. Tag 3 is the transverse gyrus of the precentral gyrus, and tag 4 is the pyramidal tract for the left hand generating involuntary movement of the left hand during DES. (F–H) Postoperative axial T2-weighted (F), fluid-attenuated inversion recovery-weighted (G), and coronal T1-weighted (H) magnetic resonance imaging revealing total tumor resection. The yellow arrow indicates the position of the hand knob. The patient experienced short-term hemiplegia in the left limb after surgery, with a muscle strength of grade 0 caused by supplementary motor area syndrome. He resumed a normal familial, social, and professional life within 3 months after surgery. DES: Direct electrical stimulation. Figure 3 is sourced from the authors' unpublished clinical work

Click here to view

For patients with DLGGs in eloquent areas, functional-based resection is more relevant. A retrospective study performed by Magill et al. suggested that among patients with tumors only in the primary motor area, an excellent extent of resection can be achieved using DES with only a risk of transient or mild postoperative motor deficits or little functional impact.[34] This result confirms the great plasticity of the adult brain cortex and makes rolandic brain tumors no longer unresectable [Figure 4]. In fact, despite a transitory worsening in the immediate postoperative period, patients will recover thanks to the identification and preservation of critical neural pathways using DES mapping combined with postoperative functional rehabilitation.[51],[52] However, permanent and severe deficits have been observed in patients with arterial or subcortical tract impairment.[2],[10],[34]
Figure 4: Maximum safe resection of gliomas in the left precentral gyrus under awake craniotomy. (A and B) Preoperative axial T2-weighted magnetic resonance imaging revealing a left precentral gyrus diffuse low-grade glioma in a 27-year-old right-handed man who experienced seizures. The neurologic and neuro-cognitive examination was normal. (C) The surface rendering of preoperative T1-weighted magnetic resonance imaging revealing that the tumor is located exactly on the precentral gyrus, which is separated into dorsal and ventral parts by the tumor. (D) The surface rendering of functional areas overlapped the T1-weighted magnetic resonance imaging with blood oxygen level dependent functional magnetic resonance imaging. Red denotes the active sites for the hand grasp task. (E) Intraoperative view before resection. An ultrasonic tumor border was marked with a dotted yellow circle. Number tags denote the zones of positive direct electrical stimulation mapping (tags 2 and 4, finger movement; 3, mouth sensation; 5, finger sensation; 7, speech arrest during counting; 8, anomia during naming). (F) Intraoperative view after tumor resection in a conscious patient. The glioma was removed until direct electrical stimulation mapping detected eloquent neural structures at both cortical and subcortical levels. Tag 6 is the pyramidal tract for right thumb movement, and tag 7 denotes the area responsible for speech arrest during counting. (G–I) Postoperative axial (G and H) and coronal (I) T2-weighted magnetic resonance imaging demonstrating total tumor resection. The yellow arrows indicate the position of the hand knob. The patient experienced paralysis of the right hand and Broca's aphasia 3 days after surgery and resumed a normal familial, social, and professional life within 3 months after surgery. Figure 4 is sourced from the authors' unpublished clinical work

Click here to view

DLGGs in the SMA are less intractable than those in the primary motor cortex. Damage to the SMA cortex may cause SMA syndrome, which is characterized by disorders of initiation ranging from complete suppression of motor and speech production to reduced spontaneous motor and speech output.[53] Owing to cortical plasticity and compensation mechanisms via the contralateral SMA complex, most cases of SMA syndrome are reversible after surgery.[10] However, FAT or FST resection results in a negative motor response,[54] suggesting that the preservation of subcortical fibers is more important than preservation of the cortex.

  Conclusion Top

Maximal resection of DLGGs improves overall, progression-free, and malignant progression-free survival. Based on these findings, AC with DES preserves the quality of life of patients with tumors in motor areas while increasing the extent of resection. Damage to the fiber tracts underlying the motor cortex, including the CST, FST, FAT, and SLF, may result in more severe and irreversible deficits than damage to the cortex itself. In addition, injury to small perforating blood vessels was the most common cause of infarction that caused moderate or severe deficits. Therefore, understanding the anatomy of the fiber tract and vessels adjacent to the motor cortex and avoiding the aforementioned damage intraoperatively are essential for preventing permanent postoperative deficits.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. J Neurooncol 2016;130:269-82.  Back to cited text no. 1
Rech F, Herbet G, Moritz-Gasser S, Duffau H. Somatotopic organization of the white matter tracts underpinning motor control in humans: An electrical stimulation study. Brain Struct Funct 2016;221:3743-53.  Back to cited text no. 2
Frigeri T, Paglioli E, de Oliveira E, Rhoton AL Jr. Microsurgical anatomy of the central lobe. J Neurosurg 2015;122:483-98.  Back to cited text no. 3
Fernández-Miranda JC, Rhoton AL Jr., Alvarez-Linera J, Kakizawa Y, Choi C, de Oliveira EP. Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 2008;62:989-1026.  Back to cited text no. 4
Rhoton AL Jr. The cerebrum. Anatomy. Neurosurgery 2007;61:37-118.  Back to cited text no. 5
Rizzolatti G, Luppino G, Matelli M. The organization of the cortical motor system: New concepts. Electroencephalogr Clin Neurophysiol 1998;106:283-96.  Back to cited text no. 6
Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE. Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis. Neuroimage 2006;31:1453-74.  Back to cited text no. 7
Behrens TE, Jenkinson M, Robson MD, Smith SM, Johansen-Berg H. A consistent relationship between local white matter architecture and functional specialisation in medial frontal cortex. Neuroimage 2006;30:220-7.  Back to cited text no. 8
Vergani F, Lacerda L, Martino J, Attems J, Morris C, Mitchell P, et al. White matter connections of the supplementary motor area in humans. J Neurol Neurosurg Psychiatry 2014;85:1377-85.  Back to cited text no. 9
Bozkurt B, Yagmurlu K, Middlebrooks EH, Karadag A, Ovalioglu TC, Jagadeesan B, et al. Microsurgical and Tractographic Anatomy of the Supplementary Motor Area Complex in Humans. World Neurosurg 2016;95:99-107.  Back to cited text no. 10
Maier MA, Armand J, Kirkwood PA, Yang HW, Davis JN, Lemon RN. Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: An anatomical and electrophysiological study. Cereb Cortex 2002;12:281-96.  Back to cited text no. 11
Yagmurlu K, Vlasak AL, Rhoton AL Jr. Three-dimensional topographic fiber tract anatomy of the cerebrum. Neurosurgery 2015;11 Suppl 2:274-305.  Back to cited text no. 12
Yagmurlu K, Middlebrooks EH, Tanriover N, Rhoton AL Jr. Fiber tracts of the dorsal language stream in the human brain. J Neurosurg 2016;124:1396-405.  Back to cited text no. 13
Catani M, Mesulam MM, Jakobsen E, Malik F, Martersteck A, Wieneke C, et al. A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain 2013;136:2619-28.  Back to cited text no. 14
Rhoton AL Jr. The supratentorial arteries. Neurosurgery 2002;51:S53-120.  Back to cited text no. 15
Rhoton AL Jr. The cerebral veins. Neurosurgery 2002;51:S159-205.  Back to cited text no. 16
Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989;71:316-26.  Back to cited text no. 17
Surbeck W, Hildebrandt G, Duffau H. The evolution of brain surgery on awake patients. Acta Neurochir (Wien) 2015;157:77-84.  Back to cited text no. 18
Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, et al. Awake craniotomy to maximize glioma resection: Methods and technical nuances over a 27-year period. J Neurosurg 2015;123:325-39.  Back to cited text no. 19
De Benedictis A, Moritz-Gasser S, Duffau H. Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery 2010;66:1074-84.  Back to cited text no. 20
Lizarazu M, Gil-Robles S, Pomposo I, Nara S, Amoruso L, Quiñones I, et al. Spatiotemporal dynamics of postoperative functional plasticity in patients with brain tumors in language areas. Brain Lang 2020;202:104741.  Back to cited text no. 21
Yuan Y, Peizhi Z, Xiang W, Yanhui L, Ruofei L, Shu J, et al. Intraoperative seizures and seizures outcome in patients undergoing awake craniotomy. J Neurosurg Sci 2019;63:301-7.  Back to cited text no. 22
Murphy M, Dinsmore J, Wilkins PR, Marsh HT. Preuss Resident Research Award: Maximal resection of low-grade intrinsic brain tumors using “awake” craniotomy and multiple marginal smear biopsies: Neurological deficit rate and long-term survival data. Clin Neurosurg 2006;53:332-5.  Back to cited text no. 23
Keles GE, Chang EF, Lamborn KR, Tihan T, Chang CJ, Chang SM, et al. Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 2006;105:34-40.  Back to cited text no. 24
Gerritsen JK, Klimek M, Dirven CM, Hoop EO, Wagemakers M, Rutten GJ, et al. The SAFE-trial: Safe surgery for glioblastoma multiforme: Awake craniotomy versus surgery under general anesthesia. Study protocol for a multicenter prospective randomized controlled trial. Contemp Clin Trials 2020;88:105876.  Back to cited text no. 25
D'Amico RS, Englander ZK, Canoll P, Bruce JN. Extent of resection in glioma-a review of the cutting edge. World Neurosurg 2017;103:538-49.  Back to cited text no. 26
Xu DS, Awad AW, Mehalechko C, Wilson JR, Ashby LS, Coons SW, et al. An extent of resection threshold for seizure freedom in patients with low-grade gliomas. J Neurosurg 2018;128:1084-90.  Back to cited text no. 27
Attari M, Salimi S. Awake craniotomy for tumor resection. Adv Biomed Res 2013;2:63.  Back to cited text no. 28
[PUBMED]  [Full text]  
Duffau H. Is non-awake surgery for supratentorial adult low-grade glioma treatment still feasible? Neurosurg Rev 2018;41:133-9.  Back to cited text no. 29
Shen E, Calandra C, Geralemou S, Page C, Davis R, Andraous W, et al. The Stony Brook awake craniotomy protocol: A technical note. J Clin Neurosci 2019;67:221-5.  Back to cited text no. 30
Hill CS, Severgnini F, McKintosh E. How I do it: Awake craniotomy. Acta Neurochir (Wien) 2017;159:173-6.  Back to cited text no. 31
Joswig H, Bratelj D, Brunner T, Jacomet A, Hildebrandt G, Surbeck W. Awake Craniotomy:First-Year Experiences and Patient Perception. World Neurosurg 2016;90:588-9600.  Back to cited text no. 32
Gerritsen JK, Arends L, Klimek M, Dirven CM, Vincent AJ. Impact of intraoperative stimulation mapping on high-grade glioma surgery outcome: A meta-analysis. Acta Neurochir (Wien) 2019;161:99-107.  Back to cited text no. 33
Magill ST, Han SJ, Li J, Berger MS. Resection of primary motor cortex tumors: Feasibility and surgical outcomes. J Neurosurg 2018;129:961-72.  Back to cited text no. 34
Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L, et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: Functional results in a consecutive series of 103 patients. J Neurosurg 2003;98:764-78.  Back to cited text no. 35
Hervey-Jumper SL, Berger MS. Technical nuances of awake brain tumor surgery and the role of maximum safe resection. J Neurosurg Sci 2015;59:351-60.  Back to cited text no. 36
Fernández Coello A, Moritz-Gasser S, Martino J, Martinoni M, Matsuda R, Duffau H. Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks. J Neurosurg 2013;119:1380-94.  Back to cited text no. 37
Ghisi D, Fanelli A, Tosi M, Nuzzi M, Fanelli G. Monitored anesthesia care. Minerva Anestesiol 2005;71:533-8.  Back to cited text no. 38
Sokhal N, Rath GP, Chaturvedi A, Dash HH, Bithal PK, Chandra PS. Anaesthesia for awake craniotomy: A retrospective study of 54 cases. Indian J Anaesth 2015;59:300-5.  Back to cited text no. 39
[PUBMED]  [Full text]  
Boetto J, Bertram L, Moulinie G, Herbet G, Moritz-Gasser S, Duffau H. Low rate of intraoperative seizures during awake craniotomy in a prospective cohort with 374 supratentorial brain lesions: Electrocorticography is not mandatory. World Neurosurg 2015;84:1838-44.  Back to cited text no. 40
Tymowski M, Kaspera W, Metta-Pieszka J, Zarudzki Ł, Ładziński P. Neuropsychological assessment of patients undergoing surgery due to low-grade glioma involving the supplementary motor area. Clin Neurol Neurosurg 2018;175:1-8.  Back to cited text no. 41
Brown TJ, Bota DA, van Den Bent MJ, Brown PD, Maher E, Aregawi D, et al. Management of low-grade glioma: A systematic review and meta-analysis. Neurooncol Pract 2019;6:249-58.  Back to cited text no. 42
Morshed RA, Young JS, Hervey-Jumper SL, Berger MS. The management of low-grade gliomas in adults. J Neurosurg Sci 2019;63:450-7.  Back to cited text no. 43
Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 2008;26:1338-45.  Back to cited text no. 44
Ali MZ, Fadel NA, Abouldahab HA. Awake craniotomy versus general anesthesia for managing eloquent cortex low-grade gliomas. Neurosciences (Riyadh) 2009;14:263-72.  Back to cited text no. 45
Pallud J, Varlet P, Devaux B, Geha S, Badoual M, Deroulers C, et al. Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology 2010;74:1724-31.  Back to cited text no. 46
Duffau H. Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 2015;11:255-65.  Back to cited text no. 47
Moritz-Gasser S, Herbet G, Duffau H. Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: A brain electrostimulation study. Neuropsychologia 2013;51:1814-22.  Back to cited text no. 48
Charras P, Herbet G, Deverdun J, de Champfleur NM, Duffau H, Bartolomeo P, et al. Functional reorganization of the attentional networks in low-grade glioma patients: A longitudinal study. Cortex 2015;63:27-41.  Back to cited text no. 49
Lemaitre AL, Herbet G, Duffau H, Lafargue G. Preserved metacognitive ability despite unilateral or bilateral anterior prefrontal resection. Brain Cogn 2018;120:48-57.  Back to cited text no. 50
Gehring K, Sitskoorn MM, Gundy CM, Sikkes SA, Klein M, Postma TJ, et al. Cognitive rehabilitation in patients with gliomas: A randomized, controlled trial. J Clin Oncol 2009;27:3712-22.  Back to cited text no. 51
Duffau H. Resecting diffuse low-grade gliomas to the boundaries of brain functions: A new concept in surgical neuro-oncology. J Neurosurg Sci 2015;59:361-71.  Back to cited text no. 52
Vassal M, Charroud C, Deverdun J, Le Bars E, Molino F, Bonnetblanc F, et al. Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area. J Neurosurg 2017;126:1181-90.  Back to cited text no. 53
Kinoshita M, de Champfleur NM, Deverdun J, Moritz-Gasser S, Herbet G, Duffau H. Role of fronto-striatal tract and frontal aslant tract in movement and speech: An axonal mapping study. Brain Struct Funct 2015;220:3399-412.  Back to cited text no. 54


  [Figure 1], [Figure 2], [Figure 3], [Figure 4]


    Similar in PUBMED
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

  In this article
Database Search ...
Anatomy of the M...
Awake Craniotomy...
Effects of Corti...
Article Figures

 Article Access Statistics
    PDF Downloaded155    
    Comments [Add]    

Recommend this journal