The neuronal reserve in glioma surgery: functional reorganization of the motor network examined by navigated transcranial magnetic stimulation and diffusion tensor imaging tractography

J Neurosurg 143:793–804, 2025

This study demonstrates that glioma-induced reorganization of the motor cortex, measured by navigated transcranial magnetic stimulation and diffusion tensor imaging, is linked to functional recovery. Individual neuronal reserve—reflected in motor area resizing, excitability, and tract integrity—may explain differences in disease progression and surgical outcomes.

• Glioma surgery outcomes vary due to individual differences in motor network compensation and adaptation.

• This study used navigated transcranial magnetic stimulation (nTMS) and diffusion tensor imaging (DTI) tractography to measure motor cortex reorganization in glioma patients.

• Motor area relocation, resizing, and changes in excitability were observed in both affected and unaffected hemispheres, indicating bilateral reorganization.

• Greater preoperative motor area size and excitability were associated with better postoperative motor function and recovery.

• Reduced integrity of the corticospinal tract correlated with motor impairment and limited reorganization capacity.

• Functional recovery was linked to increased motor area size, excitability, and area relocation, supporting the concept of an individual neuronal reserve.

• Reorganization patterns were independent of tumor grade, highlighting the importance of personalized risk stratification and treatment planning.

• The study recommends using nTMS data for tailored preoperative risk assessment and patient counseling in glioma surgery.

A novel robot-assisted method for implanting intracortical sensorimotor devices for brain-computer interface studies

J Neurosurg 142:1280–1288, 2025

A novel robot-assisted method for implanting intracortical microelectrode arrays in brain-computer interface studies was successfully demonstrated in a tetraplegic participant. The technique ensured precise placement, facilitating high-quality signal communication for motor control and sensory feedback, with promising implications for restoring upper-limb function.

• A novel robot-assisted method for implanting intracortical microelectrode arrays in brain-computer interface (BCI) studies is presented, focusing on surgical techniques and challenges.

• The technique was applied in a 31-year-old male with tetraplegia, enabling 2D control of a virtual arm with high success rates and maintaining recording quality over time.

• The robotic neurosurgery technique provides high accuracy and time efficiency, reducing human error and surgeon burden in repetitive procedures.

Preoperative imaging and robotic systems were used for precise planning and execution of array implantations, ensuring minimal cortical damage and high signal quality.

• The study demonstrated that robotic neurosurgery could be successfully translated into BCI device implantation, aiming to restore upper-limb function.

• Future challenges include refining insertion methods, increasing automation, and addressing intraoperative adjustments for microvessels.

• The study was conducted under an investigational device exemption from the US Food and Drug Administration and received institutional review board approval.

Classification of Individual Finger Movements Using Intracortical Recordings in Human Motor Cortex

Neurosurgery, Volume 87, Issue 4, 1 October 2020, Pages 630–638

Intracortical microelectrode arrays have enabled people with tetraplegia to use a brain–computer interface for reaching and grasping. In order to restore dexterous movements, it will be necessary to control individual fingers.

OBJECTIVE: To predict which finger a participant with hand paralysis was attempting to move using intracortical data recorded from the motor cortex.

METHODS: A 31-yr-old man with a C5/6 ASIA B spinal cord injury was implanted with 2 88- channel microelectrode arrays in left motor cortex. Across 3 d, the participant observed a virtual hand flex in each finger while neural firing rates were recorded. A 6-class linear discriminant analysis (LDA) classifier, with 10 × 10-fold cross-validation, was used to predict which fingermovement was being performed (flexion/extension of all 5 digits and adduction/abduction of the thumb).

RESULTS: Themean overall classification accuracywas 67% (range: 65%-76%, chance: 17%), whichoccurredat anaverageof 560ms (range:420-780ms) aftermovementonset. Individually, thumb flexion and thumb adduction were classified with the highest accuracies at 92% and 93%, respectively. The index, middle, ring, and little achieved an accuracy of 65%, 59%, 43%, and 56%, respectively, and, when incorrectly classified, were typically marked as an adjacent finger. The classification accuracies were reflected in a low-dimensional projection of the neural data into LDA space, where the thumb-related movements were most separable from the finger movements.

CONCLUSION: Classification of intention to move individual fingers was accurately predicted by intracortical recordings from a human participant with the thumb being particularly independent.

Predictors of postoperative motor function in rolandic meningiomas

J Neurosurg 130:1283–1288, 2019

Resection of supratentorial meningiomas is generally considered a low-risk procedure, but tumors involving the rolandic cortex present a unique challenge. The rate of motor function deterioration associated with resecting such tumors is not well described in the literature. Thus, the authors sought to report the rates and predictors of postoperative motor deficit following the resection of rolandic meningiomas to assist with patient counseling and surgical decision-making.

METHODS An institution’s pathology database was screened for meningiomas removed between 2000 and 2017, and patients with neuroradiological evidence of rolandic involvement were identified. Parameters screened as potential predictors included patient age, sex, preoperative motor severity, tumor location, tumor origin (falx vs convexity), histological grade, FLAIR signal (T2-weighted MRI), venous involvement (T1-weighted MRI with contrast), intratumoral hemorrhage, embolization, and degree of resection (Simpson grade). Variables of interest included preoperative weakness and postoperative motor decline (novel or worsened permanent deficit). The SPSS univariate and bivariate analysis functions were used, and statistical significance was determined with alpha < 0.05.

RESULTS In 89 patients who had undergone resection of convexity (80.9%) or parasagittal (19.1%) rolandic meningiomas, a postoperative motor decline occurred in 24.7%. Of 53 patients (59.6%) with preoperative motor deficits, 60.3% improved, 13.2% were unchanged, and 26.4% worsened following surgery. Among the 36 patients without preoperative deficits, 22.2% developed new weakness. Predictors of preoperative motor deficit included tumor size (41.6 vs 33.2 cm3, p = 0.040) and presence of FLAIR signal (69.8% vs 50.0%, p = 0.046). Predictors of postoperative motor decline were preoperative motor deficit (47.2% vs 22.2%, p = 0.017), minor (compared with severe) preoperative weakness (25.6% vs 21.4%, p < 0.001), and preoperative embolization (54.5% vs 20.5%, p = 0.014). Factors that trended toward significance included parafalcine tumor origin (41.2% vs 20.8% convexity, p = 0.08), significant venous involvement (44.4% vs 23.5% none, p = 0.09), and Simpson grade II+ (34.2% vs 17.6% grade I, p = 0.07).

CONCLUSIONS Resection of rolandic area meningiomas carries a high rate of postoperative morbidity and deserves special preoperative planning. Large tumor size, peritumoral edema, preoperative embolization, parafalcine origin, and venous involvement may further increase the risk. Alternative surgical strategies, such as aggressive internal debulking, may prevent motor decline in a subset of high-risk patients.

 

Resection of primary motor cortex tumors

J Neurosurg 129:961–972, 2018

Brain tumors involving the primary motor cortex are often deemed unresectable due to the potential neurological consequences that result from injury to this region. Nevertheless, we have challenged this dogma for many years and used asleep, as well as awake, intraoperative stimulation mapping to maximize extent of resection. It remains unclear whether these tumors can be resected with acceptable morbidity, whether performing the surgery with the patient awake or asleep impacts extent of resection, and how stimulation mapping influences outcomes.

METHODS A retrospective chart review was performed on the senior author’s cohort to identify patients treated between 1998 and 2016 who underwent resection of tumors that were located within the primary motor cortex. Clinical notes, operative reports, and radiographic images were reviewed to identify intraoperative stimulation mapping findings and functional outcomes following tumor resection. Extent of resection was quantified volumetrically. Characteristics of patients were analyzed to identify factors associated with postoperative motor deficits.

RESULTS Forty-nine patients underwent 53 resections of tumors located primarily within the motor cortex. Stimulation mapping was performed in all cases. Positive cortical sites for motor response were identified in 91% of cases, and subcortical sites in 74%. Awake craniotomy was performed in 65% of cases, while 35% were done under general anesthesia. The mean extent of resection was 91%. There was no statistically significant difference in extent of resection in cases done awake compared with those done under general anesthesia. New or worsened postoperative motor deficits occurred in 32 patients (60%), and 20 patients (38%) had a permanent deficit. Of the permanent deficits, 14 were mild, 4 were moderate, and 2 were severe (3.8% of cases). Decreased intraoperative motor response and diffusion restriction on postoperative MRI were associated with permanent deficit. Awake motor mapping surgery was associated with increased diffusion signal on postoperative MRI.

CONCLUSIONS Resection of tumors from the primary motor cortex is associated with an increased risk of motor deficit, but most of these deficits are transient or mild and have little functional impact. Excellent extent of resection can be achieved with intraoperative stimulation mapping, suggesting that these tumors are indeed amenable to resection and should not be labeled unresectable. Injury to small perforating or en passage blood vessels was the most common cause of infarction that led to moderate or severe deficits. Awake motor mapping was not superior to mapping done under general anesthesia with regard to long-term functional outcome.

 

The Impact of Diffusion Tensor Imaging Fiber Tracking of the Corticospinal Tract Based on Navigated Transcranial Magnetic Stimulation on Surgery of Motor-Eloquent Brain Lesions

Neurosurgery 83:768–782, 2018

Navigated transcranialmagnetic stimulation (nTMS) enables preoperative mapping of the motor cortex (M1). The combination of nTMSwith diffusion tensor imaging fiber tracking (DTI-FT) of the corticospinal tract (CST) has been described; however, its impact on surgery of motor-eloquent lesions has not been addressed.

OBJECTIVE: To analyze the impact of nTMS-basedmapping on surgery ofmotor-eloquent lesions.

METHODS: In this retrospective case-control study, we reviewed the data of patients operated for suspected motor-eloquent lesions between 2012 and 2015. The patients underwent nTMS mapping of M1 and, from 2014, nTMS-based DTI-FT of the CST. The impact on the preoperative risk/benefit analysis, surgical strategy, craniotomy size, extent of resection (EOR), and outcome were compared with a control group.

RESULTS: We included 35 patients who underwent nTMS mapping of M1 (group A), 35 patients who also underwent nTMS-based DTI-FT of the CST (group B), and a control group composed of 35 patients treated without nTMS (group C). The patients in groups A and B received smaller craniotomies (P = .01; P = .001), had less postoperative seizures (P = .02), and a better postoperativemotor performance (P=.04) and Karnofsky Performance Status (P=.009) than the controls. Group B exhibited an improved risk/benefit analysis (P=.006), an increased EOR of nTMS-negative lesions in absence of preoperative motor deficits (P = .01), and less motor and Karnofsky Performance Status worsening in case of preoperative motor deficits (P = .02, P = .03) than group A.

CONCLUSION: nTMS-based mapping enables a tailored surgical approach for motor eloquent lesions. It may improve the risk/benefit analysis, EOR and outcome, particularly when nTMS-based DTI-FT is performed.

Locating and Outlining the Cortical Motor Representation Areas of Facial Muscles With Navigated Transcranial Magnetic Stimulation

Locating and Outlining the Cortical Motor Representation Areas of Facial Muscles With Navigated Transcranial Magnetic Stimulation

Neurosurgery 77:394–405, 2015

Navigated transcranial magnetic stimulation (nTMS) has become established as an accurate noninvasive technique for mapping the functional motor cortex for the representation areas of upper and lower limb muscles but not yet for facial musculature.

OBJECTIVE: To characterize the applicability and clinical impact of using nTMS to map cortical motor areas of facial muscles in healthy volunteers and neurosurgical tumor patients.

METHODS: Eight healthy volunteers and 12 patients with tumor were studied. The motor threshold (MT) was determined for the abductor pollicis brevis and mentalis muscles. The lateral part of the motor cortex was mapped with suprathreshold stimulation intensity, and motor evoked potentials were recorded from several facial muscles. The patient protocol was modified according to the clinical indication.

RESULTS: In all healthy subjects, motor evoked potentials were elicited in the mentalis (mean latency, 13.4 milliseconds) and orbicularis oris (mean latency, 12.6 milliseconds) muscles. At 110% of MT of the mentalis, the motor evoked potentials of facial muscles were elicited mainly in the precentral gyrus but also from one gyrus anterior and posterior to it. The cortical areas applicable for mapping were limited by an artifact attributable to direct peripheral nerve stimulation. The mapping protocol was successful in 10 of 12 tumor patients at locating the representation area of the lower facial muscles. The MT of the facial muscles was significantly higher than that of the abductor pollicis brevis.

CONCLUSION: nTMS is an applicable and clinically beneficial noninvasive method to preoperatively map the cortical representation areas of the facial muscles in the lower part of the face. Instead of using the MT of the abductor pollicis brevis, the stimulus intensity during mapping should be proportioned to the MT of a facial muscle.

The preoperative use of navigated transcranial magnetic stimulation facilitates early resection of suspected low-grade gliomas in the motor cortex

The preoperative use of navigated transcranial magnetic stimulation facilitates early resection of suspected low-grade gliomas in the motor cortex

Acta Neurochir (2013) 155:1813–1821

Resection is recommended for low-grade gliomas, but often it is not performed if the tumor is suspected of invading the primary motor cortex. The study aim is to assess what influence preoperative navigated transcranial magnetic stimulation (nTMS) has on the treatment strategy and clinical outcome for suspected low-grade gliomas in presumed motor eloquent location.

Methods This paper reports on all our patients with gliomas in the primary motor cortex that were non-enhancing on MRI, since we began using nTMS (n=11). For the comparison group, we identified the 11 most recent such patients just before we started using nTMS.

Results Exact delineation of motor functional versus nonfunctional cortical tissue was provided by nTMS in all cases, also within the area of altered FLAIR signal. In 6 out of 11 cases, the nTMS mapping result changed the treatment plan towards early and more extensive resection. Only one nTMS patient had another seizure within the follow-up period, whereas four patients in the comparison group had further seizures. In the nTMS group, 1 of 4 patients with pre-op neurological deficits improved by one year; whereas the comparison group had increased neurological deficits in 3 of the 8 patients not having surgery. The median (range) change of tumor volume from baseline to 1 year was −83 % (−67 % to −100 %) in the nTMS group, but +12 % (+40 % to −56 %) in the comparison group (p<0.001).

Conclusions nTMS provides accurate motor mapping results also in infiltrative gliomas and enables more frequent and more extensive surgical resection of non-enhancing gliomas in or near the primary motor cortex. The substantial differences observed here in neurological and oncological outcomes suggest that further comparative research is warranted.

Influence of Navigated Transcranial Magnetic Stimulation on Surgical Planning for Tumors in or Near the Motor Cortex

Neurosurgery 70:1248–1257, 2012 DOI: 10.1227/NEU.0b013e318243881e 

Brain tumor surgery near the motor cortex requires careful planning to achieve the optimal balance between completeness of tumor resection and preservation of motor function. Navigated transcranial magnetic stimulation (nTMS) can be used to map functionally essential motor areas preoperatively.

OBJECTIVE: To evaluate how much influence, benefit, and impact nTMS has on the surgical planning for tumors near the motor cortex.

METHODS: This study reviewed the records of 73 patients with brain tumors in or near the motor cortex, mapped preoperatively with nTMS. The surgical team prospectively classified how much influence the nTMS results had on the surgical planning. Stepwise regression analysis was used to explore which factors predict the amount of influence, benefit, and impact nTMS has on the surgical planning.

RESULTS: The influence of nTMS on the surgical planning was as follows: it confirmed the expected anatomy in 22% of patients, added knowledge that was not used in 23%, added awareness of high-risk areas in 27%, modified the approach in 16%, changed the planned extent of resection in 8%, and changed the surgical indication in 3%.

CONCLUSION: nTMS had an objective benefit on the surgical planning in one fourth of the patients and a subjective benefit in an additional half of the patients. It had an impact on the surgery itself in just more than half of the patients. By mapping the spatial relationship between the tumor and functional motor cortex, nTMS improves surgical planning for tumors in or near the motor cortex.

Preoperative Functional Mapping for Rolandic Brain Tumor Surgery: Comparison of Navigated Transcranial Magnetic Stimulation to Direct Cortical Stimulation

Neurosurgery 69:581–589, 2011 DOI: 10.1227/NEU.0b013e3182181b89

Transcranial magnetic stimulation (TMS) is the only noninvasive method for presurgical stimulation mapping of cortical function. Recent technical advancements have significantly increased the focality and usability of the method.

OBJECTIVE: To compare the accuracy of a 3-dimensional magnetic resonance imaging– navigated TMS system (nTMS) with the gold standard of direct cortical stimulation (DCS).

METHODS: The primary motor areas of 20 patients with rolandic tumors were mapped preoperatively with nTMS at 110% of the individual resting motor threshold. Intraoperative DCS was available from 17 patients. The stimulus locations eliciting the largest electromyographic response in the target muscles (‘‘hotspots’’) were determined for both methods.

RESULTS: The nTMS and DCS hotspots were located on the same gyrus in all cases. The mean 6 SEM distance between the nTMS and DCS hotspots was 7.83 6 1.18 mm for the abductor pollicis brevis (APB) muscle (n = 15) and 7.07 6 0.88 mm for the tibialis anterior muscle (n = 8). When a low number of DCS stimulations was performed, the distance between the nTMS and DCS hotspots increased substantially (r = 20.86 for APB). After the exclusion of the cases with , 15 DCS APB responses, the mean 6 SEM distance between the hotspots was only 4.70 6 1.09 mm for APB (n = 8).

CONCLUSION: Peritumoral mapping of the motor cortex by nTMS agreed well with the gold standard of DCS. Thus, nTMS is a reliable tool for preoperative mapping of motor function.

Navigated Transcranial Magnetic Stimulation and Functional Magnetic Resonance Imaging: Advanced Adjuncts in Preoperative Planning for Central Region Tumors

Neurosurgery 68:1317–1325, 2011 DOI: 10.1227/NEU.0b013e31820b528c

Tumor resection in the vicinity of the motor cortex poses a challenge to all neurosurgeons. For preoperative assessment of eloquent cortical areas, functional magnetic resonance imaging (fMRI) is used, whereas intraoperatively, direct cortical stimulation (DCS) is performed. Navigated transcranial magnetic stimulation (nTMS) is comparable to DCS in activating cortical pyramidal neurons.

OBJECTIVE: To evaluate the reliability of nTMS compared with fMRI and DCS for preoperative resection planning of centrally located tumors.

METHODS: In a prospective series, 11 patients (ages, 20-63 years; mean, 41.9 ± 14.9 years, 2 women) with tumors located in or adjacent to the motor cortex were evaluated for surgery. fMRI and nTMS were applied for preoperative assessment of the extent of tumor resection. A 3-dimensional anatomic data set with superimposed fMRI data was integrated in the eXimia Navigated Brain Stimulation station for ensuing motor cortex mapping by nTMS. Responses from nTMS were evaluated by electromyographic response. During surgery, the coordinates of each DCS site were unambiguously defined and integrated into neuronavigation. A post hoc comparison of the coordinates of nTMS, fMRI, and DCS was performed.

RESULTS: Distances from nTMS to DCS (10.5 ± 5.67 mm) were significantly smaller than those from fMRI to DCS (15.0 ± 7.6 mm).

CONCLUSION: nTMS anticipates information usually only enabled by DCS and therefore allows surgical planning in eloquent cortex surgery.