A novel cognitive neurosurgery approach for supramaximal resection of non-dominant precuneal gliomas: a case report.

Despite mounting evidence pointing to the contrary, classical neurosurgery presumes many cerebral regions are non-eloquent, and therefore, their excision is possible and safe. This is the case of the precuneus and posterior cingulate, two interacting hubs engaged during various cognitive functions, including reflective self-awareness; visuospatial and sensorimotor processing; and processing social cues. This inseparable duo ensures the cortico-subcortical connectivity that underlies these processes. An adult presenting a right precuneal low-grade glioma invading the posterior cingulum underwent awake craniotomy with direct electrical stimulation (DES). A supramaximal resection was achieved after locating the superior longitudinal fasciculus II. During surgery, we found sites of positive stimulation for line bisection and mentalizing tests that enabled the identification of surgical corridors and boundaries for lesion resection. When post-processing the intraoperative recordings, we further identified areas that positively responded to DES during the trail-making and mentalizing tests. In addition, a clear worsening of the patient's self-assessment ability was observed throughout the surgery. An awake cognitive neurosurgery approach allowed supramaximal resection by reaching the cortico-subcortical functional limits. The mapping of complex functions such as social cognition and self-awareness is key to preserving patients' postoperative cognitive health by maximizing the ability to resect the lesion and surrounding areas.

"Neural dynamics supporting longitudinal plasticity of action naming across languages: MEG evidence from bilingual brain tumor patients".

Previous evidence suggests that distinct ventral and dorsal streams respectively underpin the semantic processing of object and action knowledge. Recently, we found that brain tumor patients with dorsal gliomas in frontoparietal hubs show a selective longitudinal compensation (post-vs. pre-surgery) during the retrieval of lexico-semantic information about actions (but not objects), indexed by power increases in beta rhythms (13-28 Hz). Here, we move one-step further and ask whether a similar organizational principle also stands across the different languages a bilingual speaks. To test this hypothesis, we combined a picture-naming task with MEG recordings and evaluated highly proficient Spanish-Basque bilinguals undergoing surgery for tumor resection in left frontoparietal regions. We assessed patients before and three months after surgery. At the behavioral level, we observed a similar performance across sessions irrespectively of the language at use, suggesting overall successful function preservation. At the oscillatory level, we found longitudinal selective power increases in beta for action naming in Spanish and Basque. Nevertheless, tumor resection triggered a differential reorganization of the L1 and the L2, with the latter one additionally recruiting the right hemisphere. Overall, our results provide evidence for (i) the specific involvement of frontoparietal regions in the semantic retrieval/representation of action knowledge across languages; (ii) a key role of beta oscillations as a signature of language compensation and (iii) the existence of divergent plasticity trajectories in L1 and L2 after surgery. By doing so, they provide new insights into the spectro-temporal dynamics supporting postoperative recovery in the bilingual brain.

What Can Glioma Patients Teach Us about Language (Re)Organization in the Bilingual Brain: Evidence from fMRI and MEG.

Recent evidence suggests that the presence of brain tumors (e.g., low-grade gliomas) triggers language reorganization. Neuroplasticity mechanisms called into play can transfer linguistic functions from damaged to healthy areas unaffected by the tumor. This phenomenon has been reported in monolingual patients, but much less is known about the neuroplasticity of language in the bilingual brain. A central question is whether processing a first or second language involves the same or different cortical territories and whether damage results in diverse recovery patterns depending on the language involved. This question becomes critical for preserving language areas in bilingual brain-tumor patients to prevent involuntary pathological symptoms following resection. While most studies have focused on intraoperative mapping, here, we go further, reporting clinical cases for five bilingual patients tested before and after tumor resection, using a novel multimethod approach merging neuroimaging information from fMRI and MEG to map the longitudinal reshaping of the language system. Here, we present four main findings. First, all patients preserved linguistic function in both languages after surgery, suggesting that the surgical intervention with intraoperative language mapping was successful in preserving cortical and subcortical structures necessary for brain plasticity at the functional level. Second, we found reorganization of the language network after tumor resection in both languages, mainly reflected by a shift of activity to right hemisphere nodes and the recruitment of ipsilesional left nodes. Third, we found that this reorganization varied according to the language involved, indicating that L1 and L2 follow different reshaping patterns after surgery. Fourth, oscillatory longitudinal effects were correlated with BOLD laterality changes in superior parietal and middle frontal areas. These findings may reflect that neuroplasticity impacts on the compensatory involvement of executive control regions, supporting the allocation of cognitive resources as a consequence of increased attentional demands. Furthermore, these results hint at the complementary role of this neuroimaging approach in language mapping, with fMRI offering excellent spatial localization and MEG providing optimal spectrotemporal resolution.

Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study.

Recent evidence suggests that damage to the language network triggers its functional reorganization. Yet, the spectro-temporal fingerprints of this plastic rearrangement and its relation to anatomical changes is less well understood. Here, we combined magnetoencephalographic recordings with a proxy measure of white matter to investigate oscillatory activity supporting language plasticity and its relation to structural reshaping. First, cortical dynamics were acquired in a group of healthy controls during object and action naming. Results showed segregated beta (13-28 Hz) power decreases in left ventral and dorsal pathways, in a time-window associated to lexico-semantic processing (~250-500 ms). Six patients with left tumors invading either ventral or dorsal regions performed the same naming task before and 3 months after surgery for tumor resection. When longitudinally comparing patients' responses we found beta compensation mimicking the category-based segregation showed by controls, with ventral and dorsal damage leading to selective compensation for object and action naming, respectively. At the structural level, all patients showed preoperative changes in white matter tracts possibly linked to plasticity triggered by tumor growth. Furthermore, in some patients, structural changes were also evident after surgery and showed associations with longitudinal changes in beta power lateralization toward the contralesional hemisphere. Overall, our findings support the existence of anatomo-functional dependencies in language reorganization and highlight the potential role of oscillatory markers in tracking longitudinal plasticity in brain tumor patients. By doing so, they provide valuable information for mapping preoperative and postoperative neural reshaping and plan surgical strategies to preserve language function and patient's quality of life.

MULTIMAP: Multilingual picture naming test for mapping eloquent areas during awake surgeries.

Picture naming tasks are currently the gold standard for identifying and preserving language-related areas during awake brain surgery. With multilingual populations increasing worldwide, patients frequently need to be tested in more than one language. There is still no reliable testing instrument, as the available batteries have been developed for specific languages. Heterogeneity in the selection criteria for stimuli leads to differences, for example, in the size, color, image quality, and even names associated with pictures, making direct cross-linguistic comparisons difficult. Here we present MULTIMAP, a new multilingual picture naming test for mapping eloquent areas during awake brain surgery. Recognizing that the distinction between nouns and verbs is necessary for detailed and precise language mapping, MULTIMAP consists of a database of 218 standardized color pictures representing both objects and actions. These images have been tested for name agreement with speakers of Spanish, Basque, Catalan, Italian, French, English, German, Mandarin Chinese, and Arabic, and have been controlled for relevant linguistic features in cross-language combinations. The MULTIMAP test for objects and verbs represents an alternative to the Oral Denomination 80 (DO 80) monolingual pictorial set currently used in language mapping, providing an open-source, standardized set of up-to-date pictures, where relevant linguistic variables across several languages have been taken into account in picture creation and selection.

A Practical Approach to Imaging of the Supplementary Motor Area and Its Subcortical Connections.

PURPOSE OF REVIEW: First, an anatomical and functional review of these cortical areas and subcortical connections with T-fMRI and tractography techniques; second, to demonstrate the value of this approach in neurosurgical planning in a series of patients with tumors close to the SMA. RECENT FINDINGS: Implications in language and cognitive networks with a clear hemispheric lateralization of these SMA/pre-SMA. The recommendation of the use of the advanced neuroimaging studies for surgical planning and preservation of these areas. The SMA/pre-SMA and their subcortical connections are functional areas to be taken into consideration in neurosurgical planning. These areas would be involved in the control/inhibition of movement, in verbal expression and fluency and in tasks of cognitive control capacity. Its preservation is key to the patient's postsurgical cognitive and functional evolution.

Spatiotemporal dynamics of postoperative functional plasticity in patients with brain tumors in language areas.

Postoperative functional neuroimaging provides a unique opportunity to investigate the neural mechanisms that facilitate language network reorganization. Previous studies in patients with low grade gliomas (LGGs) in language areas suggest that postoperative recovery is likely due to functional neuroplasticity in peritumoral and contra-tumoral healthy regions, but have attributed varying degrees of importance to specific regions. In this study, we used Magnetoencephalography (MEG) to investigate functional connectivity changes in peritumoral and contra-tumoral regions after brain tumor resection. MEG recordings of cortical activity during resting-state were obtained from 12 patients with LGGs in left-hemisphere language brain areas. MEG data were recorded before (Pre session), and 3 (Post_1 session) and 6 (Post_2 session) months after awake craniotomy. For each MEG session, we measured the functional connectivity of the peritumoral and contra-tumoral regions to the rest of the brain across the 1-100 Hz frequency band. We found that functional connectivity in the Post_1 and Post_2 sessions was higher than in the Pre session only in peritumoral regions and within the alpha frequency band. Functional connectivity in peritumoral regions did not differ between the Post_1 and Post_2 sessions. Alpha connectivity enhancement in peritumoral regions was observed in all patients regardless of the LGG location. Together, these results suggest that postoperative language functional reorganization occurs in peritumoral regions regardless of the location of the tumor and mostly develops within 3 months after surgery.

Survey on current practice within the European Low-Grade Glioma Network: where do we stand and what is the next step?

Diffuse low-grade glioma form a rare entity affecting young people. Despite advances in surgery, chemotherapy, and radiation therapy, diffuse low-grade glioma are still incurable. According to current guidelines, maximum safe resection, when feasible, is the first line of treatment. Apart from surgery, all other treatment modalities (temozolomide, procarbazine-CCNU-vincristine regimen, and radiation therapy) are handled very differently among different teams, and this in spite of recent results of several phase 3 studies. Based on a European survey, this paper aimed to get a picture of this heterogeneity in diffuse low-grade glioma management, to identify clinically relevant questions raised by this heterogeneity of practice, and to propose new methodological frameworks to address these questions.

Brain tumors in eloquent areas: A European multicenter survey of intraoperative mapping techniques, intraoperative seizures occurrence, and antiepileptic drug prophylaxis.

Intraoperative mapping and monitoring techniques for eloquent area tumors are routinely used world wide. Very few data are available regarding mapping and monitoring methods and preferences, intraoperative seizures occurrence and perioperative antiepileptic drug management. A questionnaire was sent to 20 European centers with experience in intraoperative mapping or neurophysiological monitoring for the treatment of eloquent area tumors. Fifteen centers returned the completed questionnaires. Data was available on 2098 patients. 863 patients (41.1%) were operated on through awake surgery and intraoperative mapping, while 1235 patients (58.8%) received asleep surgery and intraoperative electrophysiological monitoring or mapping. There was great heterogeneity between centers with some totally AW oriented (up to 100%) and other almost totally ASL oriented (up to 92%) (31% SD). For awake surgery, 79.9% centers preferred an asleep-awake-asleep anesthesia protocol. Only 53.3% of the centers used ECoG or transcutaneous EEG. The incidence of intraoperative seizures varied significantly between centers, ranging from 2.5% to 54% (p < 0.001). It there appears to be a statistically significant link between the mastery of mapping technique and the risk of intraoperative seizures. Moreover, history of preoperative seizures can significantly increase the risk of intraoperative seizures (p < 0.001). Intraoperative seizures occurrence was similar in patients with or without perioperative drugs (12% vs. 12%, p = 0.2). This is the first European survey to assess intraoperative functional mapping and monitoring protocols and the management of peri- and intraoperative seizures. This data can help identify specific aspects that need to be investigated in prospective and controlled studies.

Double dissociation between visual recognition and picture naming: a study of the visual language connectivity using tractography and brain stimulation.

BACKGROUND: Study of the corticosubcortical functional anatomy of reading and picture naming. OBJECTIVE: To study the role of the left basal occipitotemporal area and its white matter pathways. METHODS: Three patients underwent awake surgery for lesions in the left basal posterotemporal region with intraoperative electrostimulations. Intraoperative testing consisted of naming, reading, and recognition of symbols. Location of the stimulation sites was obtained by comparing the surgical cavity in the postoperative magnetic resonance imaging with the tags precisely located in each one of these sites seen on intraoperative photographs. RESULTS: A double dissociation was elicited, inducing specific visual recognition and reading disturbances during stimulation in the left posterobasal temporal cortex, without naming impairment. Stimulation of the inferior part of the sagittal stratum (inferior longitudinal fascicle) generated the same response, while a specific picture-naming impairment, consisting of semantic paraphasia, was obtained when stimulating superiorly to this fascicle, over the lateral wall and roof of the ventricle (inferior fronto-occipital fascicle). CONCLUSION: We propose the existence of a dual visual language route in the left dominant hemisphere. The first pathway seems to run basally, from the occipital lobe to the posterobasal temporal cortex, mediated by the left inferior longitudinal fascicle, subserving visual recognition. The second pathway might run superiorly and more medially, from the occipital pole directly to the frontal areas, and could be underlain by the inferior fronto-occipital fascicle, involved in naming (semantic processing). Such a model might have both fundamental and clinical implications for the selection of the tasks during awake mapping as well as for postsurgical rehabilitation.

Neurooncología funcional / Functional Neuro-Oncology

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Neurooncología funcional / Functional Neuro-Oncology

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Surgical management of World Health Organization Grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures.

OBJECT: Recent surgical studies have demonstrated that the extent of resection is significantly correlated with median survival in WHO Grade II gliomas. Consequently, thanks to advances in intraoperative functional mapping, the authors questioned whether it is actually necessary to leave a "security" margin around eloquent structures. METHODS: The authors first reviewed the classic literature, especially that based on epilepsy surgery and functional neuroimaging techniques, which led them to propose the rule of a security margin. Second, they detailed new developments in the field of intrasurgical electrical mapping, especially with regard to subcortical stimulation of the projection and long-distance association pathways. On the basis of these advances, the removal of gliomas according to functional boundaries has recently been suggested, with no margin around eloquent structures. RESULTS: Comparative results showed that the rate of permanent deficit was similar with or without a security margin, that is, < 2%. However, a higher rate of transient neurological worsening in the immediate postsurgical period was associated with the absence of a margin, with recovery following adapted rehabilitation. On the other hand, the extent of resection was in essence improved with no margin. CONCLUSIONS: This no-margin technique, based on the subpial dissection, and the repetition of both cortical and subcortical stimulation to preserve eloquent cortex as well as the white matter tracts (U-fibers, projection pathways, and long-distance connectivity) allow optimization of the extent of resection while preserving the quality of life (despite transitory impairment) thanks to mechanisms of brain plasticity.

Discrepancies between preoperative stereoencephalography language stimulation mapping and intraoperative awake mapping during resection of focal cortical dysplasia in eloquent areas.

BACKGROUND/AIMS: To compare the reliability of preoperative stereoencephalography (SEEG) and intraoperative electrostimulation regarding functional mapping, and to select the indication for surgery for focal cortical dysplasia (FCD) in language areas. METHODS: The authors present the case of a 21-year-old, right-handed female, suffering from chronic pharmacologically resistant epilepsy since the age of 8. MRI showed a subcortical hypersignal on FLAIR and T(2) sequences at the posterior end of the left superior temporal sulcus compatible with an FCD. SEEG invasive monitoring was performed to precisely identify the epileptogenic zone (EZ) and for functional language mapping. RESULTS: The stimulation of the contacts implicated in the EZ through SEEG leads induced language disturbances, which were not reproducible. Surgery was performed under local anesthesia with awake corticosubcortical mapping. Direct intraoperative stimulation in the EZ, including FCD, did not induce language disturbances. Thus, EZ could be removed completely without any postoperative language deficit. CONCLUSIONS: The present case suggests that when language disturbances which occur during invasive SEEG functional mapping, in eloquent areas, are not reproducible, resection can be considered using intraoperative electrical mapping, without inducing permanent language impairment. This may be explained by a certain degree of plasticity and reshaping of functional areas associated with a congenital lesion and chronic epilepsy.

Brain tumors and epilepsy.

When treating patients harboring a brain tumor, it is mandatory to integrate the dogmas of epilepsy into a neuro-oncological viewpoint. The frequency of seizures differs widely between low- and high-grade tumors because of different mechanisms of epileptogenesis. The modern theories of pathological neural networks, especially in low-grade gliomas, can provide the key for an in-depth understanding of the principles of connectionism that underline both seizures, cognitive impairment and plasticity. It is a consuetude that principles of general management of patients with nontumor-related epilepsy are applied to neuro-oncology. Nevertheless, since tumors are complex evolving lesions requiring a multidisciplinary treatment approach (surgery, radiotherapy and chemotherapy), it is mandatory to have a comprehensive view of the natural history of each lesion when choosing the best antiepileptic drug. More than two thirds of patients with brain tumors and medically intractable epilepsy benefit from (sub)total surgical resection. Therefore, these patients are good surgical candidates both for oncological and epileptological considerations, in order to change the natural history of the lesion and to improve the quality of life at the same time. However, 15% of patients still have intractable medical seizures after surgery. Moreover, the insula may participate more often than usually considered in (intractable) seizures. Therefore, in these patients, invasive EEG recordings and eventually a second epilepsy surgery might be proposed.