Peggy Gatignol

Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere

OBJECT Despite better knowledge of cortical language organization, its subcortical anatomofunctional connectivity remains poorly understood. The authors used intraoperative subcortical stimulation in awake patients undergoing operation for a glioma in the left dominant hemisphere to map the language pathways and to determine the contribution of such a method to surgical results. METHODS One hundred fifteen patients harboring a World Health Organization Grade II glioma within language areas underwent operation after induction of local anesthesia, using direct electrical stimulation to perform online cortical and subcortical language mapping throughout the resection. RESULTS After detection of cortical language sites, the authors identified 1 or several of the following subcortical language pathways in all patients: 1) arcuate fasciculus, eliciting phonemic paraphasia when stimulated; 2) inferior frontooccipital fasciculus, generating semantic paraphasia when stimulated; 3) subcallosal fasciculus, inducing transcortical motor aphasia during stimulation; 4) frontoparietal phonological loop, eliciting speech apraxia during stimulation; and 5) fibers coming from the ventral premotor cortex, inducing anarthria when stimulated. These structures were preserved, representing the limits of the resection. Despite a transient immediate postoperative worsening, all but 2 patients (98%) returned to baseline or better. On control MR imaging, 83% of resections were total or subtotal. CONCLUSIONS These results represent the largest experience with human subcortical language mapping ever reported. The use of intraoperative cortical and subcortical stimulation gives a unique opportunity to perform an accurate and reliable real-time anatomofunctional study of language connectivity. Such knowledge of the individual organization of language networks enables practitioners to optimize the benefit-to-risk ratio of surgery for Grade II glioma within the left dominant hemisphere.

Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation

Objectives: To describe functional recovery after surgical resection of low grade gliomas (LGG) in eloquent brain areas, and discuss the mechanisms of compensation. Methods: Seventy-seven right-handed patients without deficit were operated on for a LGG invading primary and/or secondary sensorimotor and/or language areas, as shown anatomically by pre-operative MRI and intraoperatively by electrical brain stimulation and cortico-subcortical mapping. Results: Tumours involved 31 supplementary motor areas, 28 insulas, 8 primary somatosensory areas, 4 primary motor areas, 4 Broca’s areas, and 2 left temporal language areas. All patients had immediate post-operative deficits. Recovery occurred within 3 months in all except four cases (definitive morbidity: 5%). Ninety-two percent of the lesions were either totally or extensively resected on post-operative MRI. Conclusions: These findings suggest that spatio-temporal functional re-organisation is possible in peritumoural brain, and that the process is dynamic. The recruitment of compensatory areas with long term perilesional functional reshaping would explain why: before surgery, there is no clinical deficit despite the tumour growth in eloquent regions; immediately after surgery, the occurrence of a deficit, which could be due to the resection of invaded areas participating (but not essential) to the function; and why three months after surgery, almost complete recovery had occurred. This brain plasticity, which decreases the long term risk of surgical morbidity, may be used to extend the limits of surgery in eloquent areas.

Long-term brain plasticity allowing a multistage surgical approach to World Health Organization Grade II gliomas in eloquent areas

Although the goal of surgery for World Health Organization Grade II gliomas is maximal extent of resection, complete tumor removal is not always possible when the glioma involves eloquent areas. The authors propose a multistage surgical approach to highly crucial areas that are classically considered inoperable, enabling optimization of the extent of resection while avoiding permanent cognitive deficits due to induced functional reshaping in the interim between the 2 consecutive operations. To demonstrate such plasticity, the authors used a combination of sequential functional MR imaging and intraoperative electrical stimulation mapping before and during surgeries spaced by several years in 2 patients who each underwent 2 separate resections of Grade II gliomas located in the left dominant premotor area. During several years of follow-up after the first procedure, both patients had unremarkable examination results and normal socioprofessional lives. There was no malignant transformation. Based on their experience with these cases, the authors suggest that in cases of incomplete glioma removal, a second operation before anaplasia should be considered, made possible by brain reorganization after the first operation.

The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients

Although the role of the premotor cortex (PMC) was widely studied in motor function, very few data are currently available about the participation of this structure in language. We report a series of 25 right-handed patients harboring a low-grade glioma near or within the left dominant PMC, operated on under local anesthesia with intraoperative real-time sensorimotor and language mappings using electrical stimulations all along the resection. Language tasks consisted of counting and picture naming (preceded by the reading of a short sentence). Stimulations of the left PMC induced transient speech disturbances in all patients, with disruption of both counting and reading/naming during stimulation of the ventral PMC--due to elicitation of an anarthria--while generating an anomia during stimulation of the dorsal PMC. Moreover, corresponding subcortical pathways generated the same language disorders as at the cortical level when stimulated. Eloquent structures were systematically preserved, allowing the avoidance of definitive postoperative deficit. These findings suggest first that the left dominant PMC seems to play a major role in language and second that this structure could have a well-ordered functional organization, namely with the ventral PMC, which might be involved in planification of articulation, and the dorsal PMC, which might be involved in the naming network.

Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations

OBJECT Diffusion tensor (DT) imaging tractography is increasingly used to map fiber tracts in patients with surgical brain lesions to reduce the risk of postoperative functional deficit. There are few validation studies of DT imaging tractography in these patients. The aim of this study was to compare DT imaging tractography of language fiber tracts by using intraoperative subcortical electrical stimulations. METHODS The authors included 10 patients with low-grade gliomas or dysplasia located in language areas. The MR imaging examination included 3D T1-weighted images for anatomical coregistration, FLAIR, and DT images. Diffusion tensors and fiber tracts were calculated using in-house software. Four tracts were reconstructed in each patient including the arcuate fasciculus, the inferior occipitofrontal fasciculus, and 2 premotor fasciculi (the subcallosal medialis fiber tract and cortical fibers originating from the medial and lateral premotor areas). The authors compared fiber tracts reconstructed using DT imaging with those evidenced using intraoperative subcortical language mapping. RESULTS Seventeen (81%) of 21 positive stimulations were concordant with DT imaging fiber bundles (located within 6 mm of a fiber tract). Four positive stimulations were not located in the vicinity of a DT imaging fiber tract. Stimulations of the arcuate fasciculus mostly induced articulatory and phonemic/syntactic disorders and less frequently semantic paraphasias. Stimulations of the inferior occipitofrontal fasciculus induced semantic paraphasias. Stimulations of the premotor-related fasciculi induced dysarthria and articulatory planning deficit. CONCLUSIONS There was a good correspondence between positive stimulation sites and fiber tracts, suggesting that DT imaging fiber tracking is a reliable technique but not yet optimal to map language tracts in patients with brain lesions. Negative tractography does not rule out the persistence of a fiber tract, especially when invaded by the tumor. Stimulations of the different tracts induced variable language disorders that were specific to each fiber tract.

The role of dominant striatum in language: a study using intraoperative electrical stimulations

Background: The role of the striatum in language remains poorly understood. Intraoperative electrical stimulation during surgery for tumours involving the caudate nucleus or putamen in the dominant hemisphere might be illuminating. Objectives: To study the role of these structures in language, with the aim of avoiding postoperative definitive aphasia. Methods: 11 patients with cortico-subcortical low grade gliomas were operated on while awake, and striatal functional mapping was done. Intraoperative direct electrical stimulation was used while the patients carried out motor and naming tasks during the resection. Results: In five cases of glioma involving the dominant putamen, stimulations induced anarthria, while in six cases of glioma involving the dominant caudate, stimulations elicited perseveration. There was no motor effect. The striatum was systematically preserved. Postoperatively, all patients except one had transient dysphasia which resolved within three months. Conclusions: There appear to be two separate basal ganglia systems in language, one mediated by the putamen which might have a motor role, and one by the caudate which might have a role in cognitive control. These findings could have implications for surgical strategy in lesions involving the dominant striatum.

Resection of world health organization grade II gliomas involving Broca's area: Methodological and functional considerations - Commentary

OBJECTIVEAdvances in functional mapping have enabled us to extend the indications of surgery for low-grade gliomas (LGGs) within eloquent regions. However, to our knowledge, no study has been specifically dedicated to the resection of LGGs within Brocas area. We report the first surgical series of LGGs involving this area by focusing on methodological and functional considerations. METHODSSeven patients harboring an LGG in Brocas area (revealed by partial seizures) had a language functional magnetic resonance imaging scan and then underwent operation while awake using intrasurgical electrical mapping. RESULTSThe neurological examination was normal in all patients despite mild language disturbances shown using the Boston Diagnosis Aphasia Examination. Both pre- and intraoperative cortical mapping found language reorganization with recruitment of the ventral and dorsal premotor cortices, orbitofrontal cortex, and insula, whereas no or few language sites were detected within Brocas area. Subcortically, electrostimulation allowed the identification and preservation of four structures still functional, including the arcuate fasciculus, fronto-occipital fasciculus, fibers from the ventral premotor cortex, and head of the caudate. Postoperatively, after transient language worsening, all patients recovered and returned to a normal socioprofessional life. The resection was total in three cases, subtotal in three, and partial in one patient (operated twice). CONCLUSIONOur results indicate that, in patients with no aphasia despite LGGs within Brocas area, thanks to brain plasticity, the tumor can be removed while involving this “unresectable” structure without inducing sequelae and even improving the quality of life when intractable epilepsy is relieved on the condition that subcortical language connectivity is preserved.

The insular lobe and brain plasticity: Lessons from tumor surgery.

OBJECTIVES Despite recent literature supporting the likely role of the insula in many functions, the actual participation of this multimodal lobe in the brain functioning remains unclear, i.e. has the insula an essential or compensable role? PATIENTS AND METHODS We surgically resected an insular low-grade glioma, using intraoperative electrical stimulation, in 42 patients who experienced seizures, but who presented no or only a slight neurological deficit. Surgery was performed under local anesthesia in patients with a lesion in the dominant hemisphere. The resection was systematically stopped according to cortico-subcortical functional boundaries. RESULTS Intraoperative electrical mapping induced language disturbances, pain and vertigo, but no other side effects were observed. Post-operatively, the patients experienced a transient hemiparesis in 21 cases, language disorders in 10 cases, an athymhormic syndrome in 7 cases, a Foix-Chavany-Marie syndrome in 3 cases, and micturition disturbances in one case. Despite this immediate post-surgical worsening, all the patients recovered their preoperative neurological status within 3 months, except in three cases due to a deep stroke. CONCLUSION These results show that the insula, a complex associative multimodal structure poorly studied until now, can be functionally compensated. Such a plastic potential may have important fundamental and clinical implications, in particular in the field of oncological neurosurgery.

Functional outcome after language mapping for insular World Health Organization Grade II gliomas in the dominant hemisphere: experience with 24 patients

OBJECT Despite the report of recent experiences of insular surgery in the past decade, there has been no series specifically dedicated to studying functional outcome following resection of insular WHO Grade II gliomas involving the dominant hemisphere, in patients with no or only mild preoperative language deficit. In this article, the authors analyze the contribution of awake mapping for preservation of brain function, especially language, in a homogeneous series of 24 patients who underwent surgery for insular Grade II gliomas within the dominant insular lobe. METHODS Twenty-four patients underwent surgery for an insular Grade II glioma involving the dominant hemisphere (22 left, 2 right), revealed by seizures in all but 1 case. The preoperative neurological examination result was normal in 17 patients (71%), whereas 7 patients presented with language disorders detected using an accurate language assessment performed by a speech therapist. All surgeries were performed on awake patients utilizing intra-operative language mapping involving cortical and subcortical stimulation. RESULTS There were no intrasurgical complications or postsurgical sensorimotor deficits. Despite an immediate postoperative language worsening in 12 cases (50%), all patients recovered to a normal status within 3 months, and 6 cases even improved in comparison with their preoperative examination results. The 24 patients returned to normal social and professional lives. Moreover, the surgery had a favorable impact on epilepsy in all but 4 cases (83%). On control MR imaging, 62.5% of resections were total or subtotal. Three patients underwent a second or third awake surgery, with no additional deficit. All but 2 patients (92%) are alive after a mean follow-up of 3 years (range 3-133 months). CONCLUSIONS Although insular surgery was long believed to be too risky, the present results show that the rate of permanent deficit, especially dysphasia, following resection of Grade II gliomas involving the dominant insula has been dramatically reduced (none in this patient series), thanks to the systematic use of intraoperative awake mapping, even in cases of repeated operations. Furthermore, patient quality of life may be improved due to a decrease of epilepsy after surgery. Thus, the authors suggest systematically considering resection when an insular Grade II glioma is diagnosed after seizures in a patient with no or mild deficit, even a glioma invading the dominant hemisphere.

Is the Human Left Middle Longitudinal Fascicle Essential for Language? A Brain Electrostimulation Study

Human brain pathways required for language processing are poorly known. A new white matter tract in humans, the middle longitudinal fascicle, has recently been anatomically determined by diffusion tensor imaging and suggested to be essential for language. Our aim is to determine the importance of the middle longitudinal fascicle for language processing. This study is based on 8 patients with glioma resection at least involving the superior temporal gyrus of the left dominant hemisphere. Language is systematically examined pre‐ and postoperatively at 3 months. Intraoperative electrostimulation is used to map cortical and subcortical structures as functional boundaries of the glioma resection, including those essential for language processing. The resections are extensive (on average 62 ml, ranging from 21 to 111 ml) and include a large part of the middle longitudinal fascicle in all patients. Intraoperatively, no interference with picture naming is observed by electrostimulation of the middle longitudinal fascicle, while in all patients the inferior fronto‐occipital fascicle is identified by eliciting semantic paraphasia as functional boundary. Postoperatively, no new permanent language deficits are detected by systematic language examination. Therefore, we suggest that the middle longitudinal fascicle may participate but is not essential for language processing. Hum Brain Mapp, 2011.