Eloquent noneloquence: redefinition of cortical eloquence based on outcomes of superficial cerebral cavernous malformation resection

J Neurosurg 141:291–305, 2024

Cerebral cavernous malformations (CMs) are pathological lesions that cause discrete cortical disruption with hemorrhage, and their transcortical resections can cause additional iatrogenic disruption. The analysis of microsurgically treated CMs might identify areas of “eloquent noneloquence,” or cortex that is associated with unexpected deficits when injured or transgressed.

METHODS Patients from a consecutive microsurgical series of superficial cerebral CMs who presented to the authors’ center over a 13-year period were retrospectively analyzed. Neurological outcomes were measured using the modified Rankin Scale (mRS), and new, permanent neurological or cognitive symptoms not detected by changes in mRS scores were measured as additional functional decline. Patients with multiple lesions and surgical encounters for different lesions within the study interval were represented within the cohort as multiple patient entries. Virtual object models for CMs and approach trajectories to subcortical lesions were merged into a template brain model for subtyping and Quicktome connectomic analyses. Parcellation outputs from the models were analyzed for regional cerebral clustering.

RESULTS Overall, 362 CMs were resected in 346 patients, and convexity subtypes were the most common (132/362, 36.5%). Relative to the preoperative mRS score, 327 of 362 cases (90.3%) were in patients who improved or remained stable, 35 (9.7%) were in patients whose conditions worsened, and 47 (13.0%) were in patients who had additional functional decline. Machine learning analyses of lesion objects and trajectory cylinder mapping identified 7 hotspots of novel eloquence: supplementary motor area (bilateral), anterior cingulate cortex (bilateral), posterior cingulate cortex (bilateral), anterior insula (left), frontal pole (right), mesial temporal lobe (left), and occipital cortex (right).

CONCLUSIONS Transgyral and transsulcal resections that circumvent areas of traditional eloquence and navigate areas of presumed noneloquence may nonetheless result in unfavorable outcomes, demonstrating that brain long considered by neurosurgeons to be noneloquent may be eloquent. Eloquent hotspots within multiple large-scale networks redefine the neurosurgical concept of eloquence and call for more refined dissection techniques that maximize transsulcal dissection, intracapsular resection, and tissue preservation. Human connectomics, awareness of brain networks, and prioritization of cognitive outcomes require that we update our concept of cortical eloquence and incorporate this information into our surgical strategies.

Brain connectomics applied to oncological neuroscience: from a traditional surgical strategy focusing on glioma topography to a meta-network approach

Acta Neurochirurgica (2021) 163:905–917

The classical way for surgical selection and planning in cerebral glioma mainly focused on tumor topography. The emerging science of connectomics, which aims of mapping brain connectivity, resulted in a paradigmatic shift from a modular account of cerebral organization to a meta-network perspective. Adaptive behavior is actually mediated by constant changes in interactions within and across large-scale delocalized neural systems underlying conation, cognition, and emotion.

Here, to optimize the onco-functional balance of glioma surgery, the purpose is to switch toward a connectome-based resection taking account of both relationships between the tumor and critical distributed circuits (especially subcortical pathways) as well as the perpetual instability of the meta-network. Such dynamic in the neural spatiotemporal integration permits functional reallocation leading to neurological recovery after massive resection in structures traditionally thought as “inoperable.” This better understanding of connectome increases benefit/risk ratio of surgery (i) by selecting resection in areas deemed “eloquent” according to a localizationist dogma; (ii), conversely, by refining intraoperative awake cognitive mapping and monitoring in so-called non-eloquent areas; (iii) by improving preoperative information, enabling an optimal selection of intrasurgical tasks tailored to the patient’s wishes; (iv) by developing an “oncological disconnection surgery”; (v) by defining a personalized multistep surgical strategy adapted to individual brain reshaping potential; and (vi) ultimately by preserving environmentally and socially appropriate behavior, including return to work, while increasing the extent of (possibly repeated) resection(s).

Such a holistic vision of neural processing can enhance reliability of connectomal surgery in oncological neuroscience and may also be applied to restorative neurosurgery.

Use of diffusion tensor imaging in glioma resection

DTI.glioma

Neurosurg Focus 34 (4):E1, 2013 

Diffusion tensor imaging (DTI) is increasingly used in the resection of both high- and low-grade gliomas. Whereas conventional MRI techniques provide only anatomical information, DTI offers data on CNS connectivity by enabling visualization of important white matter tracts in the brain

Importantly, DTI allows neurosurgeons to better guide their surgical approach and resection. Here, the authors review basic scientific principles of DTI, include a primer on the technology and image acquisition, and outline the modality’s evolution as a frequently used tool for glioma resection.

Current literature supporting its use is summarized, highlighting important clinical studies on the application of DTI in preoperative planning for glioma resection, preoperative diagnosis, and postoperative outcomes.

The authors conclude with a review of future directions for this technology.