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.

Surgery of Insular Diffuse Gliomas—Part 2: Probabilistic Cortico-Subcortical Atlas of Critical Eloquent Brain Structures and Probabilistic Resection Map During Transcortical Awake Resection

Neurosurgery 89:579–590, 2021

Insular diffuse glioma surgery is challenging, and tools to help surgical planning could improve the benefit-to-risk ratio.

OBJECTIVE: To provide a probabilistic resection map and frequency atlases of critical eloquent regions of insular diffuse gliomas based on our surgical experience.

METHODS: We computed cortico-subcortical “eloquent” anatomic sites identified intraoperatively by direct electrical stimulations during transcortical awake resection of insular diffuse gliomas in adults.

RESULTS: From 61 insular diffuse gliomas (39 left, 22 right; all left hemispheric dominance for language), we provided a frequency atlas of eloquence of the opercula (left/right; pars orbitalis: 0%/5.0%; pars triangularis: l5.6%/4.5%; pars opercularis: 37.8%/27.3%; precentral gyrus: 97.3%/95.4%; postcentral and supramarginal gyri: 75.0%/57.1%; temporal pole and superior temporal gyrus: 13.3%/0%), which tailored the transcortical approach (frontal operculum to reach the antero-superior insula, temporal operculum to reach the inferior insula, parietal operculum to reach the posterior insula). We provided a frequency atlas of eloquence identifying the subcortical functional boundaries (36.1% pyramidal pathways, 50.8% inferior fronto-occipital fasciculus, 13.1% arcuate and superior longitudinal fasciculi complex, 3.3% somatosensory pathways, 8.2% caudate and lentiform nuclei). Vascular boundaries and increasing errors during testing limited the resection in 8.2% and 11.5% of cases, respectively. We provided a probabilistic 3-dimensional atlas of resectability.

CONCLUSION: Functional mapping under awake conditions has to be performed intraoperatively in each patient to guide surgical approach and resection of insular diffuse gliomas in right and left hemispheres. Frequency atlases of opercula eloquence and of subcortical eloquent anatomic boundaries, and probabilistic 3-dimensional atlas of resectability could guide neurosurgeons.