In Reply: Planning Brain Tumor Resection Using a Probabilistic Atlas of Cortical and Subcortical Structures Critical for Functional Processing: A Proof of Concept.

To the Editor: We read the comments by Shalom et al1 to our work2 published in Operative Neurosurgery as proof of concept for the implementation of neurosurgical planning with the knowledge coming from the most extensive data set of functional and probabilistic cortical and subcortical evidences obtained with brain mapping and cognitive monitoring.3-5 This letter is a chance to comment and highlight some interesting evolution in the field of clinical and surgical neurosciences. As Shalom et al,1 we also appreciate the report of the experience of Andrews et al2 about the so-called “Broca Aphasia.” We all agree that resection of Broca area does not necessarily generate Broca aphasia. This phenomenon has extensively described and explained by ourselves in the past 15 years.6-10 Our work in the field of brain mapping and in the definition of the main cortical hubs and subcortical main streams for processing of language (and nonlanguage) functions not only resulted in a reappraisal of the functional anatomy of Broca area but also broke with the classic localizationist view of brain processing.8,11,12 In particular, we recently released a functional probabilistic atlas of the speech articulatory network, obtained with an unprecedented resting-state whole-brain seed-based analysis from direct electrical stimulation (DES) sites obtained during awake surgery.13 In other words, we have demonstrated using intrasurgical DES mapping that the dogmatic and static view of the brain functional organization is now overpassed, and therefore, we should evolve toward a meta-networking model based on dynamic interactions within and between neural circuits.14 In this new framework, we have provided more and more evidence about the role of white matter tracts and distributed cortical epicenters,15 leading to a considerable interindividual variability because of pathological and physiological processes.16,17 Of course, this personalized cerebral reconfiguration should be taken into account for planning safe and modern brain tumor resections.18 Just in this light, our group proposed the highest amount of brain mapping data in patients with glioma with the goal, on one hand, to clarify some mechanisms and crucial pathways of brain processing and, to the other hand, to provide a probabilistic overview of the possible distribution of such complex, multimodal, and bihemispherical networks. Indeed, it seems important to remind that we have investigated mechanisms underpinning neuroplasticity for almost 2 decades, especially in the event of glioma, using both intraoperative DES and perioperative functional neuroimaging.19-23 As consequence, we are the first to claim that DES mapping with cognitive monitoring is the gold standard for glioma surgery, especially at the subcortical level, for improving the knowledge of this complex biological system in a neurosurgical perspective, that is, at the individual level.24 DES data have the most reliable causal mapping for cognitive functions in the hands of neurosurgeons. It is also the sole tool providing inferences about the distribution of workflow at subcortical level, that is the most crucial information in neurosurgical practice and allowed development of the “connectome-based” concept.25 On this basis, the value of our DES probabilistic atlas is mainly related to the improvement for younger neurosurgeons of their mental and spatial 3-dimensional imagery of the functional cortical and subcortical networks critical for brain functions because it is of utmost importance to insist on the fact that functional MRI, regularly used for preoperative planning by many teams worldwide, is not able to differentiate essential from compensable cortical structures and that tractography is only an indirect mirror of neural functions.26 Of course, our atlas does not exclude the use of other mapping techniques because in this light, we reported the first tool for the automatic extraction of resting-state functional network at the individual level.27 Concluding, our unique atlas, computed on the basis of the real anatomo functional truth observed during awake mapping, both at cortical and axonal levels, is first of all a didactic tool which aims of giving the opportunity to young brain surgeons to better plan their surgical resection according to the limitations of neuroplasticity that we have extensively reported, ie, mostly represented by the subcortical connectivity.11,21,28 Because this is a probabilistic map, it will never replace intrasurgical DES combined with online cognitive monitoring throughout resection, but it could be helpful to better anticipate the relationships between the tumor and the neural pathways to select appropriately the tasks to be performed by the patient into the operating theater.29 This atlas which results from an integrative and multimodal approach, capable to provide reliable insights about the connectomal organization of cortices and white matter tracts, may improve the awareness of neurosurgeon about the neural structures and functions30,31 and may reinforce the link between fundamental neurosciences and neurosurgical implications.