Immersive Virtual Reality and Ocular Tracking for Brain Mapping During Awake Surgery: Prospective Evaluation Study.

BACKGROUND: Language mapping during awake brain surgery is currently a standard procedure. However, mapping is rarely performed for other cognitive functions that are important for social interaction, such as visuospatial cognition and nonverbal language, including facial expressions and eye gaze. The main reason for this omission is the lack of tasks that are fully compatible with the restrictive environment of an operating room and awake brain surgery procedures. OBJECTIVE: This study aims to evaluate the feasibility and safety of a virtual reality headset equipped with an eye-tracking device that is able to promote an immersive visuospatial and social virtual reality (VR) experience for patients undergoing awake craniotomy. METHODS: We recruited 15 patients with brain tumors near language and/or motor areas. Language mapping was performed with a naming task, DO 80, presented on a computer tablet and then in 2D and 3D via the VRH. Patients were also immersed in a visuospatial and social VR experience. RESULTS: None of the patients experienced VR sickness, whereas 2 patients had an intraoperative focal seizure without consequence; there was no reason to attribute these seizures to virtual reality headset use. The patients were able to perform the VR tasks. Eye tracking was functional, enabling the medical team to analyze the patients' attention and exploration of the visual field of the virtual reality headset directly. CONCLUSIONS: We found that it is possible and safe to immerse the patient in an interactive virtual environment during awake brain surgery, paving the way for new VR-based brain mapping procedures. TRIAL REGISTRATION: ClinicalTrials.gov NCT03010943; https://clinicaltrials.gov/ct2/show/NCT03010943.

What effects does awake craniotomy have on functional and survival outcomes for glioblastoma patients?

PURPOSE: Neurosurgeons adopt several different surgical approaches to deal with glioblastomas (GB) located in or near eloquent areas. Some attempt maximal safe resection by awake craniotomy (AC), but doubts persist concerning the real benefits of this type of surgery in this situation. We performed a retrospective study to evaluate the extent of resection (EOR), functional and survival outcomes after AC of patients with GB in critical locations. METHODS: Forty-six patients with primary GB treated with the Stupp regimen between 2004 and 2019, for whom brain mapping was feasible, were included. We assessed EOR, postoperative language and/or motor deficits three months after AC, progression-free survival (PFS) and overall survival (OS). RESULTS: Complete resection was achieved in 61% of the 46 GB patients. The median PFS was 6.8 months (CI 6.1; 9.7) and the median OS was 17.6 months (CI 14.8; 34.1). Three months after AC, more than half the patients asymptomatic before surgery remained asymptomatic, and one third of patients with symptoms before surgery experienced improvements in language, but not motor functions. The risk of postoperative deficits was higher in patients with preoperative deficits or incomplete resection. Furthermore, the presence of postoperative deficits was an independent predictive factor for shorter PFS. CONCLUSION: AC is an option for the resection of GB in critical locations. The observed survival outcomes are typical for GB patients in the Stupp era. However, the success of AC in terms of the recovery or preservation of language and/or motor functions cannot be guaranteed, given the aggressiveness of the tumor.

Overt speech feasibility using continuous functional magnetic resonance imaging: Isolation of areas involved in phonology and prosody.

To avoid motion artifacts, almost all speech-related functional magnetic resonance imagings (fMRIs) are performed covertly to detect language activations. This method may be difficult to execute, especially by patients with brain tumors, and does not allow the identification of phonological areas. Here, we aimed to evaluate overt task feasibility. Thirty-three volunteers participated in this study. They performed two functional sessions of covert and overt generation of a short sentence semantically linked with a word. Three main contrasts were performed: Covert and Overt for the isolation of language-activated areas, and Overt > Covert for the isolation of the motor cortical activation of speech. fMRI data preprocessing was performed with and without unwarping, and with and without regression of movement parameters as confounding variables. All types of results were compared to each other. For the Overt contrast, Dice coefficients showed strong overlap between each pair of types of results: 0.98 for the pair with and without unwarping, and 0.9 for the pair with and without movement parameter regression. The Overt > Covert contrast allowed isolation of motor laryngeal activations with high statistical reliability and revealed the right-lateralized temporal activity related to acoustic feedback. Overt speaking during magnetic resonance imaging induced few artifacts and did not significantly affect the results, allowing the identification of areas involved in primary motor control and prosodic regulation of speech. Unwarping and motion artifact regression in the postprocessing step, seem to not be necessary. Changes in lateralization of cortical activity by overt speech shall be explored before using these tasks for presurgical mapping.

The ventral attention network: the mirror of the language network in the right brain hemisphere.

Resting-state functional MRI (RfMRI) analyses have identified two anatomically separable fronto-parietal attention networks in the human brain: a bilateral dorsal attention network and a right-lateralised ventral attention network (VAN). The VAN has been implicated in visuospatial cognition and, thus, potentially in the unilateral spatial neglect associated with right hemisphere lesions. Its parietal, frontal and temporal endpoints are thought to be structurally supported by undefined white matter tracts. We investigated the white matter tract connecting the VAN. We used three approaches to study the structural anatomy of the VAN: (a) independent component analysis on RfMRI (50 subjects), defining the endpoints of the VAN, (b) tractography in the same 50 healthy volunteers, with regions of interest defined by the MNI coordinates of cortical areas involved in the VAN used in a seed-based approach and (c) dissection, by Klingler's method, of 20 right hemispheres, for ex vivo studies of the fibre tracts connecting VAN endpoints. The VAN includes the temporoparietal junction and the ventral frontal cortex. The endpoints of the superior longitudinal fasciculus in its third portion (SLF III) and the arcuate fasciculus (AF) overlap with the VAN endpoints. The SLF III connects the supramarginal gyrus to the ventral portion of the precentral gyrus and the pars opercularis. The AF connects the middle and inferior temporal gyrus and the middle and inferior frontal gyrus. We reconstructed the structural connectivity of the VAN and considered it in the context if the pathophysiology of unilateral neglect and right hemisphere awake brain surgery.

Resting-state functional magnetic resonance imaging versus task-based activity for language mapping and correlation with perioperative cortical mapping.

INTRODUCTION: Preoperative language mapping using functional magnetic resonance imaging (fMRI) aims to identify eloquent areas in the vicinity of surgically resectable brain lesions. fMRI methodology relies on the blood-oxygen-level-dependent (BOLD) analysis to identify brain language areas. Task-based fMRI studies the BOLD signal increase in brain areas during a language task to identify brain language areas, which requires patients' cooperation, whereas resting-state fMRI (rsfMRI) allows identification of functional networks without performing any explicit task through the analysis of the synchronicity of spontaneous BOLD signal oscillation between brain areas. The aim of this study was to compare preoperative language mapping using rsfMRI and task fMRI to cortical mapping (CM) during awake craniotomies. METHODS: Fifty adult patients surgically treated for a brain lesion were enrolled. All patients had a presurgical language mapping with both task fMRI and rsfMRI. Identified language networks were compared to perioperative language mapping using electric cortical stimulation. RESULTS: Resting-state fMRI was able to detect brain language areas during CM with a sensitivity of 100% compared to 65.6% with task fMRI. However, we were not able to perform a specificity analysis and compare task-based and rest fMRI with our perioperative setting in the current study. In second-order analysis, task fMRI imaging included main nodes of the SN and main areas involved in semantics were identified in rsfMRI. CONCLUSION: Resting-state fMRI for presurgical language mapping is easy to implement, allowing the identification of functional brain language network with a greater sensitivity than task-based fMRI, at the cost of some precautions and a lower specificity. Further study is required to compare both the sensitivity and the specificity of the two methods and to evaluate the clinical value of rsfMRI as an alternative tool for the presurgical identification of brain language areas.

Anatomical variability of the arcuate fasciculus: a systematical review.

PURPOSE: The arcuate fasciculus (AF) is a white matter fibers tract that links the lateral temporal with the frontal cortex. The AF can be divided into three components: two superficial indirect short tracts (anterior and posterior) and one deep direct long tract. Both DTI and white matter dissections studies find differences regarding the anatomy of the AF, especially its cortical connections. This paper aims at providing a comprehensive anatomical classification of the AF, using the terminologia anatomica. METHODS: Articles (n = 478) were obtained from a systematical PRISMA review. Studies which focused on primates, unhealthy subjects, as well as studies without cortical termination description and review articles were excluded from the analysis. One hundred and ten articles were retained for full-text examination, of which 19 finally fulfilled our criteria to be included in this review. RESULTS: We classified main descriptions and variations of each segment of the AF according to fiber orientation and cortical connections. Three types of connections were depicted for each segment of the AF. Concerning the anterior segment, most of the frontal fibers (59.35%) ran from the ventral portion of the precentral gyrus and the posterior part of the pars opercularis, to the supramarginal gyrus (85.0%). Main fibers of the posterior segment of the AF ran from the posterior portion of the middle temporal gyrus (100%) to the angular gyrus (92.0%). In main descriptions of the long segment of the AF, fibers ran from both the ventral portion of the precentral gyrus and posterior part of the pars opercularis (63.9%) to the middle and inferior temporal gyrus (60.3%). Minor subtypes were described in detail in the article. CONCLUSION: We provide a comprehensive classification of the anatomy of the AF, regarding the orientation and cortical connections of its fibers. Although fiber orientation is very consistent, cortical endings of the AF may be different from one study to another, or from one individual to another which is a key element to understand the anatomical basis of current models of language or to guide intraoperative stimulation during awake surgery.

Right Hemisphere Cognitive Functions: From Clinical and Anatomical Bases to Brain Mapping During Awake Craniotomy. Part II: Neuropsychological Tasks and Brain Mapping.

The nondominant hemisphere (usually right) is determinant for main cognitive functions such as visuospatial and social cognitions. Awake surgery using direct electrical stimulation for right cerebral tumor removal remains challenging due to the complexity of the functional anatomy and the difficulties in adapting the classical bedside tasks for awake surgery conditions. An understanding of semiology, anatomical bases, and an analysis of the available cognitive tasks for visuospatial and social cognition per operative mapping will allow neurosurgeons to better appreciate the functional anatomy of the right hemisphere and its application to tumor surgery. In this second review of 2 parts, we discuss the pertinence of the neuropsychological tests available for the study of nondominant hemisphere functions for the surgery on right-sided tumors in awake surgery conditions. In conjunction with part I of the review, which focuses primarily on the anatomical, functional, and semiological basis of the right hemisphere function, this article provides a comprehensive review of current knowledge supporting the awake surgery in the right hemisphere.

Using a Virtual Reality Social Network During Awake Craniotomy to Map Social Cognition: Prospective Trial.

BACKGROUND: In awake craniotomy, it is possible to temporarily inactivate regions of the brain using direct electrical stimulation, while the patient performs neuropsychological tasks. If the patient shows decreased performance in a given task, the neurosurgeon will not remove these regions, so as to maintain all brain functions. OBJECTIVE: The objective of our study was to describe our experience of using a virtual reality (VR) social network during awake craniotomy and discuss its future applications for perioperative mapping of nonverbal language, empathy, and theory of mind. METHODS: This was a single-center, prospective, unblinded trial. During wound closure, different VR experiences with a VR headset were proposed to the patient. This project sought to explore interactions with the neuropsychologist's avatar in virtual locations using a VR social network as an available experience. RESULTS: Three patients experienced VR. Despite some limitations due to patient positioning during the operation and the limitation of nonverbal cues inherent to the app, the neuropsychologist, as an avatar, could communicate with the patient and explore gesture communication while wearing a VR headset. CONCLUSIONS: With some improvements, VR social networks can be used in the near future to map social cognition during awake craniotomy. TRIAL REGISTRATION: ClinicalTrials.gov NCT03010943; https://clinicaltrials.gov/ct2/show/NCT03010943 (Archived at WebCite at http://www.webcitation.org/70CYDil0P).

Right Hemisphere Cognitive Functions: From Clinical and Anatomic Bases to Brain Mapping During Awake Craniotomy Part I: Clinical and Functional Anatomy.

The nondominant hemisphere (usually the right) is responsible for primary cognitive functions such as visuospatial and social cognition. Awake surgery using direct electric stimulation for right cerebral tumor removal remains challenging because of the complexity of the functional anatomy and difficulties in adapting standard bedside tasks to awake surgery conditions. An understanding of semiology and anatomic bases, along with an analysis of the available cognitive tasks for visuospatial and social cognition per operative mapping allow neurosurgeons to better appreciate the functional anatomy of the right hemisphere and its relevance to tumor surgery. In this article, the first of a 2-part review, we discuss the anatomic and functional basis of right hemisphere function. Whereas part II of the review focuses primarily on semiology and surgical management of right-sided tumors under awake conditions, this article provides a comprehensive review of knowledge underpinning awake surgery on the right hemisphere.