INSTRUMENTATION AND TECHNIQUE A Novel Intraoperative Brain Mapping Integrated Task-Presentation Platform N.U. Farrukh Hameed, MBBS, MCh ‡§∗ Zehao Zhao, MBBS ‡§∗ Jie Zhang, MD ‡§ Linghao Bu, MD ‡ Yuyao Zhou, MD ‡ Lei Jin, BSc ‡ Hongmin Bai, MD ¶ Weiping Li, MD || Jie Tang, MD # Junfeng Lu, MD ‡§ Jinsong Wu, MD, PhD ‡§ Ying Mao, MD, PhD ‡ ‡ Department of Neurological Surgery, Huashan Hospital, Fudan University, Shanghai, China; § Brain Function Laboratory, Neurosurgical Institute of Fudan University, Shanghai, China; ¶ General Hospital of Southern Theatre Command, Guangzhou, Guangdong Province, China; || The Shenzhen Second People’s Hospital, Shenzhen, Guangdong Province, China; # Shenzhen Sinorad Medical Electronics Co., Ltd, Shenzhen, Guangdong Province, China ∗ N.U. Farrukh Hameed and Zehao Zhao contributed equally to this work. Correspondence: Junfeng Lu, MD, Department of Neurosurgery, Huashan Hospital, Fudan University, Wulumuqi Middle Road 12#, Shanghai, 200040, China. Email: [email protected]Received, June 13, 2020. Accepted, November 11, 2020. C Congress of Neurological Surgeons 2021. All rights reserved. For permissions, please e-mail: [email protected]BACKGROUND: To be efficient, intraoperative task-presentation systems must accurately present various language and cognitive tasks to patients undergoing awake surgery, and record behavioral data without compromising convenience of surgery. OBJECTIVE: To present an integrated brain mapping task-presentation system we developed and evaluate its effectiveness in intraoperative task presentation. METHODS: The Brain Mapping Interactive Stimulation System (Brain MISS) is a flexible task presentation system that adjusts for patient comfort, needs of the surgeon, and operating team, with multivideo recording for patients’behavior. A total of 48 patients from 3 centers underwent intraoperative language task test during awake brain surgery with the Brain MISS. Each patient was assigned 5 questions each on picture naming, reading, and listening comprehension before and during awake surgeries. The accuracy of intraoper- ative stimulus-response (without electrical stimulation) was recorded. The Brain MISS was to be considered effective, if the lower limit of 95% CI of patients’ intraoperative response was ≥80% and also if the accuracy of intraoperative response of all patients was statistically higher than 80%. RESULTS: All patients successfully underwent intraoperative assessment with the Brain MISS. The overall accuracy of stimulus response was 95.8% (95% CI 90.18%-100.00%), with the lower limit being higher than 80% and the response accuracy also significantly being higher than 80% in all patients (P = .006). CONCLUSION: The Brain MISS is a portable and effective system for presenting and stream- lining complicated language and cognitive tasks during awake surgery. It can also record standardized patient response data for neuroscientific research. KEY WORDS: Awake craniotomy, Brain mapping, Task-presentation, Platform, Language mapping Operative Neurosurgery 0:1–7, 2021 DOI: 10.1093/ons/opaa476 B rain mapping is important for functional preservation during brain tumor, epilepsy, and functional surgeries. 1- 7 Contemporary brain mapping techniques rely on technology that stimulates different brain regions to identify and preserve eloquent regions during surgery. 5, 6, 8 Currently, direct cortical electrical stimulation (DCS) under awake anesthesia is used in combi- nation with different language or cognitive ABBREVIATIONS: Brain MISS, Brain Mapping Interactive Stimulation System; DCS, direct cortical electrical stimulation; KPS, Karnofsky Performance Status; LCD, liquid crystal display Supplemental digital content is available for this article at www.operativeneurosurgery-online.com. task tests to elicit anatomo-functional infor- mation. 5 , 9- 16 Task presentation during awake surgery and comprehensive recording of behavior has been a laborious undertaking since the start of this procedure over a century ago. 1 , 7 Despite their simplicity and ease of application, tradi- tional task-presentation methods such as the use of cards, laptops, or tablets remain incapable of adequately handling commonly encoun- tered challenges, which include communication between patient and surgeon, and tracking intra- operative task response over prolonged surgery duration (Figure 1). An advanced and standardized system of task- presentation and behavior recording is essential for complete functional evaluation to meet the requirements of increasingly complex intraoper- ative task-administration. Such a system must OPERATIVE NEUROSURGERY VOLUME 0 | NUMBER 0 | 2021 | 1 Downloaded from https://academic.oup.com/ons/advance-article/doi/10.1093/ons/opaa476/6129912 by guest on 07 February 2021
Transcript
INSTRUMENTATION AND TECHNIQUE
A Novel Intraoperative Brain Mapping IntegratedTask-Presentation Platform
BACKGROUND: To be efficient, intraoperative task-presentation systems must accuratelypresent various language and cognitive tasks to patients undergoing awake surgery, andrecord behavioral data without compromising convenience of surgery.OBJECTIVE: To present an integrated brain mapping task-presentation system wedeveloped and evaluate its effectiveness in intraoperative task presentation.METHODS: The Brain Mapping Interactive Stimulation System (Brain MISS) is a flexibletask presentation system that adjusts for patient comfort, needs of the surgeon, andoperating team,withmultivideo recording forpatients’behavior. A total of 48patients from3 centers underwent intraoperative language task test during awakebrain surgerywith theBrain MISS. Each patient was assigned 5 questions each on picture naming, reading, andlistening comprehension before and during awake surgeries. The accuracy of intraoper-ative stimulus-response (without electrical stimulation) was recorded. The Brain MISS wasto be considered effective, if the lower limit of 95% CI of patients’ intraoperative responsewas≥80%andalso if the accuracyof intraoperative responseof all patientswas statisticallyhigher than 80%.RESULTS: All patients successfully underwent intraoperative assessment with the BrainMISS. The overall accuracy of stimulus response was 95.8% (95% CI 90.18%-100.00%), withthe lower limit being higher than 80% and the response accuracy also significantly beinghigher than 80% in all patients (P = .006).CONCLUSION:TheBrainMISS is aportable andeffective system forpresentingand stream-lining complicated language and cognitive tasks during awake surgery. It can also recordstandardized patient response data for neuroscientific research.
KEYWORDS: Awake craniotomy, Brain mapping, Task-presentation, Platform, Language mapping
B rain mapping is important for functionalpreservation during brain tumor,epilepsy, and functional surgeries.1-7
Contemporary brain mapping techniques relyon technology that stimulates different brainregions to identify and preserve eloquent regionsduring surgery.5,6,8Currently, direct cortical electrical stimulation
(DCS) under awake anesthesia is used in combi-nation with different language or cognitive
Supplemental digital content is available for this article atwww.operativeneurosurgery-online.com.
task tests to elicit anatomo-functional infor-mation.5,9-16 Task presentation during awakesurgery and comprehensive recording of behaviorhas been a laborious undertaking since the startof this procedure over a century ago.1,7 Despitetheir simplicity and ease of application, tradi-tional task-presentation methods such as the useof cards, laptops, or tablets remain incapableof adequately handling commonly encoun-tered challenges, which include communicationbetween patient and surgeon, and tracking intra-operative task response over prolonged surgeryduration (Figure 1).An advanced and standardized system of task-
presentation and behavior recording is essentialfor complete functional evaluation to meet therequirements of increasingly complex intraoper-ative task-administration. Such a system must
FIGURE 1. The evolution of intraoperative task stimulation. Traditional task-presentation methods such as the use of cards, laptops, or tablets remainincapable of keeping up with the complex needs and advances in brain surgery and research.
also be capable of customizing tasks to patients and be equippedwith data storing capacity that can easily retrieve and share datafor reference and research purposes.The Brain Mapping Interactive Stimulation System (Brain
MISS) for awake craniotomy we designed here incorporates asimple, yet powerful, tablet user interface capable of presentingall conventional brain function assessment drills to patients. Inaddition to these, multiple hardware features have been carefullyincorporated into a single unit portable platform that can beconveniently used in restricted operation settings. We present thetechnical details of the system and demonstrate its clinical appli-cation in patients undergoing brain task stimulation in awakesurgery.
METHODS
Platform DescriptionThe Brain MISS has a flexible design that is easy to operate and
amenable to future upgrades. The design adjusts for patient comfort (size,positioning, and ease of usage), needs of the surgeon (easy interactionwith the patient and surgical team, real-time implementation of tasks,and transmission of patient responses), and the nursing team (mobility,limited size within the operating room, and minimal effort for setting upand tearing down the system) (Figure 2).
The system is comprised of controller interface, a patient interface,monitoring and display interfaces, and an application control softwarepackage. The controller terminal includes a user interface consisting ofa keyboard, a trackball, and a control display for the operator to controlthe system. Visual commands are relayed from the controller to patientinterface liquid crystal display (LCD) screen. The screen is mounted ona telescopic arm that can venture into narrow spaces during surgery suchas underneath surgical drapes, or to positions within patients’ limitedvisual scope due to head-fixation (Figure 3). Similarly, built-in speakerswithin the patient interface relay auditory task stimuli to patients. Otherinstalled components include an amplifying microphone to amplify andtransmit patients’ response to the surgeon via the monitoring interface,and a set of surveillance cameras to monitor patients’ face, hands, and feetmotion during surgery. These provide a reliable basis for the analysis and
judgment of intra- and postoperative function in awake brain surgery.The monitoring and display terminal are capable of transmitting 4separate video streams of patients’ responses. These streams, combinedwith patients’ response, are recorded for postoperative evaluation andfeedback.
A key feature of the BrainMISS is the accompanying software packagethat equips it with capabilities absent in previous brain stimulationsystems. The software interface consists of the following options: patientinformation, brain areas selection, stimulation tasks list, stimulationcontrol panel, and video recording and playback. Detailed patient infor-mation, including electrical stimulation parameters, can be entered andsaved by following the “patient information” option. The second andthird options on themain interface allow for the selection of tasks relevantto brain regions to be stimulated and a list of associated stimulatingtasks. The software also allows for the addition and deletion, as well asadjustment of the duration and execution order of these tasks (Figure 4).After customization of stimulation tasks for a patient, the stimulationcontrol panel (the fourth option) is used for the execution of the tasks inthe defined order. In addition to initiating and pausing stimulation, thiscontrol panel can be used to skip tasks or switch to the previous or nexttask. The “video recording and playback” function permits playback andsaving of stimulation data, including patient stimulation video streamsand audio responses, to a specified local directory. The system is easy tooperate and can be controlled by an operation room technician or nurse.
Tasks and Brain StimulationThe brain stimulation system is equipped with 11 commonly used
tasks, ranging from picture naming to working memory, to elicit acomplete functional picture of the brain. The picture naming task hasbeen standardized with a series of images selected from the NationalLibrary of Brain and Cognitive Sciences based on defined principleswhich include exclusion of vivid color, high contrast, and flashingimages.17 These images are sequentially displayed on the LCD screen atan interval of 4 s with a beep sound 0.5 s before the onset of each displayto signal the surgeon to stimulate (Figure 5). Other language assessmenttasks involve text reading, auditory comprehension, semantic associationand judgment, and writing tasks. In cases where a patient is significantlyimpaired, tasks are tailored based on their capacity by the surgeon.
2 | VOLUME 0 | NUMBER 0 | 2021 www.operativeneurosurgery-online.com
Dow
nloaded from https://academ
ic.oup.com/ons/advance-article/doi/10.1093/ons/opaa476/6129912 by guest on 07 February 2021
Clinical EvaluationWe performed a multicenter, clinical study to demonstrate the
intraoperative application of the Brain MISS for administering brainstimulation tests. The study protocol was approved by the hospital’sinstitutional review board and was conducted in accordance withthe Declaration of Helsinki. Informed consents were obtained fromall participants. The participants consented to publication of theirimages.
The study included patients with brain tumor scheduled to undergoawake brain surgery. All scheduled patients were required to have normalhearing, vision, and Boston Naming Test scores. Each participant wasassigned 15 test questions with 5 questions each on picture naming(5 pictures randomly displayed with word instructions requiring thepatients to respond), reading (5 words randomly displayed with wordinstructions requiring patients to read the words), and listening compre-hension (5 listening comprehension questions randomly played with
ic.oup.com/ons/advance-article/doi/10.1093/ons/opaa476/6129912 by guest on 07 February 2021
HAMEED ET AL
FIGURE 3. A, The Brain MISS easily integrates with the rest of the operation room layout. B, The patient interface arm easily adjusts for optimumplacement. C, The machine technician operates from the control terminal where all patient information is displayed and recorded. D, Surgeoninterface displays all parameters for easy monitoring and streamlines the awake mapping process.
notification sounds prompting patients to respond). Patients’ baselineresponses to the test questions were recorded prior to surgery.
During surgery, the patient completed eachmodule while the operatorjudged the effectiveness of each task according to the participants’responses before stimulation (stimulation was not applied to minimizeinterference). The primary endpoint of the study was the overall accuracyof task-response. Secondary endpoints were the accuracy of responseto the picture-naming, reading, and listening comprehension modulesduring the stimulation time for each task module. To measure the intra-operative accuracy, the intraoperative responses were compared to thepreoperative baseline response.
The sample size of the study was calculated with nQuery Advisorsoftware (www.statcon.de). TheWilson CIs method was used to estimatethe 95% CI of responses. The Fisher’s exact test was used for thecomparison of response accuracy. The Brain MISS was consideredeffective if the lower limit of 95% CI of patients’ intraoperative responsefeedback was ≥80% (target value determined from consultation withneurosurgeons) or the accuracy of intraoperative response of all patientswas higher than 80% signified by P-value < .05. Fisher exact proba-bility method is used for statistical inference and 95% CI is estimated byWilson score. All statistical analyses were performed with SAS StatisticalSoftware (www.sas.com).
RESULTS
From January 2015 to December 2019, the Brain MISS hasbeen successfully applied for intraoperative awake brain mapping
in 350 patients at our institution. To further evaluate the perfor-mance of the system, the Brain MISS was tested on a totalof 48 patients with an equal number recruited from 3 medicalcenters. No patient withdrew from the study or had any protocolviolation. The mean age of patients was 39.0 (11.3) and 26(54.1%) patients were male. Patients’ demographics are summa-rized in Table 1. All patients had normal vision, listening, cardiacfunction, and pulmonary function. One patient had mild hepaticand renal dysfunction. A total of 22 patients (43.1%) had ahistory of past medical conditions. The mean Karnofsky Perfor-mance Status (KPS) score was 94.9 (6.12): 28 (54.9%) patientsscored 100, 20 (39.2%) scored 90, and 3 (5.9%) scored 80. Allpatients had scores in the normal range for mini-mental stateexam and Boston Naming Test.
EndpointsThe overall accuracy of intraoperative stimulus response was
95.8% (95% CI 90.18% -100.00%), with the lower limit beinghigher than 80%. The response accuracy of all patients was alsosignificantly higher than 80% (P = .006).
The breakdown of the accuracy of intraoperative response is asfollows: for picture naming, the 95% CI is 93.88% to 100.00%with response accuracy (97.9%) of all patients significantly beinghigher than 80% (P = .002). For reading and listening compre-hension, the 95% CIs were 93.88% to 100.00% and 86.90% to
4 | VOLUME 0 | NUMBER 0 | 2021 www.operativeneurosurgery-online.com
Dow
nloaded from https://academ
ic.oup.com/ons/advance-article/doi/10.1093/ons/opaa476/6129912 by guest on 07 February 2021
FIGURE 4. Illustration of the software interface showing the patient information, regions of brain stimu-lation, and different stimulation tasks which can be selected based on surgical requirement.
100.00%, respectively, with response accuracy (97.9, 93.8%) ofall patients being significantly higher than 80% for both reading(P= .002) and listening (P= .017) (Table 2 and SupplementaryDigital Content 1-3).
Illustrative CaseTo highlight the practical use of the Brain MISS in the context
of surgical decision-making, a case is described below.The case is of a 28-yr-old right-handed male who presented
with 2-mo history of seizures. Physical examination was normal,and the patient had intact sensation and motor function on bothsides. Cognitive assessment tests were unremarkable with normalresults on mini-mental state examination (score of 27), KPS scoreof 100, Boston Naming Test (score of 25), and Aphasia Batteryof Chinese with an aphasia quotient of 96.9 (above normal cut-off ). Magnetic resonance imaging revealed a left frontal lobetumor which was resected under awake craniotomy. Monitoredanesthesia care was adopted for the patient. Following awakecraniotomy under nerve blockade combined with intravenousanesthesia, intraoperative mapping was started with numbercounting as described previously using the Brain MISS. DCS wasused to establish functional cortical areas that were marked on thebrain with sterile tags. The detailed description of the case andsurgery has been presented in the Video, Supplemental DigitalContent 4. The complete clinical trial protocol is presented inSupplementary Digital Content 5.
DISCUSSION
Efficient brain mapping facilitates the identification ofeloquent brain regions to elicit complete information on languageand motor deficits.3,18 In this study, we introduced the novelBrain MISS and demonstrated its application in the clinicalsetting. Using this platform, all patients successfully underwentintraoperative task presentation with very high accuracy duringpicture naming, reading, and listening comprehension tasks.Over the years, during awake craniotomy, picture naming tasks
have been presented to patients on cards, laptops, and eventuallyby tablet computers.1,3,5,6,8,19 This has posed significant diffi-culties for surgeons in tracking tasks intraoperatively and forcedthem to rely on technicians as intermediaries to present thesedata to patients for prolonged operative durations. The BrainMISS described in this report offers multiple tasks that expandon the functionality of traditional brain stimulation systems.20,21Furthermore, the platform can also be used for other clinicalprocedures such as electrode placement for deep brain stimu-lation and epilepsy. The simple stimulation software permitssurgeons and other health-care providers, such as neurophysiolo-gists, to independently tailor stimulation to every patient’s uniquesituation. The same tasks can be administered to patients duringpreoperative patient evaluation and intraoperatively. Patients are,therefore, acquainted with the testing platform intraoperatively,relieving anxiety and allowing for more accurate testing results.By keeping a record of patients’ stimulation responses, the system
ic.oup.com/ons/advance-article/doi/10.1093/ons/opaa476/6129912 by guest on 07 February 2021
HAMEED ET AL
FIGURE 5. Illustration of the stimulation protocol for a picture-naming task. The surgeon is prompted by a beep0.5 s before the appearance of each picture to apply cortical stimulation. This standardizes the stimulation processand streamlines the mapping process.
TABLE 1. Summary of Patient Characteristics
Items Overall
Male 26 (54.2%)Age (years), mean [SD] 38.97 ± 11.27Weight (kg), mean [SD] 63.50 ± 14.21Height (cm), mean [SD] 165.84 ± 9.32Normal vision 48 (100.0%)Normal hearing 48 (100.0%)KPS score 94.90 ± 6.12Mini-mental state exam (≥ 28/30) 48 (100%)Boston Naming Test (≥ 25/30) 48 (100%)Past medical conditions∗ 22 (43.1%)Glioma diagnosis 32 (66.67%)Intraoperative/postoperative complications 0 (0%)
SD: standard deviation. ∗ Including comorbidities and previous surgeries.
also facilitates comparison of patient performances for intraoper-ative decision-making, and also during postoperative follow-up tomonitor recovery.The assessment of stimulus response is crucial to the design of
any stimulation system. The Brain MISS demonstrated a >97%accuracy for stimulus response. This value can serve as a parameterto measure how effective the system is in presenting tasks to apatient during awake surgery. Considering the short durationof anesthesia-controlled lucid interval during which all brainmapping is done, an effective system can save time and energyof the entire team and the patient, benefitting the entire surgicalprocess.
During stimulation, intraoperative neurophysiologicalmonitoring waveform, a continuous video stream of patients’face, hands, and feet to the surgeon’s interface enables real-timemonitoring of patients’ facial and muscular activity during motortask mapping. These eliminate the need for an intermediaryto relay patient status to a surgeon. The entire surgical team,through multiple LCD screens, can directly visualize the effectsof DCS and other interventions. This permits close follow-up of the entire process and minimizes risks of omission andrepetitions.Hardware features have been incorporated into the Brain
MISS without compromising size and mobility while factoringin the tight confines of an operating room. The Brain MISShas proven to be extremely portable and labor-saving. Thesystem is also equipped with a storage capacity to store data oneach patient’s stimulation results. These data can be queried forshared decision-making. A standardized approach to record datameans that patient data across different hospitals and locationscan be pooled for larger comprehensive analyses and clinicalresearch.
CONCLUSION
The application of the Brain MISS task presentation system iseffective in the real hospital setting with favorable presentationresults. Its portability and accuracy render it as an intraoperativetask presentation platform which can facilitate the work of neuro-surgeons, surgical technicians, and patients during awake surgery.In addition to this, it can also provide valuable complete recordsfor neuroscience research.
6 | VOLUME 0 | NUMBER 0 | 2021 www.operativeneurosurgery-online.com
Dow
nloaded from https://academ
ic.oup.com/ons/advance-article/doi/10.1093/ons/opaa476/6129912 by guest on 07 February 2021
INTEGRATED INTRAOPERATIVE BRAIN MAPPING PLATFORM
TABLE 2. Efficiency of Stimulation Recognition of the Brain Stimulation System
Efficiency was defined as the proportion of patients that correctly recognized stimulations and gave feedback. A correlation of ≥80% between intra- and preoperative feedbackwas considered efficient, which meant lower limit of the 2-sided 95% CI (97.5% 1-sided CI) ≥80%.
FundingThis work was supported by grants from: Shanghai Municipal Science
and Technology Major Project (No. 2018SHZDZX01), Shanghai Rising-Star Program (No. 19QA1401700), Shanghai Young Talents Program(No. 2017YQ014), Shanghai Shenkang Hospital Development Center (No.SHDC12018114), and National Natural Science Foundation of China (No.81701289).
DisclosuresJunfeng Lu, Jinsong Wu, and Jie Tang designed the Brain Mapping Interactive
Stimulation System.
REFERENCES1. Penfield W, Roberts L. Speech and Brain Mechanisms. New Jersey, USA: Princeton
University Press; 2014.2. Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in
left, dominant hemisphere. An electrical stimulation mapping investigation in 117patients. J Neurosurg. 1989;71(3):316-326.
3. Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping forglioma resection. N Engl J Med. 2008;358(1):18-27.
4. Breshears JD, Molinaro AM, Chang EF. A probabilistic map of the human ventralsensorimotor cortex using electrical stimulation. J Neurosurg. 2015;123(2):340-349.
5. Wu J, Lu J, Zhang H, et al. Direct evidence from intraoperative electrocor-tical stimulation indicates shared and distinct speech production center betweenChinese and English languages. Hum Brain Mapp. 2015;36(12):4972-4985.
6. Chang EF, Breshears JD, Raygor KP, Lau D, Molinaro AM, Berger MS.Stereotactic probability and variability of speech arrest and anomia sites duringstimulation mapping of the language dominant hemisphere. J Neurosurg.2017;126(1):114-121.
7. Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebralcortex of man as studied by electrical stimulation. Brain. 1937;60(4):389-443.
8. Sarubbo S, TateM, De Benedictis A, et al. Mapping critical cortical hubs and whitematter pathways by direct electrical stimulation: an original functional atlas of thehuman brain. Neuroimage. 2020;205(1):116237.
9. Benzagmout M, Gatignol P, Duffau H. Resection of World Health Organizationgrade II gliomas involving Broca’s area: methodological and functional considera-tions. Neurosurgery. 2007;61(4):741-753; discussion 752-743.
10. De Benedictis A, Moritz-Gasser S, Duffau H. Awake mapping optimizes theextent of resection for low-grade gliomas in eloquent areas. Neurosurgery.2010;66(6):1074-1084; discussion 1084.
11. Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L. Intraoper-ative subcortical stimulation mapping of language pathways in a consecutive seriesof 115 patients with grade II glioma in the left dominant hemisphere. J Neurosurg.2008;109(3):461-471.
12. Grundy PL, Weidmann C, Bernstein M. Day-case neurosurgery for braintumours: the early United Kingdom experience. Br J Neurosurg. 2008;22(3):360-367.
13. Gupta DK, Chandra PS, Ojha BK, Sharma BS, Mahapatra AK, Mehta VS.Awake craniotomy versus surgery under general anesthesia for resection of intrinsiclesions of eloquent cortex–a prospective randomised study. Clin Neurol Neurosurg.2007;109(4):335-343.
14. Parney IF, Goerss SJ, McGee K, Huston J 3rd, Perkins WJ, Meyer FB. Awakecraniotomy, electrophysiologic mapping, and tumor resection with high-field intra-operative MRI. World Neurosurg. 2010;73(5):547-551.
15. Rofes A, Miceli G. Language mapping with verbs and sentences in awake surgery:a review. Neuropsychol Rev. 2014;24(2):185-199.
16. Talacchi A, Santini B, Savazzi S, GerosaM. Cognitive effects of tumour and surgicaltreatment in glioma patients. J Neurooncol. 2011;103(3):541-549.
17. Snodgrass JG, Vanderwart M. A standardized set of 260 pictures: norms for nameagreement, image agreement, familiarity, and visual complexity. J Exp Psychol HumLearn. 1980;6(2):174-215.
18. De Witte E, Marien P. The neurolinguistic approach to awake surgery reviewed.Clin Neurol Neurosurg. 2013;115(2):127-145.
19. Tate MC, Herbet G, Moritz-Gasser S, Tate JE, Duffau H. Probabilistic map ofcritical functional regions of the human cerebral cortex: Broca’s area revisited.Brain.2014;137(10):2773-2782.
20. Morrison MA, Tam F, Garavaglia MM, et al. A novel tablet computer platform foradvanced language mapping during awake craniotomy procedures. J Neurosurg.2016;124(4):938-944.
21. Yoshimitsu K, Suzuki T, Muragaki Y, Chernov M, Iseki H. Development ofmodified intraoperative examination monitor for awake surgery (IEMAS) systemfor awake craniotomy during brain tumor resection. Proceedings of the Annual Inter-national Conference of the IEEE Engineering in Medicine and Biology Society. BuenosAires, Argentina: IEEE; 2010;6050-6053.
Supplemental digital content is available for this article at www.operativeneurosurgery-online.com.
