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CC BY 4.0 · J Neuroanaesth Crit Care 2023; 10(02): 077-086
DOI: 10.1055/s-0043-1777444
Review Article

Intraoperative Stimulation Mapping in Neurosurgery for Anesthesiologists—Part 1: The Technical Nuances

Naeema S. Masohood 
1   Department of Anesthesiology and Pain Medicine, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada
,
Gabriel Paquin-Lanthier
1   Department of Anesthesiology and Pain Medicine, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada
,
Jason Chui
2   Department of Anesthesia & Perioperative Medicine, Schulich School of Medicine and Dentistry, Western University, London, Ontario, Canada
,
Nancy Lu
3   Division of Perioperative Surgical Services, Department of Neurosurgical Intraoperative Monitoring, Toronto Western Hospital, University Health Network, Toronto, Canada
,
Tumul Chowdhury
1   Department of Anesthesiology and Pain Medicine, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada
,
Lashmi Venkatraghavan
1   Department of Anesthesiology and Pain Medicine, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada
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Abstract

Brain mapping has evolved tremendously in the past decade, fueled by advances in functional neuroimaging technology in neuro-oncology and epilepsy surgery. Despite this, wide anatomic-functional interindividual variability and intraoperative brain shift continue to challenge neurosurgeons performing surgery within or near eloquent brain regions. As such, intraoperative direct cortical and subcortical stimulation mapping remains the gold standard for localizing eloquent brain regions with precision for a safe and tailored resection. Intraoperative stimulation mapping (ISM) allows for maximizing the extent of resection while minimizing postoperative neurological deficits, resulting in better patient outcomes. Understanding the technical nuances of ISM is imperative for the anesthesiologist to provide better anesthetic management tailored to the surgery and stimulation mapping planned. A comprehensive search was performed on electronic databases to identify articles describing intraoperative cortical and subcortical mapping, language, and motor mapping. In the first part of this narrative review, we summarize the salient technical aspects of ISM and the common neurophysiological tasks assessed intraoperatively relevant to the anesthesiologist.

Keywords

direct electrical stimulation - intraoperative stimulation mapping - awake craniotomy - language mapping - motor mapping


Publication History

Article published online:
23 February 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Duffau H. Diffuse low-grade glioma, oncological outcome and quality of life: a surgical perspective. Curr Opin Oncol 2018; 30 (06) 383-389
    CrossrefPubMedGoogle Scholar
  • 2 Edelvik A, Taft C, Ekstedt G, Malmgren K. Health-related quality of life and emotional well-being after epilepsy surgery: a prospective, controlled, long-term follow-up. Epilepsia 2017; 58 (10) 1706-1715
    CrossrefPubMedGoogle Scholar
  • 3 Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989; 71 (03) 316-326
    CrossrefPubMedGoogle Scholar
  • 4 Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L. New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 2005; 128 (Pt 4): 797-810
    CrossrefPubMedGoogle Scholar
  • 5 Duffau H. A two-level model of interindividual anatomo-functional variability of the brain and its implications for neurosurgery. Cortex 2017; 86: 303-313
    CrossrefPubMedGoogle Scholar
  • 6 Borchers S, Himmelbach M, Logothetis N, Karnath HO. Direct electrical stimulation of human cortex - the gold standard for mapping brain functions?. Nat Rev Neurosci 2011; 13 (01) 63-70
    CrossrefPubMedGoogle Scholar
  • 7 Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937; 60 (04) 389-443
    CrossrefPubMedGoogle Scholar
  • 8 Ojemann GA, Whitaker HA. Language localization and variability. Brain Lang 1978; 6 (02) 239-260
    CrossrefPubMedGoogle Scholar
  • 9 Taniguchi M, Cedzich C, Schramm J. Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 1993; 32 (02) 219-226
    CrossrefPubMedGoogle Scholar
  • 10 Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional cortex and subcortical white matter located within gliomas. Neurosurgery 1996; 38 (04) 678-684 , discussion 684–685
    CrossrefPubMedGoogle Scholar
  • 11 Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS. Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 2004; 100 (03) 369-375
    CrossrefPubMedGoogle Scholar
  • 12 Bello L, Gallucci M, Fava M. et al. Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery 2007; 60 (01) 67-80 , discussion 80–82
    CrossrefPubMedGoogle Scholar
  • 13 Yamaguchi F, Takahashi H, Teramoto A. Navigation-assisted subcortical mapping: intraoperative motor tract detection by bipolar needle electrode in combination with neuronavigation system. J Neurooncol 2009; 93 (01) 121-125
    CrossrefPubMedGoogle Scholar
  • 14 Bello L, Castellano A, Fava E. et al. Intraoperative use of diffusion tensor imaging fiber tractography and subcortical mapping for resection of gliomas: technical considerations. Neurosurg Focus 2010; 28 (02) E6
    CrossrefPubMedGoogle Scholar
  • 15 Duffau H. Stimulation mapping of myelinated tracts in awake patients. Brain Plast 2016; 2 (01) 99-113
    CrossrefPubMedGoogle Scholar
  • 16 Ortiz KJ, Hawayek MI, Middlebrooks EH. et al. Intraoperative direct stimulation identification and preservation of critical white matter tracts during brain surgery. World Neurosurg 2021; 146: 64-74
    CrossrefPubMedGoogle Scholar
  • 17 Duffau H, Capelle L, Sichez N. et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 2002; 125 (Pt 1): 199-214
    CrossrefPubMedGoogle Scholar
  • 18 Duffau H, Capelle L, Denvil D. et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 2003; 98 (04) 764-778
    CrossrefPubMedGoogle Scholar
  • 19 Mandonnet E, Winkler PA, Duffau H. Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir (Wien) 2010; 152 (02) 185-193
    CrossrefPubMedGoogle Scholar
  • 20 Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp Brain Res 1998; 118 (04) 477-488
    CrossrefPubMedGoogle Scholar
  • 21 Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res 1998; 118 (04) 489-500
    CrossrefPubMedGoogle Scholar
  • 22 Logothetis NK, Kayser C, Oeltermann A. In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron 2007; 55 (05) 809-823
    CrossrefPubMedGoogle Scholar
  • 23 Tehovnik EJ, Tolias AS, Sultan F, Slocum WM, Logothetis NK. Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 2006; 96 (02) 512-521
    CrossrefPubMedGoogle Scholar
  • 24 Tolias AS, Sultan F, Augath M. et al. Mapping cortical activity elicited with electrical microstimulation using FMRI in the macaque. Neuron 2005; 48 (06) 901-911
    CrossrefPubMedGoogle Scholar
  • 25 Logothetis NK, Augath M, Murayama Y. et al. The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 2010; 13 (10) 1283-1291
    CrossrefPubMedGoogle Scholar
  • 26 Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 1999; 89 (02) 335-346
    CrossrefPubMedGoogle Scholar
  • 27 Yingling CD. Cortical mapping. In: Koht A, Sloan TB, Toleikis JR. eds. Monitoring the Nervous System for Anesthesiologists and Other Health Care Professionals. Switzerland: Springer; 2012: 165-180
    Google Scholar
  • 28 Al-Adli NN, Young JS, Sibih YE, Berger MS. Technical aspects of motor and language mapping in glioma patients. Cancers (Basel) 2023; 15 (07) 2173
    CrossrefPubMedGoogle Scholar
  • 29 Rossi M, Sciortino T, Conti Nibali M. et al. Clinical pearls and methods for intraoperative motor mapping. Neurosurgery 2021; 88 (03) 457-467
    CrossrefPubMedGoogle Scholar
  • 30 Morshed RA, Young JS, Lee AT, Berger MS, Hervey-Jumper SL. Clinical pearls and methods for intraoperative awake language mapping. Neurosurgery 2021; 89 (02) 143-153
    CrossrefPubMedGoogle Scholar
  • 31 Bello L, Riva M, Fava E. et al. Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways. Neuro-oncol 2014; 16 (08) 1110-1128
    CrossrefPubMedGoogle Scholar
  • 32 Nathan SS, Sinha SR, Gordon B, Lesser RP, Thakor NV. Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalogr Clin Neurophysiol 1993; 86 (03) 183-192
    CrossrefPubMedGoogle Scholar
  • 33 Schucht P, Seidel K, Jilch A, Beck J, Raabe A. A review of monopolar motor mapping and a comprehensive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Review Neurochirurgie 2017; 63 (03) 175-180
    CrossrefPubMedGoogle Scholar
  • 34 Moiyadi A, Velayutham P, Shetty P. et al. Combined motor evoked potential monitoring and subcortical dynamic mapping in motor eloquent tumors allows safer and extended resections. World Neurosurg 2018; 120: e259-e268
    CrossrefPubMedGoogle Scholar
  • 35 Axelson HW, Latini F, Jemstedt M, Ryttlefors M, Zetterling M. Continuous subcortical language mapping in awake glioma surgery. Front Oncol 2022; 12: 947119
    CrossrefPubMedGoogle Scholar
  • 36 Pouratian N, Cannestra AF, Bookheimer SY, Martin NA, Toga AW. Variability of intraoperative electrocortical stimulation mapping parameters across and within individuals. J Neurosurg 2004; 101 (03) 458-466
    CrossrefPubMedGoogle Scholar
  • 37 Taylor MD, Bernstein M. Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. J Neurosurg 1999; 90 (01) 35-41
    CrossrefPubMedGoogle Scholar
  • 38 Hervey-Jumper SL, Li J, Lau D. et al. Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 2015; 123 (02) 325-339
    CrossrefPubMedGoogle Scholar
  • 39 Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008; 358 (01) 18-27
    CrossrefPubMedGoogle Scholar
  • 40 Kim SS, McCutcheon IE, Suki D. et al. Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 2009; 64 (05) 836-845 , discussion 345–346
    CrossrefPubMedGoogle Scholar
  • 41 Vakani R, Nair DR. Electrocorticography and functional mapping. Handb Clin Neurol 2019; 160: 313-327
    CrossrefPubMedGoogle Scholar
  • 42 Aydinlar EI, Dikmen PY, Kocak M, Sahillioğlu E, Pamir MN. Intraoperative motor speech mapping under general anesthesia using long-latency response from laryngeal muscles. Clin Neurol Neurosurg 2020; 190: 105672
    CrossrefPubMedGoogle Scholar
  • 43 Kim KM, Kim SM, Kang H. et al. Preservation of language function by mapping the arcuate fasciculus using intraoperative corticocortical evoked potential under general anesthesia in glioma surgery. J Neurosurg 2022; 18: 1-9
    PubMedGoogle Scholar
  • 44 De Witte E, Satoer D, Colle H, Robert E, Visch-Brink E, Mariën P. Subcortical language and non-language mapping in awake brain surgery: the use of multimodal tests. Acta Neurochir (Wien) 2015; 157 (04) 577-588
    CrossrefPubMedGoogle Scholar
  • 45 Papatzalas C, Fountas K, Kapsalaki E, Papathanasiou I. The use of standardized intraoperative language tests in awake craniotomies: a scoping review. Neuropsychol Rev 2022; 32 (01) 20-50
    CrossrefPubMedGoogle Scholar
  • 46 De Witte E, Satoer D, Robert E. et al. The Dutch Linguistic Intraoperative Protocol: a valid linguistic approach to awake brain surgery. Brain Lang 2015; 140: 35-48
    CrossrefPubMedGoogle Scholar
  • 47 Bilotta F, Stazi E, Titi L. et al. Diagnostic work up for language testing in patients undergoing awake craniotomy for brain lesions in language areas. Br J Neurosurg 2014; 28 (03) 363-367
    CrossrefPubMedGoogle Scholar
  • 48 Pascual JSG, Khu KJO, Starreveld YP. Cortical mapping in multilinguals undergoing awake brain surgery for brain tumors: illustrative cases and systematic review. Neuropsychologia 2023; 179: 108450
    CrossrefPubMedGoogle Scholar
  • 49 Gisbert-Muñoz S, Quiñones I, Amoruso L. et al. MULTIMAP: multilingual picture naming test for mapping eloquent areas during awake surgeries. Behav Res Methods 2021; 53 (02) 918-927
    CrossrefPubMedGoogle Scholar
  • 50 Ruis C. Monitoring cognition during awake brain surgery in adults: a systematic review. J Clin Exp Neuropsychol 2018; 40 (10) 1081-1104
    CrossrefPubMedGoogle Scholar
  • 51 Bu L, Lu J, Zhang J, Wu J. Intraoperative cognitive mapping tasks for direct electrical stimulation in clinical and neuroscientific contexts. Front Hum Neurosci 2021; 15: 612891
    CrossrefPubMedGoogle Scholar
  • 52 Rossi M, Nibali MC, Torregrossa F, Bello L, Grasso G. Innovation in neurosurgery: the concept of cognitive mapping. World Neurosurg 2019; 131: 364-370
    CrossrefPubMedGoogle Scholar
  • 53 Riva M, Fava E, Gallucci M. et al. Monopolar high-frequency language mapping: can it help in the surgical management of gliomas? A comparative clinical study. J Neurosurg 2016; 124 (05) 1479-1489
    CrossrefPubMedGoogle Scholar
  • 54 Verst SM, de Aguiar PHP, Joaquim MAS, Vieira VG, Sucena ABC, Maldaun MVC. Monopolar 250-500 Hz language mapping: Results of 41 patients. Clin Neurophysiol Pract 2018; 4: 1-8
    PubMedGoogle Scholar
  • 55 Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 2008; 109 (03) 461-471
    CrossrefPubMedGoogle Scholar
  • 56 Nossek E, Korn A, Shahar T. et al. Intraoperative mapping and monitoring of the corticospinal tracts with neurophysiological assessment and 3-dimensional ultrasonography-based navigation. Clinical article. J Neurosurg 2011; 114 (03) 738-746
    CrossrefPubMedGoogle Scholar
  • 57 Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A. The warning-sign hierarchy between quantitative subcortical motor mapping and continuous motor evoked potential monitoring during resection of supratentorial brain tumors. J Neurosurg 2013; 118 (02) 287-296
    CrossrefPubMedGoogle Scholar
  • 58 Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg 2014; 120 (05) 1015-1024
    CrossrefPubMedGoogle Scholar
  • 59 Shiban E, Krieg SM, Haller B. et al. Intraoperative subcortical motor evoked potential stimulation: how close is the corticospinal tract?. J Neurosurg 2015; 123 (03) 711-720
    CrossrefPubMedGoogle Scholar
  • 60 Eseonu CI, Rincon-Torroella J, ReFaey K. et al. Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: evaluating perioperative complications and extent of resection. Neurosurgery 2017; 81 (03) 481-489
    CrossrefPubMedGoogle Scholar
  • 61 Han SJ, Morshed RA, Troncon I. et al. Subcortical stimulation mapping of descending motor pathways for perirolandic gliomas: assessment of morbidity and functional outcome in 702 cases. J Neurosurg 2018; 131 (01) 201-208
    CrossrefPubMedGoogle Scholar
  • 62 Plans G, Fernández-Conejero I, Rifà-Ros X, Fernández-Coello A, Rosselló A, Gabarrós A. Evaluation of the high-frequency monopolar stimulation technique for mapping and monitoring the corticospinal tract in patients with supratentorial gliomas. a proposal for intraoperative management based on neurophysiological data analysis in a series of 92 patients. Neurosurgery 2017; 81 (04) 585-594
    CrossrefPubMedGoogle Scholar
  • 63 Carrabba G, Fava E, Giussani C. et al. Cortical and subcortical motor mapping in Rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 2007; 51 (02) 45-51
    PubMedGoogle Scholar
  • 64 Fornia L, Rossi M, Rabuffetti M. et al. Direct electrical stimulation of premotor areas: different effects on hand muscle activity during object manipulation. Cereb Cortex 2020; 30 (01) 391-405
    CrossrefPubMedGoogle Scholar
  • 65 Chen X, Scangos KW, Stuphorn V. Supplementary motor area exerts proactive and reactive control of arm movements. J Neurosci 2010; 30 (44) 14657-14675
    CrossrefPubMedGoogle Scholar
  • 66 Yingling CD, Ojemann S, Dodson B, Harrington MJ, Berger MS. Identification of motor pathways during tumor surgery facilitated by multichannel electromyographic recording. J Neurosurg 1999; 91 (06) 922-927
    CrossrefPubMedGoogle Scholar
  • 67 Kombos T, Suess O, Ciklatekerlio O, Brock M. Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg 2001; 95 (04) 608-614
    CrossrefPubMedGoogle Scholar
  • 68 Kombos T, Suess O, Kern BC. et al. Comparison between monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir (Wien) 1999; 141 (12) 1295-1301
    CrossrefPubMedGoogle Scholar
  • 69 Szelényi A, Bello L, Duffau H. et al; Workgroup for Intraoperative Management in Low-Grade Glioma Surgery within the European Low-Grade Glioma Network. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010; 28 (02) E7
    CrossrefPubMedGoogle Scholar
  • 70 Szelényi A, Senft C, Jardan M. et al. Intra-operative subcortical electrical stimulation: a comparison of two methods. Clin Neurophysiol 2011; 122 (07) 1470-1475
    CrossrefPubMedGoogle Scholar
  • 71 Tate MC, Guo L, McEvoy J, Chang EF. Safety and efficacy of motor mapping utilizing short pulse train direct cortical stimulation. Stereotact Funct Neurosurg 2013; 91 (06) 379-385
    CrossrefPubMedGoogle Scholar
  • 72 Szelényi A, Joksimovic B, Seifert V. Intraoperative risk of seizures associated with transient direct cortical stimulation in patients with symptomatic epilepsy. J Clin Neurophysiol 2007; 24 (01) 39-43
    CrossrefPubMedGoogle Scholar
  • 73 Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A. Low-threshold monopolar motor mapping for resection of primary motor cortex tumors. Neurosurgery 2012; 71 (1, suppl Operative): 104-114 , discussion 114–115
    PubMedGoogle Scholar
  • 74 Gogos AJ, Young JS, Morshed RA. et al. Triple motor mapping: transcranial, bipolar, and monopolar mapping for supratentorial glioma resection adjacent to motor pathways. J Neurosurg 2020; 134 (06) 1728-1737
    CrossrefPubMedGoogle Scholar
  • 75 Viganò L, Callipo V, Lamperti M. et al. Transcranial versus direct electrical stimulation for intraoperative motor-evoked potential monitoring: prognostic value comparison in asleep brain tumor surgery. Front Oncol 2022; 12: 963669
    CrossrefPubMedGoogle Scholar
  • 76 Silverstein JW, Shah HA, Unadkat P. et al. Short and long-term prognostic value of intraoperative motor evoked potentials in brain tumor patients: a case series of 121 brain tumor patients. J Neurooncol 2023; 161 (01) 127-133
    CrossrefPubMedGoogle Scholar
  • 77 Wood CC, Spencer DD, Allison T, McCarthy G, Williamson PD, Goff WR. Localization of human sensorimotor cortex during surgery by cortical surface recording of somatosensory evoked potentials. J Neurosurg 1988; 68 (01) 99-111
    CrossrefPubMedGoogle Scholar
  • 78 Cedzich C, Taniguchi M, Schäfer S, Schramm J. Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. Neurosurgery 1996; 38 (05) 962-970
    CrossrefPubMedGoogle Scholar
  • 79 Kurian J, Pernik MN, Traylor JI, Hicks WH, El Shami M, Abdullah KG. Neurological outcomes following awake and asleep craniotomies with motor mapping for eloquent tumor resection. Clin Neurol Neurosurg 2022; 213: 107128
    CrossrefPubMedGoogle Scholar
  • 80 Murcia D, D'Souza S, Abozeid M, Thompson JA, Djoyum TD, Ormond DR. Investigation of asleep versus awake motor mapping in resective brain surgery. World Neurosurg 2022; 157: e129-e136
    CrossrefPubMedGoogle Scholar
  • 81 Rossi M, Fornia L, Puglisi G. et al. Assessment of the praxis circuit in glioma surgery to reduce the incidence of postoperative and long-term apraxia: a new intraoperative test. J Neurosurg 2018; 130 (01) 17-27
    CrossrefPubMedGoogle Scholar
  • 82 Desmurget M, Richard N, Beuriat PA. et al. Selective inhibition of volitional hand movements after stimulation of the dorsoposterior parietal cortex in humans. Curr Biol 2018; 28 (20) 3303-3309.e3
    CrossrefPubMedGoogle Scholar
  • 83 Almairac F, Herbet G, Moritz-Gasser S, Duffau H. Parietal network underlying movement control: disturbances during subcortical electrostimulation. Neurosurg Rev 2014; 37 (03) 513-516 , discussion 516–517
    CrossrefPubMedGoogle Scholar
  • 84 Viganò L, Fornia L, Rossi M. et al. Anatomo-functional characterisation of the human “hand-knob”: a direct electrophysiological study. Cortex 2019; 113: 239-254
    CrossrefPubMedGoogle Scholar
  • 85 Schebesch KM, Rosengarth K, Brawanski A. et al. Clinical benefits of combining different visualization modalities in neurosurgery. Front Surg 2019; 6: 56
    CrossrefPubMedGoogle Scholar
  • 86 Peck KK, Bradbury M, Petrovich N. et al. Presurgical evaluation of language using functional magnetic resonance imaging in brain tumor patients with previous surgery. Neurosurgery 2009; 64 (04) 644-652 , discussion 652–653
    CrossrefPubMedGoogle Scholar
  • 87 Krings T, Schreckenberger M, Rohde V. et al. Metabolic and electrophysiological validation of functional MRI. J Neurol Neurosurg Psychiatry 2001; 71 (06) 762-771
    CrossrefPubMedGoogle Scholar
  • 88 Vassal F, Schneider F, Nuti C. Intraoperative use of diffusion tensor imaging-based tractography for resection of gliomas located near the pyramidal tract: comparison with subcortical stimulation mapping and contribution to surgical outcomes. Br J Neurosurg 2013; 27 (05) 668-675
    CrossrefPubMedGoogle Scholar
  • 89 Krieg SM, Picht T, Sollmann N. et al. Resection of motor eloquent metastases aided by preoperative nTMS-based motor maps-comparison of two observational cohorts. Front Oncol 2016; 6: 261
    CrossrefPubMedGoogle Scholar
  • 90 Assaf BA, Karkar KM, Laxer KD. et al. Magnetoencephalography source localization and surgical outcome in temporal lobe epilepsy. Clin Neurophysiol 2004; 115 (09) 2066-2076
    CrossrefPubMedGoogle Scholar
  • 91 Kreidenhuber R, De Tiège X, Rampp S. Presurgical functional cortical mapping using electromagnetic source imaging. Front Neurol 2019; 10: 628
    CrossrefPubMedGoogle Scholar
  • 92 Nakamura A, Yamada T, Goto A. et al. Somatosensory homunculus as drawn by MEG. Neuroimage 1998; 7 (4 Pt 1): 377-386
    CrossrefPubMedGoogle Scholar
  • 93 Zlatkina V, Amiez C, Petrides M. The postcentral sulcal complex and the transverse postcentral sulcus and their relation to sensorimotor functional organization. Eur J Neurosci 2016; 43 (10) 1268-1283
    CrossrefPubMedGoogle Scholar
  • 94 Li Q, Dong JW, Del Ferraro G. et al. Functional translocation of Broca's area in a low-grade left frontal glioma: graph theory reveals the novel, adaptive network connectivity. Front Neurol 2019; 10: 702
    CrossrefPubMedGoogle Scholar
  • 95 Pouratian N, Bookheimer SY. The reliability of neuroanatomy as a predictor of eloquence: a review. Neurosurg Focus 2010; 28 (02) E3
    CrossrefPubMedGoogle Scholar
  • 96 Hamberger MJ, Cole J. Language organization and reorganization in epilepsy. Neuropsychol Rev 2011; 21 (03) 240-251
    CrossrefPubMedGoogle Scholar
  • 97 Gerard IJ, Kersten-Oertel M, Hall JA, Sirhan D, Collins DL. Brain shift in neuronavigation of brain tumors: an updated review of intra-operative ultrasound applications. Front Oncol 2021; 10: 618837
    CrossrefPubMedGoogle Scholar
  • 98 Thiel A, Herholz K, Koyuncu A. et al. Plasticity of language networks in patients with brain tumors: a positron emission tomography activation study. Ann Neurol 2001; 50 (05) 620-629
    CrossrefPubMedGoogle Scholar
  • 99 Ille S, Engel L, Albers L. et al. Functional reorganization of cortical language function in glioma patients-a preliminary study. Front Oncol 2019; 9: 446
    CrossrefPubMedGoogle Scholar
  • 100 Fang S, Zhou C, Wang Y, Jiang T. Contralesional functional network reorganization of the insular cortex in diffuse low-grade glioma patients. Sci Rep 2021; 11 (01) 623
    CrossrefPubMedGoogle Scholar
  • 101 Lv K, Cao X, Wang R. et al. Neuroplasticity of glioma patients: brain structure and topological network. Front Neurol 2022; 13: 871613
    CrossrefPubMedGoogle Scholar
  • 102 Southwell DG, Hervey-Jumper SL, Perry DW, Berger MS. Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex. J Neurosurg 2016; 124 (05) 1460-1469
    CrossrefPubMedGoogle Scholar
  • 103 Spena G, Nava A, Cassini F. et al. Preoperative and intraoperative brain mapping for the resection of eloquent-area tumors. A prospective analysis of methodology, correlation, and usefulness based on clinical outcomes. Acta Neurochir (Wien) 2010; 152 (11) 1835-1846
    CrossrefPubMedGoogle Scholar
  • 104 Voets NL, Pretorius P, Birch MD, Apostolopoulos V, Stacey R, Plaha P. Diffusion tractography for awake craniotomy: accuracy and factors affecting specificity. J Neurooncol 2021; 153 (03) 547-557
    CrossrefPubMedGoogle Scholar
  • 105 Lolli VE, Coolen T, Sadeghi N, Voordecker P, Lefranc F. BOLD fMRI and DTI fiber tracking for preoperative mapping of eloquent cerebral regions in brain tumor patients: impact on surgical approach and outcome. Neurol Sci 2023; 44 (08) 2903-2914
    CrossrefPubMedGoogle Scholar
  • 106 Voets NL, Plaha P, Parker Jones O, Pretorius P, Bartsch A. Presurgical localization of the primary sensorimotor cortex in gliomas : when is resting state FMRI beneficial and sufficient?. Clin Neuroradiol 2021; 31 (01) 245-256
    CrossrefPubMedGoogle Scholar
  • 107 González-Darder JM, González-López P, Talamantes F. et al. Multimodal navigation in the functional microsurgical resection of intrinsic brain tumors located in eloquent motor areas: role of tractography. Neurosurg Focus 2010; 28 (02) E5
    CrossrefPubMedGoogle Scholar
  • 108 Pinsker MO, Nabavi A, Mehdorn HM. Neuronavigation and resection of lesions located in eloquent brain areas under local anesthesia and neuropsychological-neurophysiological monitoring. Minim Invasive Neurosurg 2007; 50 (05) 281-284
    Article in Thieme ConnectPubMedGoogle Scholar
  • 109 Sacko O, Lauwers-Cances V, Brauge D, Sesay M, Brenner A, Roux FE. Awake craniotomy vs surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 2011; 68 (05) 1192-1198 , discussion 1198–1199
    CrossrefPubMedGoogle Scholar
  • 110 Smith JS, Chang EF, Lamborn KR. et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 2008; 26 (08) 1338-1345
    CrossrefPubMedGoogle Scholar
  • 111 Majchrzak K, Kaspera W, Bobek-Billewicz B. et al. The assessment of prognostic factors in surgical treatment of low-grade gliomas: a prospective study. Clin Neurol Neurosurg 2012; 114 (08) 1135-1144
    CrossrefPubMedGoogle Scholar
  • 112 McGirt MJ, Chaichana KL, Attenello FJ. et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 2008; 63 (04) 700-707 , author reply 707–708
    CrossrefPubMedGoogle Scholar
  • 113 Ius T, Isola M, Budai R. et al. Low-grade glioma surgery in eloquent areas: volumetric analysis of extent of resection and its impact on overall survival. A single-institution experience in 190 patients: clinical article. J Neurosurg 2012; 117 (06) 1039-1052
    CrossrefPubMedGoogle Scholar
  • 114 Stummer W, Reulen HJ, Meinel T. et al; ALA-Glioma Study Group. Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 2008; 62 (03) 564-576 , discussion 564–576
    CrossrefPubMedGoogle Scholar
  • 115 Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. J Neurooncol 2016; 130 (02) 269-282
    CrossrefPubMedGoogle Scholar
  • 116 Oppenlander ME, Wolf AB, Snyder LA. et al. An extent of resection threshold for recurrent glioblastoma and its risk for neurological morbidity. J Neurosurg 2014; 120 (04) 846-853
    CrossrefPubMedGoogle Scholar
  • 117 Keles GE, Chang EF, Lamborn KR. et al. Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 2006; 105 (01) 34-40
    CrossrefPubMedGoogle Scholar
  • 118 McGirt MJ, Chaichana KL, Gathinji M. et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 2009; 110 (01) 156-162
    CrossrefPubMedGoogle Scholar
  • 119 Yang K, Nath S, Koziarz A. et al. Biopsy versus subtotal versus gross total resection in patients with low-grade glioma: a systematic review and meta-analysis. World Neurosurg 2018; 120: e762-e775
    CrossrefPubMedGoogle Scholar
  • 120 Almenawer SA, Badhiwala JH, Alhazzani W. et al. Biopsy versus partial versus gross total resection in older patients with high-grade glioma: a systematic review and meta-analysis. Neuro-oncol 2015; 17 (06) 868-881
    CrossrefPubMedGoogle Scholar
  • 121 Gerritsen JKW, Zwarthoed RH, Kilgallon JL. et al. Effect of awake craniotomy in glioblastoma in eloquent areas (GLIOMAP): a propensity score-matched analysis of an international, multicentre, cohort study. Lancet Oncol 2022; 23 (06) 802-817
    CrossrefPubMedGoogle Scholar
  • 122 Gerritsen JKW, Arends L, Klimek M, Dirven CMF, Vincent AJE. Impact of intraoperative stimulation mapping on high-grade glioma surgery outcome: a meta-analysis. Acta Neurochir (Wien) 2019; 161 (01) 99-107
    CrossrefPubMedGoogle Scholar
  • 123 Bu LH, Zhang J, Lu JF, Wu JS. Glioma surgery with awake language mapping versus generalized anesthesia: a systematic review. Neurosurg Rev 2021; 44 (04) 1997-2011
    CrossrefPubMedGoogle Scholar