Skip to main content

Advertisement

SpringerLink
Log in

Development of an educational method to rethink and learn oncological brain surgery in an “a la carte” connectome-based perspective

  • Technical Note
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Understanding the structural connectivity of white matter tracts (WMT) and their related functions is a prerequisite to implementing an “a la carte” “connectomic approach” to glioma surgery. However, accessible resources facilitating such an approach are lacking. Here we present an educational method that is readily accessible, simple, and reproducible that enables the visualization of WMTs on individual patient images via an atlas-based approach.

Methods

Our method uses the patient’s own magnetic resonance imaging (MRI) images and consists of three main steps: data conversion, normalization, and visualization; these are accomplished using accessible software packages and WMT atlases. We implement our method on three common cases encountered in glioma surgery: a right supplementary motor area tumor, a left insular tumor, and a left temporal tumor.

Results

Using patient-specific perioperative MRIs with open-sourced and co-registered atlas-derived WMTs, we highlight the critical subnetworks requiring specific surgical monitoring identified intraoperatively using direct electrostimulation mapping with cognitive monitoring. The aim of this didactic method is to provide the neurosurgical oncology community with an accessible and ready-to-use educational tool, enabling neurosurgeons to improve their knowledge of WMTs and to better learn their oncologic cases, especially in glioma surgery using awake mapping.

Conclusions

Taking no more than 3–5 min per patient and irrespective of their resource settings, we believe that this method will enable junior surgeons to develop an intuition, and a robust 3-dimensional imagery of WMT by regularly applying it to their cases both before and after surgery to develop an “a la carte” connectome-based perspective to glioma surgery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

WMT:

White matter tracts

MRI:

Magnetic resonance imaging

DTI:

Diffusion tensor imaging

SMA:

Supplementary motor area

DICOM:

Digital Imaging and Communications in Medicine

T1W:

T1-weighted

FLAIR:

Fluid-attenuated inversion recovery

NIFTI:

Neuroimaging Informatics Technology Initiative

MNI:

Montreal Neurological Institute

3D:

3-Dimensional

2D:

2-Dimensional

CST:

Corticospinal tract

NMN:

Negative motor network

FAT:

Frontal aslant tract

FST:

Fronto-striatal tract

DES:

Direct electrical stimulation

VPMC:

Ventral premotor cortex

PrG:

Precentral gyrus

SLF-III:

Superior longitudinal fasciculus III

AF:

Arcuate fasciculus

IFOF:

Inferior fronto-occipital fasciculus

MFG:

Middle frontal gyrus

DLPFC:

Dorsolateral prefrontal cortex

PPTT:

Pyramids and Palm Trees Test

ILF:

Inferior longitudinal fasciculus

STG:

Superior temporal gyrus

MTG:

Middle temporal gyrus

ITG:

Inferior temporal gyrus

TR:

Thalamic radiations

References

  1. Abson-Kraemer DL, Spencer DD (2008) Temporal lobectomy under general anesthesia. In: Starr PA, Barbaro NM, Larson PS (eds) Functional neurosurgery. Neurosurgical operative atlas, 2nd edn. Thieme, New York, pp 29–35

  2. Almairac F, Herbet G, Moritz-Gasser S, de Champfleur NM, Duffau H (2015) The left inferior fronto-occipital fasciculus subserves language semantics: a multilevel lesion study. Brain Struct Funct 220:1983–1995. https://doi.org/10.1007/s00429-014-0773-1

    Article  PubMed  Google Scholar 

  3. Azad TD, Duffau H (2020) Limitations of functional neuroimaging for patient selection and surgical planning in glioma surgery. Neurosurg Focus 48:E12. https://doi.org/10.3171/2019.11.FOCUS19769

    Article  PubMed  Google Scholar 

  4. Bello L, Gambini A, Castellano A, Carrabba G, Acerbi F, Fava E, Giussani C, Cadioli M, Blasi V, Casarotti A, Papagno C, Gupta AK, Gaini S, Scotti G, Falini A (2008) Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39:369–382. https://doi.org/10.1016/j.neuroimage.2007.08.031

    Article  PubMed  Google Scholar 

  5. Burgel U, Madler B, Honey CR, Thron A, Gilsbach J, Coenen VA (2009) Fiber tracking with distinct software tools results in a clear diversity in anatomical fiber tract portrayal. Cent Eur Neurosurg 70:27–35. https://doi.org/10.1055/s-0028-1087212

    Article  CAS  PubMed  Google Scholar 

  6. Catani M, Dell’acqua F, Vergani F, Malik F, Hodge H, Roy P, Valabregue R, Thiebaut de Schotten M (2012) Short frontal lobe connections of the human brain. Cortex 48:273–291. https://doi.org/10.1016/j.cortex.2011.12.001

    Article  PubMed  Google Scholar 

  7. Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94. https://doi.org/10.1006/nimg.2002.1136

    Article  PubMed  Google Scholar 

  8. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132. https://doi.org/10.1016/j.cortex.2008.05.004

    Article  PubMed  Google Scholar 

  9. Caverzasi E, Hervey-Jumper SL, Jordan KM, Lobach IV, Li J, Panara V, Racine CA, Sankaranarayanan V, Amirbekian B, Papinutto N, Berger MS, Henry RG (2016) Identifying preoperative language tracts and predicting postoperative functional recovery using HARDI q-ball fiber tractography in patients with gliomas. J Neurosurg 125:33–45. https://doi.org/10.3171/2015.6.JNS142203

    Article  PubMed  Google Scholar 

  10. De Benedictis A, Duffau H (2011) Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery 68:1709–1723; discussion 1723. https://doi.org/10.1227/NEU.0b013e3182124690

  11. De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30:2559–2565. https://doi.org/10.1200/JCO.2011.38.4818

    Article  PubMed  Google Scholar 

  12. Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4:476–486. https://doi.org/10.1016/S1474-4422(05)70140-X

    Article  PubMed  Google Scholar 

  13. Duffau H (2006) New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity–a review. J Neurooncol 79:77–115. https://doi.org/10.1007/s11060-005-9109-6

    Article  PubMed  Google Scholar 

  14. Duffau H (2014) The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58:325–337. https://doi.org/10.1016/j.cortex.2013.08.005

    Article  PubMed  Google Scholar 

  15. Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11:255–265. https://doi.org/10.1038/nrneurol.2015.51

    Article  PubMed  Google Scholar 

  16. Duffau H (2016) Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up. Acta Neurochir (Wien) 158:51–58. https://doi.org/10.1007/s00701-015-2621-3

    Article  PubMed  Google Scholar 

  17. Duffau H (2017) A two-level model of interindividual anatomo-functional variability of the brain and its implications for neurosurgery. Cortex 86:303–313. https://doi.org/10.1016/j.cortex.2015.12.009

    Article  PubMed  Google Scholar 

  18. Duffau H (2021) Awake surgery for left posterior insular low-grade glioma through the parietorolandic operculum: the need to preserve the functional connectivity. A case series. Front Surg 8:824003. https://doi.org/10.3389/fsurg.2021.824003

    Article  PubMed  Google Scholar 

  19. Duffau H (2021) New philosophy, clinical pearls, and methods for intraoperative cognition mapping and monitoring “a la carte” in brain tumor patients. Neurosurgery 88:919–930. https://doi.org/10.1093/neuros/nyaa363

    Article  PubMed  Google Scholar 

  20. Duffau H (2022) Awake mapping with transopercular approach in right insular-centered low-grade gliomas improves neurological outcomes and return to work. Neurosurgery 91:182–190. https://doi.org/10.1227/neu.0000000000001966

    Article  PubMed  Google Scholar 

  21. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, Capelle L (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–96) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851. https://doi.org/10.1136/jnnp.2004.048520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Duffau H, Mandonnet E (2013) The “onco-functional balance” in surgery for diffuse low-grade glioma: integrating the extent of resection with quality of life. Acta Neurochir (Wien) 155:951–957. https://doi.org/10.1007/s00701-013-1653-9

    Article  PubMed  Google Scholar 

  23. Duffau H, Ng S, Lemaitre AL, Moritz-Gasser S, Herbet G (2022) Constant multi-tasking with time constraint to preserve across-network dynamics throughout awake surgery for low-grade glioma: a necessary step to enable patients resuming an active life. Front Oncol 12:924762. https://doi.org/10.3389/fonc.2022.924762

    Article  PubMed  PubMed Central  Google Scholar 

  24. Essayed WI, Zhang F, Unadkat P, Cosgrove GR, Golby AJ, O’Donnell LJ (2017) White matter tractography for neurosurgical planning: a topography-based review of the current state of the art. Neuroimage Clin 15:659–672. https://doi.org/10.1016/j.nicl.2017.06.011

    Article  PubMed  PubMed Central  Google Scholar 

  25. Fernandez-Miranda JC, Rhoton Jr. AL, Alvarez-Linera J, Kakizawa Y, Choi C, de Oliveira EP (2008) Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 62:989–1026; discussion 1026–1028. https://doi.org/10.1227/01.neu.0000333767.05328.49

  26. Giampiccolo D, Moritz-Gasser S, Ng S, Lemaitre AL, Duffau H (2022) Jargonaphasia as a disconnection syndrome: a study combining white matter electrical stimulation and disconnectome mapping. Brain Stimul 15:87–95. https://doi.org/10.1016/j.brs.2021.11.012

    Article  PubMed  Google Scholar 

  27. Grisot G, Haber SN, Yendiki A (2021) Diffusion MRI and anatomic tracing in the same brain reveal common failure modes of tractography. Neuroimage 239:118300. https://doi.org/10.1016/j.neuroimage.2021.118300

    Article  PubMed  Google Scholar 

  28. Gungor A, Baydin S, Middlebrooks EH, Tanriover N, Isler C, Rhoton AL Jr (2017) The white matter tracts of the cerebrum in ventricular surgery and hydrocephalus. J Neurosurg 126:945–971. https://doi.org/10.3171/2016.1.JNS152082

    Article  PubMed  Google Scholar 

  29. Henderson F, Abdullah KG, Verma R, Brem S (2020) Tractography and the connectome in neurosurgical treatment of gliomas: the premise, the progress, and the potential. Neurosurg Focus 48:E6. https://doi.org/10.3171/2019.11.FOCUS19785

    Article  PubMed  PubMed Central  Google Scholar 

  30. Herbet G, Duffau H (2020) Revisiting the functional anatomy of the human brain: toward a meta-networking theory of cerebral functions. Physiol Rev 100:1181–1228. https://doi.org/10.1152/physrev.00033.2019

    Article  PubMed  Google Scholar 

  31. Herbet G, Duffau H (2022) Contribution of the medial eye field network to the voluntary deployment of visuospatial attention. Nat Commun 13:328. https://doi.org/10.1038/s41467-022-28030-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, Menjot de Champfleur N, Duffau H (2014) Inferring a dual-stream model of mentalizing from associative white matter fibres disconnection. Brain 137:944–959. https://doi.org/10.1093/brain/awt370

    Article  PubMed  Google Scholar 

  33. Herbet G, Maheu M, Costi E, Lafargue G, Duffau H (2016) Mapping neuroplastic potential in brain-damaged patients. Brain 139:829–844. https://doi.org/10.1093/brain/awv394

    Article  PubMed  Google Scholar 

  34. Herbet G, Moritz-Gasser S, Boiseau M, Duvaux S, Cochereau J, Duffau H (2016) Converging evidence for a cortico-subcortical network mediating lexical retrieval. Brain 139:3007–3021. https://doi.org/10.1093/brain/aww220

    Article  PubMed  Google Scholar 

  35. Herbet G, Moritz-Gasser S, Lemaitre AL, Almairac F, Duffau H (2019) Functional compensation of the left inferior longitudinal fasciculus for picture naming. Cogn Neuropsychol 36:140–157. https://doi.org/10.1080/02643294.2018.1477749

    Article  PubMed  Google Scholar 

  36. Herbet G, Zemmoura I, Duffau H (2018) Functional anatomy of the inferior longitudinal fasciculus: from historical reports to current hypotheses. Front Neuroanat 12:77. https://doi.org/10.3389/fnana.2018.00077

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H (2011) Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain.” Neuroimage 56:992–1000. https://doi.org/10.1016/j.neuroimage.2011.03.022

    Article  PubMed  Google Scholar 

  38. Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL (2004) Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 25:356–369

    PubMed  PubMed Central  Google Scholar 

  39. Kinoshita M, de Champfleur NM, Deverdun J, Moritz-Gasser S, Herbet G, Duffau H (2015) Role of fronto-striatal tract and frontal aslant tract in movement and speech: an axonal mapping study. Brain Struct Funct 220:3399–3412. https://doi.org/10.1007/s00429-014-0863-0

    Article  PubMed  Google Scholar 

  40. Krainik A, Lehericy S, Duffau H, Vlaicu M, Poupon F, Capelle L, Cornu P, Clemenceau S, Sahel M, Valery CA, Boch AL, Mangin JF, Bihan DL, Marsault C (2001) Role of the supplementary motor area in motor deficit following medial frontal lobe surgery. Neurology 57:871–878. https://doi.org/10.1212/wnl.57.5.871

    Article  CAS  PubMed  Google Scholar 

  41. Kucukyuruk B, Yagmurlu K, Tanriover N, Uzan M, Rhoton Jr. AL, (2014) Microsurgical anatomy of the white matter tracts in hemispherotomy. Neurosurgery 10 Suppl 2:305–324; discussion 324. https://doi.org/10.1227/NEU.0000000000000288

  42. Lemaitre AL, Herbet G, Ng S, Moritz-Gasser S, Duffau H (2022) Cognitive preservation following awake mapping-based neurosurgery for low-grade gliomas: a longitudinal, within-patient design study. Neuro Oncol 24:781–793. https://doi.org/10.1093/neuonc/noab275

    Article  PubMed  Google Scholar 

  43. Maier-Hein KH, Neher PF, Houde JC, Cote MA, Garyfallidis E, Zhong J, Chamberland M, Yeh FC, Lin YC, Ji Q, Reddick WE, Glass JO, Chen DQ, Feng Y, Gao C, Wu Y, Ma J, He R, Li Q, Westin CF, Deslauriers-Gauthier S, Gonzalez JOO, Paquette M, St-Jean S, Girard G, Rheault F, Sidhu J, Tax CMW, Guo F, Mesri HY, David S, Froeling M, Heemskerk AM, Leemans A, Bore A, Pinsard B, Bedetti C, Desrosiers M, Brambati S, Doyon J, Sarica A, Vasta R, Cerasa A, Quattrone A, Yeatman J, Khan AR, Hodges W, Alexander S, Romascano D, Barakovic M, Auria A, Esteban O, Lemkaddem A, Thiran JP, Cetingul HE, Odry BL, Mailhe B, Nadar MS, Pizzagalli F, Prasad G, Villalon-Reina JE, Galvis J, Thompson PM, Requejo FS, Laguna PL, Lacerda LM, Barrett R, Dell’Acqua F, Catani M, Petit L, Caruyer E, Daducci A, Dyrby TB, Holland-Letz T, Hilgetag CC, Stieltjes B, Descoteaux M (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8:1349. https://doi.org/10.1038/s41467-017-01285-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Martino J, De Witt Hamer PC, Berger MS, Lawton MT, Arnold CM, de Lucas EM, Duffau H (2013) Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct 218:105–121. https://doi.org/10.1007/s00429-012-0386-5

    Article  PubMed  Google Scholar 

  45. Martino J, Vergani F, Robles SG, Duffau H (2010) New insights into the anatomic dissection of the temporal stem with special emphasis on the inferior fronto-occipital fasciculus: implications in surgical approach to left mesiotemporal and temporoinsular structures. Neurosurgery 66:4–12. https://doi.org/10.1227/01.NEU.0000348564.28415.FA

    Article  PubMed  Google Scholar 

  46. Morell AA, Eichberg DG, Shah AH, Luther E, Lu VM, Kader M, Higgins DMO, Merenzon M, Patel NV, Komotar RJ, Ivan ME (2022) Using machine learning to evaluate large-scale brain networks in patients with brain tumors: traditional and non-traditional eloquent areas. Neurooncol Adv 4:vdac142. https://doi.org/10.1093/noajnl/vdac142

    Article  PubMed  PubMed Central  Google Scholar 

  47. Moritz-Gasser S, Herbet G, Duffau H (2013) Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: a brain electrostimulation study. Neuropsychologia 51:1814–1822. https://doi.org/10.1016/j.neuropsychologia.2013.06.007

    Article  PubMed  Google Scholar 

  48. Ng S, Herbet G, Lemaitre AL, Cochereau J, Moritz-Gasser S, Duffau H (2020) Neuropsychological assessments before and after awake surgery for incidental low-grade gliomas. J Neurosurg 1–10. https://doi.org/10.3171/2020.7.JNS201507

  49. Ng S, Herbet G, Moritz-Gasser S, Duffau H (2020) Return to work following surgery for incidental diffuse low-grade glioma: a prospective series with 74 patients. Neurosurgery 87:720–729. https://doi.org/10.1093/neuros/nyz513

    Article  PubMed  Google Scholar 

  50. Ng S, Lemaitre AL, Moritz-Gasser S, Herbet G, Duffau H (2022) Recurrent low-grade gliomas: does reoperation affect neurocognitive functioning? Neurosurgery 90:221–232. https://doi.org/10.1227/NEU.0000000000001784

    Article  PubMed  Google Scholar 

  51. Ng S, Moritz-Gasser S, Lemaitre AL, Duffau H, Herbet G (2021) White matter disconnectivity fingerprints causally linked to dissociated forms of alexia. Commun Biol 4:1413. https://doi.org/10.1038/s42003-021-02943-z

    Article  PubMed  PubMed Central  Google Scholar 

  52. Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R (2000) Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 47:1070–1079; discussion 1079–1080. https://doi.org/10.1097/00006123-200011000-00008

  53. Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures–initial experience. Radiology 234:218–225. https://doi.org/10.1148/radiol.2341031984

    Article  PubMed  Google Scholar 

  54. Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56:130–137; discussion 138. https://doi.org/10.1227/01.neu.0000144842.18771.30

  55. Obara T, Blonski M, Brzenczek C, Mezieres S, Gaudeau Y, Pouget C, Gauchotte G, Verger A, Vogin G, Moureaux JM, Duffau H, Rech F, Taillandier L (2020) Adult diffuse low-grade gliomas: 35-year experience at the Nancy France Neurooncology Unit. Front Oncol 10:574679. https://doi.org/10.3389/fonc.2020.574679

    Article  PubMed  PubMed Central  Google Scholar 

  56. Pujol S, Wells W, Pierpaoli C, Brun C, Gee J, Cheng G, Vemuri B, Commowick O, Prima S, Stamm A, Goubran M, Khan A, Peters T, Neher P, Maier-Hein KH, Shi Y, Tristan-Vega A, Veni G, Whitaker R, Styner M, Westin CF, Gouttard S, Norton I, Chauvin L, Mamata H, Gerig G, Nabavi A, Golby A, Kikinis R (2015) The DTI challenge: toward standardized evaluation of diffusion tensor imaging tractography for neurosurgery. J Neuroimaging 25:875–882. https://doi.org/10.1111/jon.12283

    Article  PubMed  PubMed Central  Google Scholar 

  57. Rech F, Duffau H, Pinelli C, Masson A, Roublot P, Billy-Jacques A, Brissart H, Civit T (2017) Intraoperative identification of the negative motor network during awake surgery to prevent deficit following brain resection in premotor regions. Neurochirurgie 63:235–242. https://doi.org/10.1016/j.neuchi.2016.08.006

    Article  CAS  PubMed  Google Scholar 

  58. Rech F, Herbet G, Moritz-Gasser S, Duffau H (2016) Somatotopic organization of the white matter tracts underpinning motor control in humans: an electrical stimulation study. Brain Struct Funct 221:3743–3753. https://doi.org/10.1007/s00429-015-1129-1

    Article  PubMed  Google Scholar 

  59. Rech F, Wassermann D, Duffau H (2020) New insights into the neural foundations mediating movement/language interactions gained from intrasurgical direct electrostimulations. Brain Cogn 142:105583. https://doi.org/10.1016/j.bandc.2020.105583

    Article  PubMed  Google Scholar 

  60. Rorden C, Bonilha L, Fridriksson J, Bender B, Karnath HO (2012) Age-specific CT and MRI templates for spatial normalization. Neuroimage 61:957–965. https://doi.org/10.1016/j.neuroimage.2012.03.020

    Article  PubMed  Google Scholar 

  61. Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358:18–27. https://doi.org/10.1056/NEJMoa067819

    Article  CAS  PubMed  Google Scholar 

  62. Santos C, Velasquez C, Esteban J, Fernandez L, Mandonnet E, Duffau H, Martino J (2021) Transopercular insular approach, overcoming the training curve using a cadaveric simulation model: 2-dimensional operative video. Oper Neurosurg (Hagerstown) 21:E561–E562. https://doi.org/10.1093/ons/opab342

    Article  PubMed  Google Scholar 

  63. Sarubbo S, Annicchiarico L, Corsini F, Zigiotto L, Herbet G, Moritz-Gasser S, Dalpiaz C, Vitali L, Tate M, De Benedictis A, Amorosino G, Olivetti E, Rozzanigo U, Petralia B, Duffau H, Avesani P (2021) Planning brain tumor resection using a probabilistic atlas of cortical and subcortical structures critical for functional processing: a proof of concept. Oper Neurosurg (Hagerstown) 20:E175–E183. https://doi.org/10.1093/ons/opaa396

    Article  PubMed  Google Scholar 

  64. Sarubbo S, De Benedictis A, Maldonado IL, Basso G, Duffau H (2013) Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Struct Funct 218:21–37. https://doi.org/10.1007/s00429-011-0372-3

    Article  PubMed  Google Scholar 

  65. Sarubbo S, De Benedictis A, Merler S, Mandonnet E, Balbi S, Granieri E, Duffau H (2015) Towards a functional atlas of human white matter. Hum Brain Mapp 36:3117–3136. https://doi.org/10.1002/hbm.22832

    Article  PubMed  PubMed Central  Google Scholar 

  66. Sarubbo S, Duffau H (2021) Connectomic evidences driving a functional approach in neuro-oncological surgery. J Neurosurg Sci 65:545–547. https://doi.org/10.23736/S0390-5616.21.05517-X

    Article  PubMed  Google Scholar 

  67. Sarubbo S, Tate M, De Benedictis A, Merler S, Moritz-Gasser S, Herbet G, Duffau H (2020) Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: an original functional atlas of the human brain. Neuroimage 205:116237. https://doi.org/10.1016/j.neuroimage.2019.116237

    Article  PubMed  Google Scholar 

  68. Sarubbo S, Tate M, De Benedictis A, Merler S, Moritz-Gasser S, Herbet G, Duffau H (2020) A normalized dataset of 1821 cortical and subcortical functional responses collected during direct electrical stimulation in patients undergoing awake brain surgery. Data Brief 28:104892. https://doi.org/10.1016/j.dib.2019.104892

    Article  PubMed  Google Scholar 

  69. Schilling KG, Nath V, Hansen C, Parvathaneni P, Blaber J, Gao Y, Neher P, Aydogan DB, Shi Y, Ocampo-Pineda M, Schiavi S, Daducci A, Girard G, Barakovic M, Rafael-Patino J, Romascano D, Rensonnet G, Pizzolato M, Bates A, Fischi E, Thiran JP, Canales-Rodriguez EJ, Huang C, Zhu H, Zhong L, Cabeen R, Toga AW, Rheault F, Theaud G, Houde JC, Sidhu J, Chamberland M, Westin CF, Dyrby TB, Verma R, Rathi Y, Irfanoglu MO, Thomas C, Pierpaoli C, Descoteaux M, Anderson AW, Landman BA (2019) Limits to anatomical accuracy of diffusion tractography using modern approaches. Neuroimage 185:1–11. https://doi.org/10.1016/j.neuroimage.2018.10.029

    Article  PubMed  Google Scholar 

  70. Schilling KG, Rheault F, Petit L, Hansen CB, Nath V, Yeh FC, Girard G, Barakovic M, Rafael-Patino J, Yu T, Fischi-Gomez E, Pizzolato M, Ocampo-Pineda M, Schiavi S, Canales-Rodriguez EJ, Daducci A, Granziera C, Innocenti G, Thiran JP, Mancini L, Wastling S, Cocozza S, Petracca M, Pontillo G, Mancini M, Vos SB, Vakharia VN, Duncan JS, Melero H, Manzanedo L, Sanz-Morales E, Pena-Melian A, Calamante F, Attye A, Cabeen RP, Korobova L, Toga AW, Vijayakumari AA, Parker D, Verma R, Radwan A, Sunaert S, Emsell L, De Luca A, Leemans A, Bajada CJ, Haroon H, Azadbakht H, Chamberland M, Genc S, Tax CMW, Yeh PH, Srikanchana R, McKnight CD, Yang JY, Chen J, Kelly CE, Yeh CH, Cochereau J, Maller JJ, Welton T, Almairac F, Seunarine KK, Clark CA, Zhang F, Makris N, Golby A, Rathi Y, O’Donnell LJ, Xia Y, Aydogan DB, Shi Y, Fernandes FG, Raemaekers M, Warrington S, Michielse S, Ramirez-Manzanares A, Concha L, Aranda R, Meraz MR, Lerma-Usabiaga G, Roitman L, Fekonja LS, Calarco N, Joseph M, Nakua H, Voineskos AN, Karan P, Grenier G, Legarreta JH, Adluru N, Nair VA, Prabhakaran V, Alexander AL, Kamagata K, Saito Y, Uchida W, Andica C, Abe M, Bayrak RG, Wheeler-Kingshott C, D’Angelo E, Palesi F, Savini G, Rolandi N, Guevara P, Houenou J, Lopez-Lopez N, Mangin JF, Poupon C, Roman C, Vazquez A, Maffei C, Arantes M, Andrade JP, Silva SM, Calhoun VD, Caverzasi E, Sacco S, Lauricella M, Pestilli F, Bullock D, Zhan Y, Brignoni-Perez E, Lebel C, Reynolds JE, Nestrasil I, Labounek R, Lenglet C, Paulson A, Aulicka S, Heilbronner SR, Heuer K, Chandio BQ, Guaje J, Tang W, Garyfallidis E, Raja R, Anderson AW, Landman BA, Descoteaux M (2021) Tractography dissection variability: what happens when 42 groups dissect 14 white matter bundles on the same dataset? Neuroimage 243:118502.https://doi.org/10.1016/j.neuroimage.2021.118502

  71. Sheth SA, Mian MK, Eskandar EN, Cosgrove GR (2008) Temporal lobe operations in intractable epilepsy. In: Quiñones-Hinojosa A (ed) Schmidek & Sweet operative neurosurgical techniques: indications, methods, and results, 6th edn. Saunders Elsevier, Philadelphia, pp 1265–1272

  72. Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DG, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54:49–59. https://doi.org/10.1016/j.neuroimage.2010.07.055

    Article  PubMed  Google Scholar 

  73. Valdes PA, Fan X, Ji S, Harris BT, Paulsen KD, Roberts DW (2010) Estimation of brain deformation for volumetric image updating in protoporphyrin IX fluorescence-guided resection. Stereotact Funct Neurosurg 88:1–10. https://doi.org/10.1159/000258143

    Article  PubMed  Google Scholar 

  74. Vanderweyen DC, Theaud G, Sidhu J, Rheault F, Sarubbo S, Descoteaux M, Fortin D (2020) The role of diffusion tractography in refining glial tumor resection. Brain Struct Funct 225:1413–1436. https://doi.org/10.1007/s00429-020-02056-z

    Article  PubMed  Google Scholar 

  75. Wang X, Pathak S, Stefaneanu L, Yeh FC, Li S, Fernandez-Miranda JC (2016) Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain. Brain Struct Funct 221:2075–2092. https://doi.org/10.1007/s00429-015-1028-5

    Article  PubMed  Google Scholar 

  76. Wyler AR (2008) Temporal lobectomy. In: Starr PAB, Nicholas M.; Larson, Paul S. (ed) Functional neurosurgery. Neurosurgical Operative Atlas, 2nd edn. Thieme

  77. Yang JY, Beare R, Seal ML, Harvey AS, Anderson VA, Maixner WJ (2017) A systematic evaluation of intraoperative white matter tract shift in pediatric epilepsy surgery using high-field MRI and probabilistic high angular resolution diffusion imaging tractography. J Neurosurg Pediatr 19:592–605. https://doi.org/10.3171/2016.11.PEDS16312

    Article  PubMed  Google Scholar 

  78. Yang JY, Yeh CH, Poupon C, Calamante F (2021) Diffusion MRI tractography for neurosurgery: the basics, current state, technical reliability and challenges. Phys Med Biol 66. https://doi.org/10.1088/1361-6560/ac0d90

  79. Yeh FC, Panesar S, Fernandes D, Meola A, Yoshino M, Fernandez-Miranda JC, Vettel JM, Verstynen T (2018) Population-averaged atlas of the macroscale human structural connectome and its network topology. Neuroimage 178:57–68. https://doi.org/10.1016/j.neuroimage.2018.05.027

    Article  PubMed  Google Scholar 

  80. Yeung JT, Taylor HM, Nicholas PJ, Young IM, Jiang I, Doyen S, Sughrue ME, Teo C (2021) Using Quicktome for intracerebral surgery: early retrospective study and proof of concept. World Neurosurg 154:e734–e742. https://doi.org/10.1016/j.wneu.2021.07.127

    Article  PubMed  Google Scholar 

  81. Yeung JT, Taylor HM, Young IM, Nicholas PJ, Doyen S, Sughrue ME (2021) Unexpected hubness: a proof-of-concept study of the human connectome using pagerank centrality and implications for intracerebral neurosurgery. J Neurooncol 151:249–256. https://doi.org/10.1007/s11060-020-03659-6

    Article  PubMed  Google Scholar 

  82. Yordanova YN, Duffau H, Herbet G (2017) Neural pathways subserving face-based mentalizing. Brain Struct Funct 222:3087–3105. https://doi.org/10.1007/s00429-017-1388-0

    Article  PubMed  Google Scholar 

  83. Zhang F, Wu Y, Norton I, Rigolo L, Rathi Y, Makris N, O’Donnell LJ (2018) An anatomically curated fiber clustering white matter atlas for consistent white matter tract parcellation across the lifespan. Neuroimage 179:429–447. https://doi.org/10.1016/j.neuroimage.2018.06.027

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, University of Texas Medical Branch, Galveston, TX, 77555, USA

    Pablo A. Valdes

  2. Department of Neurosurgery, Hôpital Gui de Chauliac, CHU Montpellier, 80 Av Augustin Fliche, 34295, Montpellier, France

    Pablo A. Valdes, Sam Ng & Hugues Duffau

  3. Team “Plasticity of Central Nervous System, Human Stem Cells and Glial Tumors”, Institute of Functional Genomics, INSERM U1191, University of Montpellier, 141 Rue de la cardonille, 34091, Montpellier, France

    Sam Ng & Hugues Duffau

  4. Department of Neurosurgery, Harvard Medical School/Brigham and Women’s Hospital, Boston, MA, 02115, USA

    Joshua D. Bernstock

  5. David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA

    Joshua D. Bernstock

Authors
  1. Pablo A. Valdes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sam Ng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joshua D. Bernstock
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hugues Duffau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pablo A. Valdes.

Ethics declarations

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the Montpellier University Medical Center and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. All patients provided informed consent to participate under a study protocol approved by the institutional review board of the Montpellier University Medical Center (#202000557).

Conflict of interest

PAV is a consultant for an unrelated fluorescence-guided surgery study for NX Development Corp. JDB has an equity position in Treovir LLC, an oHSV clinical stage company, and is a member of the POCKiT Diagnostics Board of Scientific Advisors.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Previous presentations

None.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 6695 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valdes, P.A., Ng, S., Bernstock, J.D. et al. Development of an educational method to rethink and learn oncological brain surgery in an “a la carte” connectome-based perspective. Acta Neurochir 165, 2489–2500 (2023). https://doi.org/10.1007/s00701-023-05626-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-023-05626-2

Keywords

Search

Navigation