Cortical and white matter anatomy relevant for the lateral and superior approaches to resect intraaxial lesions within the frontal lobe.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
10 Dec 2022
10 Dec 2022
Historique:
received:
28
03
2022
accepted:
29
11
2022
entrez:
10
12
2022
pubmed:
11
12
2022
medline:
15
12
2022
Statut:
epublish
Résumé
Despite being associated with high-order neurocognitive functions, the frontal lobe plays an important role in core neurological functions, such as motor and language functions. The aim of this study was to present a neurosurgical perspective of the cortical and subcortical anatomy of the frontal lobe in terms of surgical treatment of intraaxial frontal lobe lesions. We also discuss the results of direct brain mapping when awake craniotomy is performed. Ten adult cerebral hemispheres were prepared for white matter dissection according to the Klingler technique. Intraaxial frontal lobe lesions are approached with a superior or lateral trajectory during awake conditions. The highly eloquent cortex within the frontal lobe is identified within the inferior frontal gyrus (IFG) and precentral gyrus. The trajectory of the approach is mainly related to the position of the lesion in relation to the arcuate fascicle/superior longitudinal fascicle complex and ventricular system. Knowledge of the cortical and subcortical anatomy and its function within the frontal lobe is essential for preoperative planning and predicting the risk of immediate and long-term postoperative deficits. This allows surgeons to properly set the extent of the resection and type of approach during preoperative planning.
Identifiants
pubmed: 36496517
doi: 10.1038/s41598-022-25375-z
pii: 10.1038/s41598-022-25375-z
pmc: PMC9741612
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
21402Informations de copyright
© 2022. The Author(s).
Références
Alvarez, J. A. & Emory, E. Executive function and the frontal lobes: A meta-analytic review. Neuropsychol. Rev. 16, 17–42. https://doi.org/10.1007/s11065-006-9002-x (2006).
doi: 10.1007/s11065-006-9002-x
Yasargil, M. G. et al. Tumours of the limbic and paralimbic systems. Acta Neurochir. (Wien) 118, 40–52. https://doi.org/10.1007/BF01400725 (1992).
doi: 10.1007/BF01400725
Duffau, H. & Capelle, L. Preferential brain locations of low-grade gliomas. Cancer 100, 2622–2626. https://doi.org/10.1002/cncr.20297 (2004).
doi: 10.1002/cncr.20297
Dziedzic, T. A., Bala, A. & Marchel, A. Anatomical aspects of the insula, opercula and peri-insular white matter for a transcortical approach to insular glioma resection. Neurosurg. Rev. https://doi.org/10.1007/s10143-021-01602-5 (2021).
doi: 10.1007/s10143-021-01602-5
Duffau, H. et al. The role of dominant premotor cortex in language: A study using intraoperative functional mapping in awake patients. Neuroimage 20, 1903–1914. https://doi.org/10.1016/s1053-8119(03)00203-9 (2003).
doi: 10.1016/s1053-8119(03)00203-9
De Benedictis, A., Moritz-Gasser, S. & Duffau, H. Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery 66, 1074–1084. https://doi.org/10.1227/01.NEU.0000369514.74284.78 (2010) (discussion 1084).
doi: 10.1227/01.NEU.0000369514.74284.78
Smith, J. S. et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J. Clin. Oncol. 26, 1338–1345. https://doi.org/10.1200/JCO.2007.13.9337 (2008).
doi: 10.1200/JCO.2007.13.9337
Duffau, H. Diffuse low-grade glioma, oncological outcome and quality of life: A surgical perspective. Curr. Opin. Oncol. 30, 383–389. https://doi.org/10.1097/CCO.0000000000000483 (2018).
doi: 10.1097/CCO.0000000000000483
Brown, T. J. et al. Management of low-grade glioma: A systematic review and meta-analysis. NeuroOncol. Pract. 6, 249–258. https://doi.org/10.1093/nop/npy034 (2019).
doi: 10.1093/nop/npy034
Sanai, N., Mirzadeh, Z. & Berger, M. S. Functional outcome after language mapping for glioma resection. N. Engl. J. Med. 358, 18–27. https://doi.org/10.1056/NEJMoa067819 (2008).
doi: 10.1056/NEJMoa067819
Acioly, M. A., Cunha, A. M., Parise, M., Rodrigues, E. & Tovar-Moll, F. Recruitment of contralateral supplementary motor area in functional recovery following medial frontal lobe surgery: An fMRI case study. J. Neurol. Surg. A Cent. Eur. Neurosurg. 76, 508–512. https://doi.org/10.1055/s-0035-1558408 (2015).
doi: 10.1055/s-0035-1558408
Vassal, M. et al. Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area. J. Neurosurg. 126, 1181–1190. https://doi.org/10.3171/2016.4.JNS152484 (2017).
doi: 10.3171/2016.4.JNS152484
Ebeling, U., Rikli, D., Huber, P. & Reulen, H. J. The coronal suture, a useful bony landmark in neurosurgery? Craniocerebral topography between bony landmarks on the skull and the brain. Acta Neurochir (Wien) 89, 130–134. https://doi.org/10.1007/BF01560378 (1987).
doi: 10.1007/BF01560378
Frigeri, T., Paglioli, E., De Oliveira, E. & Rhoton, A. L. Microsurgical anatomy of the central lobe. J. Neurosurg. 122, 483–498. https://doi.org/10.3171/2014.11.JNS14315 (2015).
doi: 10.3171/2014.11.JNS14315
Berger, M. S. & Hadjipanayis, C. G. Surgery of intrinsic cerebral tumors. Neurosurgery 61, 279–304. https://doi.org/10.1227/01.NEU.0000255489.88321.18 (2007) (discussion 304–275).
doi: 10.1227/01.NEU.0000255489.88321.18
Dziedzic, T. & Bernstein, M. Awake craniotomy for brain tumor: Indications, technique and benefits. Exp. Rev. Neurother. 14, 1405–1415. https://doi.org/10.1586/14737175.2014.979793 (2014).
doi: 10.1586/14737175.2014.979793
Nachev, P., Kennard, C. & Husain, M. Functional role of the supplementary and pre-supplementary motor areas. Nat. Rev. Neurosci. 9, 856–869. https://doi.org/10.1038/nrn2478 (2008).
doi: 10.1038/nrn2478
Hiroshima, S., Anei, R., Murakami, N. & Kamada, K. Functional localization of the supplementary motor area. Neurol. Med. Chir. (Tokyo) 54, 511–520. https://doi.org/10.2176/nmc.oa2012-0321 (2014).
doi: 10.2176/nmc.oa2012-0321
Nakajima, R. et al. Intraoperative motor symptoms during brain tumor resection in the supplementary motor area (SMA) without positive mapping during awake surgery. Neurol. Med. Chir. (Tokyo) 55, 442–450. https://doi.org/10.2176/nmc.oa.2014-0343 (2015).
doi: 10.2176/nmc.oa.2014-0343
Voets, N. L., Bartsch, A. & Plaha, P. Brain white matter fibre tracts: A review of functional neuro-oncological relevance. J. Neurol. Neurosurg. Psychiatry 88, 1017–1025. https://doi.org/10.1136/jnnp-2017-316170 (2017).
doi: 10.1136/jnnp-2017-316170
Kinoshita, M. et al. 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 (2015).
doi: 10.1007/s00429-014-0863-0
Young, J. S., Morshed, R. A., Mansoori, Z., Cha, S. & Berger, M. S. Disruption of frontal aslant tract is not associated with long-term postoperative language deficits. World Neurosurg. 133, 192–195. https://doi.org/10.1016/j.wneu.2019.09.128 (2020).
doi: 10.1016/j.wneu.2019.09.128
Catani, M. et al. Short frontal lobe connections of the human brain. Cortex 48, 273–291. https://doi.org/10.1016/j.cortex.2011.12.001 (2012).
doi: 10.1016/j.cortex.2011.12.001
Ookawa, S. et al. Frontal fibers connecting the superior frontal gyrus to broca area: A corticocortical evoked potential study. World Neurosurg. 107, 239–248. https://doi.org/10.1016/j.wneu.2017.07.166 (2017).
doi: 10.1016/j.wneu.2017.07.166
Yamao, Y. & Matsumoto, R. Intraoperative cortico-cortical evoked potentials for monitoring the arcuate fasciculus: Feasible under general anesthesia?. Clin. Neurophysiol. 133, 175–176. https://doi.org/10.1016/j.clinph.2021.07.033 (2022).
doi: 10.1016/j.clinph.2021.07.033
Baker, C. M. et al. The crossed frontal aslant tract: A possible pathway involved in the recovery of supplementary motor area syndrome. Brain Behav. 8, e00926. https://doi.org/10.1002/brb3.926 (2018).
doi: 10.1002/brb3.926
Kendir, S. et al. Window anatomy for neurosurgical approaches. Laboratory investigation. J. Neurosurg. 111, 365–370. https://doi.org/10.3171/2008.10.JNS08159 (2009).
doi: 10.3171/2008.10.JNS08159
Van Geemen, K., Herbet, G., Moritz-Gasser, S. & Duffau, H. Limited plastic potential of the left ventral premotor cortex in speech articulation: Evidence from intraoperative awake mapping in glioma patients. Hum. Brain Mapp. 35, 1587–1596. https://doi.org/10.1002/hbm.22275 (2014).
doi: 10.1002/hbm.22275
Duffau, H. et al. Functional recovery after surgical resection of low grade gliomas in eloquent brain: Hypothesis of brain compensation. J. Neurol. Neurosurg. Psychiatry 74, 901–907. https://doi.org/10.1136/jnnp.74.7.901 (2003).
doi: 10.1136/jnnp.74.7.901
Fornia, L. et al. Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions. Nat. Commun. 11, 705. https://doi.org/10.1038/s41467-020-14517-4 (2020).
doi: 10.1038/s41467-020-14517-4
Roux, F. E. et al. The graphemic/motor frontal area Exner’s area revisited. Ann. Neurol. 66, 537–545. https://doi.org/10.1002/ana.21804 (2009).
doi: 10.1002/ana.21804
Matsuo, K. et al. Discrimination of Exner’s area and the frontal eye field in humans—Functional magnetic resonance imaging during language and saccade tasks. Neurosci. Lett. 340, 13–16. https://doi.org/10.1016/s0304-3940(03)00050-8 (2003).
doi: 10.1016/s0304-3940(03)00050-8
Vassal, F., Schneider, F., Sontheimer, A., Lemaire, J. J. & Nuti, C. Intraoperative visualisation of language fascicles by diffusion tensor imaging-based tractography in glioma surgery. Acta Neurochir (Wien) 155, 437–448. https://doi.org/10.1007/s00701-012-1580-1 (2013).
doi: 10.1007/s00701-012-1580-1
Fernandez Coello, A. et al. Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks. J. Neurosurg. 119, 1380–1394. https://doi.org/10.3171/2013.6.JNS122470 (2013).
doi: 10.3171/2013.6.JNS122470
Rhoton, A. L. The cerebrum. Anatomy. Neurosurgery 61, 37–118. https://doi.org/10.1227/01.NEU.0000255490.88321.CE (2007) (discussion 118–119).
doi: 10.1227/01.NEU.0000255490.88321.CE
Dziedzic, T. A., Balasa, A., Jezewski, M. P., Michalowski, L. & Marchel, A. White matter dissection with the Klingler technique: A literature review. Brain Struct. Funct. 226, 13–47. https://doi.org/10.1007/s00429-020-02157-9 (2021).
doi: 10.1007/s00429-020-02157-9
Yeh, F. C., Verstynen, T. D., Wang, Y., Fernandez-Miranda, J. C. & Tseng, W. Y. Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE 8, e80713. https://doi.org/10.1371/journal.pone.0080713 (2013).
doi: 10.1371/journal.pone.0080713