Abstract
Brain mapping during awake craniotomy for gliomas can help preserve neurological functions, including maintenance of central and peripheral vision. However, the consecutive changes in the visual field remain unknown. We retrospectively assessed 14 patients who underwent awake craniotomy for gliomas infiltrating into the optic radiation. Cortico-subcortical direct electrical stimulation (DES) was intraoperatively applied until transient visual symptoms were elicited and recorded. The visual fields were examined consecutively in the preoperative period and postoperative subacute and chronic periods. To evaluate the anatomo-functional validity of the recordings, all DES-elicited points were overlaid onto a three-dimensional template that included the optic radiation, using voxel-based morphometry (VBM) mapping. All patients experienced visual symptoms that were classified as phosphenes, blurred vision, or hallucinations during DES, and surgical resection was limited to within the functional boundaries. In VBM, almost all the subcortical positive mapping points overlapped with the surface of the optic radiation, and the distribution of sites that induced visual phenomena in the upper or lower visual fields could be differentiated in the anatomical space. We observed no postoperative visual deficit in four patients (29%), time-dependent improvements in five out of eight patients that presented transient quadrantanopia or partial visual defect (36% out of 57%), and permanent hemianopsia (14%) in two patients with occipital lesions. Intraoperative DES that identifies and preserves optic radiation in awake craniotomy for gliomas is a reliable and effective technique to reduce risk of permanent deficits, but has a low success rate in patients with occipital involvement.
Similar content being viewed by others
Data Availability
Data will be made available on reasonable request.
Code Availability
Not applicable.
Abbreviations
- DES:
-
Direct electrical stimulation
- DTI:
-
Diffusion tensor imaging
- DWI:
-
Diffusion weighted imaging
- FLAIR:
-
Fluid-attenuated inversion recovery
- MRI:
-
Magnetic resonance imaging
- QOL:
-
Quality of life
- VEP:
-
Visual evoked potential
- 3D:
-
Three-dimensional
References
And KT, Kolmel HW (1991) Patterns of recovery from homonymous hemianopia subsequent to infarction in the distribution of the posterior cerebral artery. Neuro-Ophthalmology 11(1):33–39. https://doi.org/10.3109/01658109109009640
Berardi N, Pizzorusso T, Ratto GM, Maffei L (2003) Molecular basis of plasticity in the visual cortex. Trends Neurosci 26(7):369–378. https://doi.org/10.1016/S0166-2236(03)00168-1
Bova SM, Giovenzana A, Signorini S, La Piana R, Uggetti C, Bianchi PE, Fazzi E (2008) Recovery of visual functions after early acquired occipital damage. Dev Med Child Neurol 50(4):311–315. https://doi.org/10.1111/j.1469-8749.2008.02044.x
Brett M, Leff AP, Rorden C, Ashburner J (2001) Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 14(2):486–500. https://doi.org/10.1006/nimg.2001.0845
Bron AM, Viswanathan AC, Thelen U, de Natale R, Ferreras A, Gundgaard J, Schwartz G, Buchholz P (2010) International vision requirements for driver licensing and disability pensions: using a milestone approach in characterization of progressive eye disease. Clin Ophthalmol 4:1361–1369. https://doi.org/10.2147/OPTH.S15359
Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44(8):1105–1132. https://doi.org/10.1016/j.cortex.2008.05.004
Çelebisoy M, Çelebisoy N, Bayam E, Köse T (2011) Recovery of visual-field defects after occipital lobe infarction: a perimetric study. J Neurol Neurosurg Psychiatry 82(6):695–702. https://doi.org/10.1136/jnnp.2010.214387
Charras P, Herbet G, Deverdun J, de Champfleur NM, Duffau H, Bartolomeo P, Bonnetblanc F (2015) Functional reorganization of the attentional networks in low-grade glioma patients: a longitudinal study. Cortex 63:27–41. https://doi.org/10.1016/j.cortex.2014.08.010
Curatolo JM, Macdonell RA, Berkovic SF, Fabinyi GC (2000) Intraoperative monitoring to preserve central visual fields during occipital corticectomy for epilepsy. J Clin Neurosci 7(3):234–237. https://doi.org/10.1054/jocn.1999.0208
Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, Mitchell MC, Sichez JP, Van Effenterre R (2003) Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74(7):901–907. https://doi.org/10.1136/jnnp.74.7.901
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(6):845–851. https://doi.org/10.1136/jnnp.2004.048520
Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L (2008) 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 109(3):461–471. https://doi.org/10.3171/JNS/2008/109/9/0461
Duffau H, Taillandier L (2015) New concepts in the management of diffuse low-grade glioma: proposal of a multistage and individualized therapeutic approach. Neuro Oncol 17(3):332–342. https://doi.org/10.1093/neuonc/nou153
Duffau H, Velut S, Mitchell MC, Gatignol P, Capelle L (2004) Intra-operative mapping of the subcortical visual pathways using direct electrical stimulations. Acta Neurochir (Wien) 146(3):265–269. https://doi.org/10.1007/s00701-003-0199-7 (discussion 269–270)
Gras-Combe G, Moritz-Gasser S, Herbet G, Duffau H (2012) Intraoperative subcortical electrical mapping of optic radiations in awake surgery for glioma involving visual pathways. J Neurosurg 117(3):466–473. https://doi.org/10.3171/2012.6.JNS111981
Guzzetta A, Fiori S, Scelfo D, Conti E, Bancale A (2013) Reorganization of visual fields after periventricular haemorrhagic infarction: potentials and limitations. Dev Med Child Neurol 55(Suppl 4):23–26. https://doi.org/10.1111/dmcn.12302
Hartwigsen G, Volz LJ (2021) Probing rapid network reorganization of motor and language functions via neuromodulation and neuroimaging. Neuroimage 224:117449. https://doi.org/10.1016/j.neuroimage.2020.117449
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
Horibe M, Mukuno K, Matsuzaki H, Handa T, Matsubayashi S, Nanba T, Tamura C, Shoji N, Shimizu K (2005) Examination of the intracranial disease patient in aware of visual loss and aware of abnormal visual field. JORTHOPTJ 34:157–163. https://doi.org/10.4263/jorthoptic.34.157
Hubel DH, Wiesel TN (1963) Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol 26:994–1002. https://doi.org/10.1152/jn.1963.26.6.994
Jiao Y, Lin F, Wu J, Li H, Fu W, Huo R, Cao Y, Wang S, Zhao J (2020) Plasticity in language cortex and white matter tracts after resection of dominant inferior parietal lobule arteriovenous malformations: a combined fMRI and DTI study. J Neurosurg 134(3):953–960. https://doi.org/10.3171/2019.12.JNS191987
Kamada K, Todo T, Morita A, Masutani Y, Aoki S, Ino K, Kawai K, Kirino T (2005) Functional monitoring for visual pathway using real-time visual evoked potentials and optic-radiation tractography. Neurosurgery 57(1):121–127. https://doi.org/10.1227/01.neu.0000163526.60240.b6 (discussion 121–127)
Kinoshita M, Miyashita K, Tsutsui T, Furuta T, Nakada M (2016a) Critical neural networks in awake surgery for gliomas. Neurol Med Chir 56(11):674–686. https://doi.org/10.2176/nmc.ra.2016-0069
Kinoshita M, Nakajima R, Shinohara H, Miyashita K, Tanaka S, Okita H, Nakada M, Hayashi Y (2016b) Chronic spatial working memory deficit associated with the superior longitudinal fasciculus: a study using voxel-based lesion-symptom mapping and intraoperative direct stimulation in right prefrontal glioma surgery. J Neurosurg 125(4):1024–1032. https://doi.org/10.3171/2015.10.JNS1591
Krolak-Salmon P, Guenot M, Tiliket C, Isnard J, Sindou M, Mauguiere F, Vighetto A (2000) Anatomy of optic nerve radiations as assessed by static perimetry and MRI after tailored temporal lobectomy. Br J Ophthalmol 84(8):884–889. https://doi.org/10.1136/bjo.84.8.884
Kwon HB, Sabatini BL (2011) Glutamate induces de novo growth of functional spines in developing cortex. Nature 474(7349):100–104. https://doi.org/10.1038/nature09986
Liu X, Kinoshita M, Shinohara H, Hori O, Ozaki N, Nakada M (2020) Does the superior fronto-occipital fascicle exist in the human brain? Fiber dissection and brain functional mapping in 90 patients with gliomas. NeuroImage Clin 25:102192. https://doi.org/10.1016/j.nicl.2020.102192
Maldaun MV, Khawja SN, Levine NB, Rao G, Lang FF, Weinberg JS, Tummala S, Cowles CE, Ferson D, Nguyen AT, Sawaya R, Suki D, Prabhu SS (2014) Awake craniotomy for gliomas in a high-field intraoperative magnetic resonance imaging suite: analysis of 42 cases. J Neurosurg 121(4):810–817. https://doi.org/10.3171/2014.6.JNS132285
Maldonado IL, Moritz-Gasser S, de Champfleur NM, Bertram L, Moulinié G, Duffau H (2011) Surgery for gliomas involving the left inferior parietal lobule: new insights into the functional anatomy provided by stimulation mapping in awake patients. J Neurosurg 115(4):770–779. https://doi.org/10.3171/2011.5.JNS112
Maya-Vetencourt JF, Pizzorusso T (2013) Molecular mechanisms at the basis of plasticity in the developing visual cortex: epigenetic processes and gene programs. J Exp Neurosci 7:75–83. https://doi.org/10.4137/JEN.S12958
Mazerand E, Le Renard M, Hue S, Lemée JM, Klinger E, Menei P (2017) Intraoperative subcortical electrical mapping of the optic tract in awake surgery using a virtual reality headset. World Neurosurg 97:424–430. https://doi.org/10.1016/j.wneu.2016.10.031
Nakajima R, Kinoshita M, Nakada M (2020) Motor functional reorganization is triggered by tumor infiltration into the primary motor area and repeated surgery. Front Hum Neurosci 14:327. https://doi.org/10.3389/fnhum.2020.00327
Nakajima R, Kinoshita M, Okita H, Yahata T, Matsui M, Nakada M (2018) Neural networks mediating high-level mentalizing in patients with right cerebral hemispheric gliomas. Front Behav Neurosci 12:33. https://doi.org/10.3389/fnbeh.2018.00033
Nakajima R, Kinoshita M, Okita H, Yahata T, Nakada M (2019) Glioma surgery under awake condition can lead to good independence and functional outcome excluding deep sensation and visuospatial cognition. Neurooncol Pract 6(5):354–363. https://doi.org/10.1093/nop/npy054
Nguyen HS, Sundaram SV, Mosier KM, Cohen-Gadol AA (2011) A method to map the visual cortex during an awake craniotomy. J Neurosurg 114(4):922–926. https://doi.org/10.3171/2010.11.JNS101293
Papageorgiou E, Hardiess G, Schaeffel F, Wiethoelter H, Karnath HO, Mallot H, Schoenfisch B, Schiefer U (2007) Assessment of vision-related quality of life in patients with homonymous visual field defects. Graefes Arch Clin Exp Ophthalmol 245(12):1749–1758. https://doi.org/10.1007/s00417-007-0644-z
Papanikolaou A, Keliris GA, Papageorgiou TD, Shao Y, Krapp E, Papageorgiou E, Stingl K, Bruckmann A, Schiefer U, Logothetis NK, Smirnakis SM (2014) Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects. Proc Natl Acad Sci U S A 111(16):E1656–E1665. https://doi.org/10.1073/pnas.1317074111
Penfield W, Rasmussen T (1950) The cerebral cortex of man: a clinical study of localization of function. MacMillan Company, New York
Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, Thiebaut de Schotten M (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221(3):1751–1766. https://doi.org/10.1007/s00429-015-1001-3
Sabel BA, Thut G, Haueisen J, Henrich-Noack P, Herrmann CS, Hunold A, Kammer T, Matteo B, Sergeeva EG, Waleszczyk W, Antal A (2020) Vision modulation, plasticity and restoration using non-invasive brain stimulation - an IFCN-sponsored review. Clin Neurophysiol 131(4):887–911. https://doi.org/10.1016/j.clinph.2020.01.008
Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358(1):18–27. https://doi.org/10.1056/NEJMoa067819
Shahar T, Korn A, Barkay G, Biron T, Hadanny A, Gazit T, Nossek E, Ekstein M, Kesler A, Ram Z (2018) Elaborate mapping of the posterior visual pathway in awake craniotomy. J Neurosurg 128(5):1503–1511. https://doi.org/10.3171/2017.2.JNS162757
Shinoura N, Suzuki Y, Yamada R, Kodama T, Takahashi M, Yagi K (2006) Restored activation of primary motor area from motor reorganization and improved motor function after brain tumor resection. AJNR Am J Neuroradiol 27(6):1275–1282
Tate MC, Herbet G, Moritz-Gasser S, Tate JE, Duffau H (2014) Probabilistic map of critical functional regions of the human cerebral cortex: Broca’s area revisited. Brain 137(10):2773–2782. https://doi.org/10.1093/brain/awu168
Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402(6760):421–425. https://doi.org/10.1038/46574
Winston GP, Daga P, White MJ, Micallef C, Miserocchi A, Mancini L, Modat M, Stretton J, Sidhu MK, Symms MR, Lythgoe DJ, Thornton J, Yousry TA, Ourselin S, Duncan JS, McEvoy AW (2014) Preventing visual field deficits from neurosurgery. Neurology 83(7):604–611. https://doi.org/10.1212/WNL.0000000000000685
Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071–1089. https://doi.org/10.1146/annurev.neuro.24.1.1071
Funding
This work was supported by the JSPS KAKENHI (20K17923 to TI, and 20K09385 to MK).
Author information
Authors and Affiliations
Contributions
T.I. and M.K. wrote the main manuscript text and all figures. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors report no competing interests.
Ethics Approval
The approval for this study was granted by the Medical Ethics Committee of Kanazawa University (2020–032 [3359]).
Consent to Participate
Written informed consent for the use of the patient’s images was obtained from all patients in this study.
Consent to Publication
Written informed consent for the use of the patient’s images was obtained from all patients in this study.
Additional information
Handling Editor: Christoph Michel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary file1 (MP4 67396 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ichinose, T., Kinoshita, M., Nakajima, R. et al. Recovery of Visual Field After Awake Stimulation Mapping of the Optic Pathway in Glioma Patients. Brain Topogr 36, 87–98 (2023). https://doi.org/10.1007/s10548-022-00922-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-022-00922-z