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01-03-2021 | Glioma | Original Article

New insights into the anatomo-functional architecture of the right sagittal stratum and its surrounding pathways: an axonal electrostimulation mapping study

Authors: David Hassanein Berro, Guillaume Herbet, Hugues Duffau

Published in: Brain Structure and Function | Issue 2/2021

Abstract

The sagittal stratum (SS) is a large sheet-like structure where major axonal fiber tracts cross, though its anatomical delineations are still debated. Here we investigated the poorly studied anatomo-functional organization of the right SS using direct electrical stimulation (DES) in patients undergoing wide-awake surgery for a cerebral glioma. Seventeen patients were included. There were six males, the mean age was 38 years old. One patient underwent surgery twice. Fourteen patients were right-handed and one was ambidextrous. Behavior tasks were used to monitor online the patients’ functions during DES, including visual and somesthetic processes, semantics, language, spatial and social cognition. Beyond the cortical DES, the mapping of axonal pathways evoked various functional responses. At the level of the core of the right SS, there were visual disturbances, visual hemi-agnosia, semantic paraphasia, left spatial neglect, confusion and comprehension difficulties, anomia, and mentalizing disturbances. At the level of the surrounding axonal pathways, there were left spatial neglect, anomia, vertigo, dysesthesia, and hearing disturbances. Our functionally defined three-dimensional map indicates that this complex region has a multilayered functional architecture, and supports an organization founded on two anatomical systems: a core system formed by the optic radiations, inferior longitudinal fasciculus, and inferior fronto-occipital fasciculus, and a peripheral one composed of surrounding or intersecting white matter tracts, including the superior longitudinal fasciculus/arcuate fasciculus, thalamocortical radiations, auditory radiations, and parieto-insular vestibular system. These results should prompt neurosurgeons to achieve awake DES mapping within the right SS because of the likelihood of causing multiple and irreversible structural disconnections.

Baron-Cohen S, Wheelwright S, Hill J et al (2001) The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry Allied Discip 42:241–251. https://doi.org/10.1017/S0021963001006643CrossRef

Benson DF, Davis RJ, Snyder BD (1988) Posterior Cortical Atrophy. Arch Neurol 45:789–793. https://doi.org/10.1001/archneur.1988.00520310107024CrossRefPubMed

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.2008.05.004CrossRefPubMed

Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain 126:2093–2107. https://doi.org/10.1093/brain/awg203CrossRefPubMed

Chan-Seng E, Moritz-Gasser S, Duffau H (2014) Awake mapping for low-grade gliomas involving the left sagittal stratum: anatomofunctional and surgical considerations. J Neurosurg 120:1069–1077. https://doi.org/10.3171/2014.1.jns132015CrossRefPubMed

Coello AF, Duvaux S, De Benedictis A et al (2013) Involvement of the right inferior longitudinal fascicle in visual hemiagnosia: a brain stimulation mapping study—case report. J Neurosurg 118:202–205. https://doi.org/10.3171/2012.10.JNS12527CrossRef

Dejerine J, Dejerine-Klumpke A (1895) Anatomie des centres nerveux. Rueff et Cie, Paris

Di Carlo DT, Benedetto N, Duffau H et al (2019) Microsurgical anatomy of the sagittal stratum. Acta Neurochir (Wien). https://doi.org/10.1007/s00701-019-04019-8CrossRef

Duffau H (2009) A personal consecutive series of surgically treated 51 cases of insular WHO Grade II glioma: advances and limitations - Clinical article. J Neurosurg 110:696–708. https://doi.org/10.3171/2008.8.JNS08741CrossRefPubMed

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.2015.51CrossRefPubMed

Duffau H, Capelle L, Sichez N et al (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125:199–214. https://doi.org/10.1093/brain/awf016CrossRefPubMed

Duffau H, Velut S, Mitchell MC et al (2004) Intra-operative mapping of the subcortical visual pathways using direct electrical stimulations. Acta Neurochir (Wien) 146:265–270. https://doi.org/10.1007/s00701-003-0199-7CrossRef

Duffau H, Gatignol P, Mandonnet E et al (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797–810. https://doi.org/10.1093/brain/awh423CrossRefPubMed

Duffau H, Leroy M, Gatignol P (2008) Cortico-subcortical organization of language networks in the right hemisphere: an electrostimulation study in left-handers. Neuropsychologia 46:3197–3209. https://doi.org/10.1016/j.neuropsychologia.2008.07.017CrossRefPubMed

Foulon C, Cerliani L, Kinkingnéhun S et al (2018) Advanced lesion symptom mapping analyses and implementation as BCBtoolkit. Gigascience 7:1–17CrossRef

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: clinical article. J Neurosurg 117:466–473. https://doi.org/10.3171/2012.6.JNS111981CrossRefPubMed

Herbet G, Lafargue G, Moritz-Gasser S et al (2015) Interfering with the neural activity of mirror-related frontal areas impairs mentalistic inferences. Brain Struct Funct 220:2159–2169. https://doi.org/10.1007/s00429-014-0777-xCrossRefPubMed

Herbet G, Moritz-Gasser S, Duffau H (2017a) Direct evidence for the contributive role of the right inferior fronto-occipital fasciculus in non-verbal semantic cognition. Brain Struct Funct 222:1597–1610. https://doi.org/10.1007/s00429-016-1294-xCrossRefPubMed

Herbet G, Yordanova YN, Duffau H (2017b) Left spatial neglect evoked by electrostimulation of the right inferior fronto-occipital fasciculus. Brain Topogr 30:747–756. https://doi.org/10.1007/s10548-017-0574-yCrossRefPubMed

Herbet G, Zemmoura I, Duffau H (2018) Functional anatomy of the inferior longitudinal fasciculus: from historical reports to current hypotheses. Front Neuroanat 12:1–15. https://doi.org/10.3389/fnana.2018.00077CrossRef

Herbet G, Lemaitre AL, Moritz-Gasser S et al (2019) The antero-dorsal precuneal cortex supports specific aspects of bodily awareness. Brain 142:2207–2214. https://doi.org/10.1093/brain/awz179CrossRefPubMed

Hosoya T, Adachi M, Yamaguchi K, Haku T (1998) MRI anatomy of white matter layers around the trigone of the lateral ventricle. Neuroradiology 40:477–482. https://doi.org/10.1007/s002340050629CrossRefPubMed

Howard D, Patterson K (1992) Pyramids and palm trees: a test of semantic access. Edmonds, Suffolk, UK Thames Val Test Co

Hua K, Zhang J, Wakana S et al (2008) Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage 39:336–347. https://doi.org/10.1016/j.neuroimage.2007.07.053CrossRefPubMed

Jellison BJ, Field AS, Medow J et al (2004) Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. Am J Neuroradiol 25:356–369PubMed

Jenkinson M, Beckmann CF, Behrens TEJ et al (2012) FSL. Neuroimage 62:782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015CrossRefPubMed

Klingler J, Ludwig E (1956) Atlas Cerebri Humani

Krolak-Salmon P, Guenot M, Tiliket G et al (2000) Anatomy of optic nerve radiations as assessed by static perimetry and MRI after tailored temporal lobectomy. Br J Ophthalmol 84:884–889. https://doi.org/10.1136/bjo.84.8.884CrossRefPubMedPubMedCentral

Mandonnet E, Gatignol P, Duffau H (2009) Evidence for an occipito-temporal tract underlying visual recognition in picture naming. Clin Neurol Neurosurg 111:601–605. https://doi.org/10.1016/j.clineuro.2009.03.007CrossRefPubMed

Martino J, Brogna C, Robles SG et al (2010) Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46:691–699. https://doi.org/10.1016/j.cortex.2009.07.015CrossRefPubMed

Metz-Lutz M, Kremin H, Deloche G (1991) Standardisation d’un test de dénomination orale: contrôle des effets de l’âge, du sexe et du niveau de scolarité chez les sujets adultes normaux. Rev Neuropsychol 1:73–95

Migliaccio R, Agosta F, Scola E et al (2012) Ventral and dorsal visual streams in posterior cortical atrophy: a DT MRI study. Neurobiol Aging 33:2572–2584. https://doi.org/10.1016/j.neurobiolaging.2011.12.025CrossRefPubMedPubMedCentral

Mori S, Oishi K, Jiang H et al (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40:570–582. https://doi.org/10.1016/j.neuroimage.2007.12.035CrossRefPubMedPubMedCentral

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.2013.06.007CrossRefPubMed

Mowinckel AM, Vidal-Piñeiro D (2019) Visualisation of Brain Statistics with R-packages ggseg and ggseg3d

Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. https://doi.org/10.1016/0028-3932(71)90067-4CrossRef

Ortibus E, Verhoeven J, Sunaert S et al (2012) Integrity of the inferior longitudinal fasciculus and impaired object recognition in children: a diffusion tensor imaging study. Dev Med Child Neurol 54:38–43. https://doi.org/10.1111/j.1469-8749.2011.04147.xCrossRefPubMed

Rech F, Herbet G, Moritz-Gasser S, Duffau H (2014) Disruption of bimanual movement by unilateral subcortical electrostimulation. Hum Brain Mapp 35:3439–3445. https://doi.org/10.1002/hbm.22413CrossRefPubMed

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/s00429-015-1129-1CrossRefPubMed

Rojkova K, Volle E, Urbanski M et al (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221:1751–1766. https://doi.org/10.1007/s00429-015-1001-3CrossRefPubMed

Rolland A, Herbet G, Duffau H (2018) Awake surgery for gliomas within the right inferior parietal lobule: new insights into the functional connectivity gained from stimulation mapping and surgical implications. World Neurosurg 112:e393–e406. https://doi.org/10.1016/j.wneu.2018.01.053CrossRefPubMed

Sachs H (1892) Das Hemisphärenmark des menschlichen Grosshirns: Der Hinterhauptlappen/von Heinrich Sachs

Sarubbo S, De Benedictis A, Merler S et al (2015a) Towards a functional atlas of human white matter. Hum Brain Mapp 36:3117–3136. https://doi.org/10.1002/hbm.22832CrossRefPubMedPubMedCentral

Sarubbo S, De Benedictis A, Milani P et al (2015b) The course and the anatomo-functional relationships of the optic radiation: a combined study with “post mortem” dissections and “in vivo” direct electrical mapping. J Anat 226:47–59. https://doi.org/10.1111/joa.12254CrossRefPubMed

Sarubbo S, Tate M, De Benedictis A et al (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.2019.116237CrossRefPubMed

Schucht P, Moritz-Gasser S, Herbet G et al (2013) Subcortical electrostimulation to identify network subserving motor control. Hum Brain Mapp 34:3023–3030. https://doi.org/10.1002/hbm.22122CrossRefPubMed

Tate MC, Herbet G, Moritz-Gasser S et al (2014) Probabilistic map of critical functional regions of the human cerebral cortex: broca’s area revisited. Brain 137:2773–2782. https://doi.org/10.1093/brain/awu168CrossRefPubMed

Thiebaut De Schotten M, Urbanski M, Duffau H et al (2005) Neuroscience: direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309:2226–2228. https://doi.org/10.1126/science.1116251CrossRefPubMed

Unger A, Alm KH, Collins JA, O’Leary JM, Olson IR (2016) Variation in white matter connectivity predicts the ability to remember faces and discriminate their emotions. J Int Neuropsychol Soc. 22(2):180–190CrossRef

Urbanski M, Thiebaut de Schotten M et al (2011) DTI-MR tractography of white matter damage in stroke patients with neglect. Exp Brain Res 208(4):491–505CrossRef

Van Essen DC, Ugurbil K, Auerbach E et al (2012) The human connectome project: a data acquisition perspective. Neuroimage 62:2222–2231CrossRef

Yeh FC, Verstynen TD, Wang Y et al (2013) Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE. https://doi.org/10.1371/journal.pone.0080713CrossRefPubMedPubMedCentral

Yeh FC, Panesar S, Fernandes D et al (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.2018.05.027CrossRefPubMedPubMedCentral

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

Title: New insights into the anatomo-functional architecture of the right sagittal stratum and its surrounding pathways: an axonal electrostimulation mapping study
Authors: David Hassanein Berro
Guillaume Herbet
Hugues Duffau
Publication date: 01-03-2021
Publisher: Springer Berlin Heidelberg
Keywords: Glioma
Glioma
Glioma
Published in: Brain Structure and Function / Issue 2/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-020-02186-4

At a glance: The STEP trials

Springer Medicine

New insights into the anatomo-functional architecture of the right sagittal stratum and its surrounding pathways: an axonal electrostimulation mapping study

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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