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 map** 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 map** within the right SS because of the likelihood of causing multiple and irreversible structural disconnections.
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References
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/S0021963001006643
Benson DF, Davis RJ, Snyder BD (1988) Posterior Cortical Atrophy. Arch Neurol 45:789–793. https://doi.org/10.1001/archneur.1988.00520310107024
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
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/awg203
Chan-Seng E, Moritz-Gasser S, Duffau H (2014) Awake map** 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.jns132015
Coello AF, Duvaux S, De Benedictis A et al (2013) Involvement of the right inferior longitudinal fascicle in visual hemiagnosia: a brain stimulation map** study—case report. J Neurosurg 118:202–205. https://doi.org/10.3171/2012.10.JNS12527
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/s00701-019-04019-8
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.JNS08741
Duffau H (2015) Stimulation map** of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11:255–265. https://doi.org/10.1038/nrneurol.2015.51
Duffau H, Capelle L, Sichez N et al (2002) Intraoperative map** of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125:199–214. https://doi.org/10.1093/brain/awf016
Duffau H, Velut S, Mitchell MC et al (2004) Intra-operative map** of the subcortical visual pathways using direct electrical stimulations. Acta Neurochir (Wien) 146:265–270. https://doi.org/10.1007/s00701-003-0199-7
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/awh423
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.2008.07.017
Foulon C, Cerliani L, Kinkingnéhun S et al (2018) Advanced lesion symptom map** analyses and implementation as BCBtoolkit. Gigascience 7:1–17
Gras-Combe G, Moritz-Gasser S, Herbet G, Duffau H (2012) Intraoperative subcortical electrical map** 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.JNS111981
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-x
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-x
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-y
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.2018.00077
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/awz179
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/s002340050629
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.2007.07.053
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 25:356–369
Jenkinson M, Beckmann CF, Behrens TEJ et al (2012) FSL. Neuroimage 62:782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015
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.84.8.884
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.2009.03.007
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.2009.07.015
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.2011.12.025
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.2007.12.035
Moritz-Gasser S, Herbet G, Duffau H (2013) Map** 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
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)90067-4
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.x
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.22413
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
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/s00429-015-1001-3
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 map** and surgical implications. World Neurosurg 112:e393–e406. https://doi.org/10.1016/j.wneu.2018.01.053
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.22832
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 map**. J Anat 226:47–59. https://doi.org/10.1111/joa.12254
Sarubbo S, Tate M, De Benedictis A et al (2020) Map** 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
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.22122
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/awu168
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.1116251
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):180–190
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):491–505
Van Essen DC, Ugurbil K, Auerbach E et al (2012) The human connectome project: a data acquisition perspective. Neuroimage 62:2222–2231
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.0080713
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.2018.05.027
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
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Berro, D.H., Herbet, G. & Duffau, H. New insights into the anatomo-functional architecture of the right sagittal stratum and its surrounding pathways: an axonal electrostimulation map** study. Brain Struct Funct 226, 425–441 (2021). https://doi.org/10.1007/s00429-020-02186-4
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DOI: https://doi.org/10.1007/s00429-020-02186-4