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Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: an original functional atlas of the human brain
Open accessAbstract
OBJECTIVE: The structural and functional organization of brain networks subserving basic daily activities (i.e. language, visuo-spatial cognition, movement, semantics, etc.) are not completely understood to date. Here, we report the first probabilistic cortical and subcortical atlas of critical structures mediating human brain functions based on direct electrical stimulation (DES), a well-validated tool for the exploration of cerebral processing and for performing safe surgical interventions in eloquent areas. METHODS: We collected 1162 cortical and 659 subcortical DES responses during testing of 16 functional domains in 256 patients undergoing awake surgery. Spatial coordinates for each functional response were calculated, and probability distributions for the entire patient cohort were mapped onto a standardized three-dimensional brain template using a multinomial statistical analysis. In addition, matching analyses were performed against prior established anatomy-based cortical and white matter (WM) atlases. RESULTS: The probabilistic maps for each functional domain were provided. The topographical analysis demonstrated a wide spatial distribution of cortical functional responses, while subcortical responses were more restricted, localizing to known WM pathways. These DES-derived data showed reliable matching with existing cortical and WM atlases as well as recent neuroimaging and neurophysiological data. CONCLUSIONS: We present the first integrated and comprehensive cortical-subcortical atlas of structures essential for humans' neural functions based on highly-specific DES mapping during real-time neuropsychological testing. This novel atlas can serve as a complementary tool for neuroscientists, along with data obtained from other modalities, to improve and refine our understanding of the functional anatomy of critical brain networks.
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“By combining tractography atlases with intraoperative electrical stimulation for functional mapping, researchers have constructed probabilistic atlases of white matter pathways and structural hubs that define a minimal common brain connectome with a low inter-individual variability and a low potential of post-lesional compensation (Herbet et al., 2016; Sarubbo et al., 2020).”
From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Sarubbo et al., 2020
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“Recent improvements in connectomic data has also allowed others to expand the clinical utility of DES in identifying critical hubs on an individualized basis (89, 102).”
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“Recently more evidence derived from intraoperative stimulation mapping and MEG connectivity studies was published on the outstanding importance of certain functional nodes within the cortico-subcortical networks to preserve neurological functioning (Lee et al., 2020; Sarubbo et al., 2020).”
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InfluentialSelf-citationMiddle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
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Self-citationElectrical Stimulation Mapping of Brain Function: A Comparison of Subdural Electrodes and Stereo-EEG
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“This is particularly relevant with SEEG because it allows direct stimulation of white matter containing axonal pathways (Sarubbo et al., 2020).”
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“In clinical prac‐ tice, this novel concept led to a paradigmatic shift, that is, to achieve a surgical resection up to the identification of the neural circuits critical for brain processing identified by DES [67], and not according to the data provide by neuroimaging, which underestimates gli‐ oma infiltration.”
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“critical neural networks (Sarubbo et al., 2020), as well as atlases of potentials and limitations”
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Self-citationIntegrating direct electrical brain stimulation with the human connectome
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“Furthermore, DES offers two major interests in comparison with the commonly used FNI to study the human connectome.”
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Recent Advances in the Diagnosis and Treatment of Brain Tumors
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“One group with extensive experience in this area has generated a probabilistic atlas of numerous functional perturbations across sensorimotor and language domains throughout the brain (Sarubbo et al., 2020).”
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“Both the mMTG and vPrG mirror the pattern of higher error rates of the LH and align with findings from nTMS [6,81] and intraoperative DES [68,77,80].”
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“Second, the intraoperative pictures of the surgical field were used as a control to navigation to confirm the exact location of the eloquent spots as described by other authors [64,81].”
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“Furthermore, a more diffuse pattern of the tumor, with a wider invasion of the white matter tracts, is correlated with more severe deterioration due to the low plastic potential of axonal fibers [27,28].”
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Where is the speech production area? Evidence from direct cortical electrical stimulation mapping
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Self-citationPreoperative assessment of eloquence in neurosurgery: a systematic review
Rammeloo, E., Schouten, J., Krikour, K., Bos, E., Berger, M. S., Nahed, B., Vincent, A., & Gerritsen, J. (2023) · Journal of Neuro-Oncology · doi:10.1007/s11060-023-04509-x · Cited by 11
Zhu, W., Deng, S., Jiang, H.-L., Zhang, J.-Y., Li, B.-X., Liu, W., Jia, Q., & Meng, Z. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1140588 · Cited by 11
“In the inferior frontal gyrus, Broca’s area consists of the perisylvian and deltoid cortices, including Brodmann’s area 44 and 45, and is responsible for language production planning and execution, coordinated with posterior parietal and temporal areas through specific bidirectional fiber tracts (Indefrey and Levelt,…”
BackgroundSubject-Specific Automatic Reconstruction of White Matter Tracts
Meesters, S. P. L., Landers, M., Rutten, G., & Florack, L. (2023) · Journal of digital imaging · doi:10.1007/s10278-023-00883-0 · Cited by 11
“An approach that has emerged in recent years, and potentially could be useful for tuning tractography results in patients, is comparing the results of tractography to intraoperative electrical stimulation mapping [58–60].”
ResultDuffau, H. (2022) · Frontiers in Surgery · doi:10.3389/fsurg.2021.824003 · Cited by 11
“Indeed, despite mechanisms of neural reconfiguration which may be elicited by slow-growing LGG (29), such a potential of neuroplasticity is very limited at the level of the white matter connectivity, thus with a high risk of permanent deficit in the event of tracts injury (16, 30, 31).”
BackgroundSelf-citationPallud, J., Roux, A., Trancart, B., Peeters, S. M., Moiraghi, A., Edjlali, M., Oppenheim, C., Varlet, P., Chrétien, F., Dhermain, F., et al. (2021) · Neurosurgery · doi:10.1093/neuros/nyab255 · Cited by 11
Sellier, A., Moritz-Gasser, S., Lemaître, A.-L., Herbet, G., & Duffau, H. (2020) · Journal of Neurosurgery · doi:10.3171/2020.6.jns201071 · Cited by 11
Self-citationFunctional anatomy and topographical organization of the frontotemporal arcuate fasciculus
Basile, G. A., Nozais, V., Quartarone, A., Giustiniani, A., Ielo, A., Cerasa, A., Milardi, D., Abdallah, M., de Schotten, M. T., Forkel, S. J., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-07274-3 · Cited by 10
“In keeping with these fi ndings, DES in the middle and superior temporal gyrus and peri-insular white matter results in word deafness and phonemic paraphasia 18,66 – 68 , strengthening the hypothesis that the ventral AF may be involved in sensory and motor phonological processes.”
Roelofs, A. (2024) · Brain Structure and Function · doi:10.1007/s00429-024-02785-5 · Cited by 13
“Marchina et al. and Wang et al. (2013) did not specify the nature of the errors, but it is likely that they were mainly phonological errors, as observed with direct electrical stimulation of the AF (Giampiccolo and Duffau 2022; Sarubbo et al. 2020).”
White matter tracts contribute selectively to cognitive functioning in patients with glioma
Andreoli, M., Mackie, M., Aaby, D., & Tate, M. C. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1221753 · Cited by 10
Self-citationOncological and functional neurosurgery: Perspectives for the decade regarding diffuse gliomas
Duffau, H. (2023) · Revue Neurologique · doi:10.1016/j.neurol.2023.01.724 · Cited by 12
Self-citationDynamics in cognition and health-related quality of life in grade 2 and 3 gliomas after surgery
Wettervik, T. S., Munkhammar, Å. A., Jemstedt, M., Ersson, M., Latini, F., Ryttlefors, M., & Zetterling, M. (2022) · Acta Neurochirurgica · doi:10.1007/s00701-022-05408-2 · Cited by 11
Viganó, L., Howells, H., Fornia, L., Rossi, M., Nibali, M. C., Puglisi, G., Leonetti, A., Simone, L., Bello, L., & Cerri, G. (2021) · Cortex; a journal devoted to the study of the nervous system and behavior · doi:10.1016/j.cortex.2021.01.005 · Cited by 10
Kumar, P. R., Jha, R. K., & Katti, A. P. (2023) · Acta Neurologica Belgica · doi:10.1007/s13760-023-02170-9 · Cited by 13
“Deconvolution of the dMRI signal measured on the streamlines is similar in LiFE [33], COMMIT [15, 16, 38], COMMIT 2 [37], and COMMIT2tree [31] utilising traditional multicompartment models [32] assign a single contribution, or "weight," to each of them.”
InfluentialGobbo, M., de Pellegrin, S., Bonaudo, C., Semenza, C., della Puppa, A., & Salillas, E. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107727 · Cited by 9
Li, Q., Pasquini, L., Ferraro, G. D., Gene, M. N., Peck, K. K., Makse, H. A., & Holodny, A. I. (2021) · Scientific Reports · doi:10.1038/s41598-021-90151-4 · Cited by 16
Zigiotto, L., Venturini, R., Coletta, L., Venturini, M., Monte, D. D., Vavassori, L., Corsini, F., Annicchiarico, L., Avesani, P., Papagno, C., et al. (2025) · Neurosurgery · doi:10.1227/neu.0000000000003591 · Cited by 8
“15-21 However, not all patients can undergo AwS and not all cognitive functions can be monitored during surgery, 22-25 such as attention.”
Self-citationSauvageot, S., Boetto, J., & Duffau, H. (2023) · Journal of neurosurgery · doi:10.3171/2023.2.jns222755 · Cited by 13
Self-citationPatient-reported quality of life in grade 2 and 3 gliomas after surgery, can we do more?
Wettervik, T., Ersson, M., Latini, F., Ryttlefors, M., & Zetterling, M. (2022) · Clinical neurology and neurosurgery (Dutch-Flemish ed. Print) · doi:10.1016/j.clineuro.2022.107175 · Cited by 8
“The tumors were considered eloquent in case of infiltration of the white matter pathways in the “minimal common brain” (inferior fronto-occipital fascicle (IFOF), arcuate fasciculus (AF), corticospinal tract (CST), and optic radiation (OR)) [23,24].”
BackgroundOhlerth, A., Bastiaanse, R., Negwer, C., Sollmann, N., Schramm, S., Schröder, A., & Krieg, S. M. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.748274 · Cited by 11
“The dorsal stream’s main function in phonological processing, typically seen in induced phonological errors through stimulation of the AF, is mostly found in the LH (Silva and Citterio, 2017; Sarubbo et al., 2020).”
BackgroundMethodInfluentialMorales, H. (2021) · Seminars in Ultrasound CT and MRI · doi:10.1053/j.sult.2021.07.005 · Cited by 9
Bifurcation and Oscillations of a Multi-ring Coupling Neural Network with Discrete Delays
Zhou, S., Xiao, M., Wang, L., & Cheng, Z.-S. (2021) · Cognitive Computation · doi:10.1007/s12559-021-09920-y · Cited by 8
Delineation of organs at risk in radiotherapy and perspectives.
Eber, J., Bockel, S., Antoni, D., Khamphan, C., Noël, G., & Fèvre, C. L. (2025) · Cancer Radiothérapie · doi:10.1016/j.canrad.2025.104758 · Cited by 7
Rofes, A., D'Agata, F., Guerrini, F., & Spena, G. (2024) · Journal of Neurosurgery · doi:10.3171/2023.10.jns231493 · Cited by 7
Structural networking of the developing brain: from maturation to neurosurgical implications
BENEDICTIS, A. D., Rossi‐Espagnet, M. C., Palma, L. D., Sarubbo, S., & Marras, C. E. (2023) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2023.1242757 · Cited by 11
Self-citationDuffau, H. (2023) · Neurosurgery · doi:10.1227/neu.0000000000002508 · Cited by 7
Self-citationZhang, J., Yao, Y., Wu, J., Rolls, E. T., Sun, C., Bu, L., Lu, J., Lin, C., Feng, J., Mao, Y. Q., et al. (2022) · Human Brain Mapping · doi:10.1002/hbm.26161 · Cited by 7
“However, the two indirect effects through the mediators-damage in MTG or ITG cortices-were significant elicit phonological error without disruption of comprehension further supported the above statement (Corina et al., 2010; Sarubbo et al., 2019).”
ResultThe connectivity-based parcellation of the angular gyrus: fiber dissection and MR tractography study
Yakar, F., Çeltikçi, P., Doğruel, Y., Egemen, E., & Güngör, A. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02555-1 · Cited by 7
“In a recent study (Sarubbo et al. 2020), human neural functions, cortical and subcortical structures were evaluated by real-time neurophysiological testing.”
BackgroundTractography in brain tumor surgery: current clinical impact and future challenges
Sarubbo, S., Vergani, F., & Yang, J. Y. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-02956-y · Cited by 6
“…fasciculus, inferior fronto-occipital fasciculus and inferior longitudinal fascicle, subserving in different modalities of language process - ing (Sarubbo et al. 2020 ) superior longitudinal fascicle and frontal-aslant tract, crucial for language and motor planning (Zigiotto et al. 2020 ;…”
Self-citationValdes, P. A., Ng, S., Bernstock, J., & Duffau, H. (2023) · Acta Neurochirurgica · doi:10.1007/s00701-023-05626-2 · Cited by 6
Self-citationBala, A., Olejnik, A., Dziedzic, T., Piwowarska, J., Podgórska, A., & Marchel, A. (2023) · Journal of Neuropsychology · doi:10.1111/jnp.12311 · Cited by 6
Extended testing for cognition: has awake brain mapping moved to the next level?
Samandouras, G. (2021) · Acta Neurochirurgica · doi:10.1007/s00701-021-05010-y · Cited by 6
“Fortunately, a wealth of initial DES data is emerging from high-quality cognitive studies [22, 27, 32].”
BackgroundInfluentialDEBATE: is tractography accurate enough to be used to inform surgery?
Vergani, F., Sarubbo, S., & Yang, J. Y. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-02948-y · Cited by 5
Self-citationMore widespread functionality of posterior language area in patients with brain tumors
Nakajima, R., Osada, T., Kinoshita, M., Ogawa, A., Okita, H., Konishi, S., & Nakada, M. (2024) · Human Brain Mapping · doi:10.1002/hbm.26801 · Cited by 5
“The types of positive responses in the naming task included anomia, perseveration, phonemic aphasia, repetition disorder, and semantic aphasia (Leonard et al., 2019; Sarubbo et al., 2020).”
BackgroundMethodFahlström, M., Mirza, S., Munkhammar, Å. A., Zetterling, M., & Latini, F. (2024) · Brain Sciences · doi:10.3390/brainsci14030213 · Cited by 5
“The mechanisms of cortical–subcortical plasticity at the individual level, with important anatomical-functional variability, are not fully understood [13–15].”
BackgroundMethodZigiotto, L., Amorosino, G., Saviola, F., Jovicich, J., Annicchiarico, L., Rozzanigo, U., Olivetti, E., Avesani, P., & Sarubbo, S. (2023) · Journal of Neuropsychology · doi:10.1111/jnp.12339 · Cited by 5
Self-citation
Metadata
- Authors
- Sarubbo, S., Tate, M., De Benedictis, A., Merler, S., Moritz-Gasser, S., Herbet, G., & Duffau, H.
- Affiliations
- Provincia Autonoma di Trento (IT)
- Northwestern University (US)
- Fondazione Bruno Kessler (IT)
- Inserm (FR)
- Corresponding author
- Sarubbo, Silvio
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2020-01
- Volume
- 205
- Pages
- 116237
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC7217287
- OpenAlex
- W2981249254
- Cited by
- 206
- References
- 81
- Citations by year
- 2026: 22 · 2025: 35 · 2024: 18 · 2023: 35 · 2022: 35 · 2021: 41 · 2020: 18
- FWCI
- 15.87
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- NeuroImage (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Iris (University of Trento) (submittedVersion, cc-by-nc-nd)
- HAL (submittedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- National Center for Advancing Translational Sciences (KL2TR001424, MT)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Keywords
- direct electrical stimulation, cortical hubs, white matter tracts, subcortical structures, awake craniotomy, eloquent brain areas, probabilistic mapping, brain networks, language, visuospatial cognition, movement, semantics, neurosurgical planning
- MeSH terms
- Adult, Atlases as Topic, Brain Mapping, Cerebral Cortex, Electric Stimulation, Humans, Magnetic Resonance Imaging, Neural Pathways, Neurosurgical Procedures, Preoperative Period, White Matter
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