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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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“Thus DES has allowed the computation of cortical and subcortical probabilistic functional atlases of the human brain that are consistent with the current neuroscience literature (Ius et al., 2011; Tate et al., 2014; Sarubbo et al., 2015a; Herbet et al., 2016).”
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A framework for focal and connectomic mapping of transiently disrupted brain function
Elmalem, M. S., Moody, H., Ruffle, J., de Schotten, M. T., Haggard, P., Diehl, B., Nachev, P., & Jha, A. (2022) · Communications Biology · doi:10.1038/s42003-023-04787-1 · Cited by 5
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Vasileiadi, M., Schuler, A.-L., Woletz, M., Witz, V., Grosshagauer, S., Coetzee, J., & Tik, M. (2025) · Brain Stimulation · doi:10.1016/j.brs.2025.103010 · Cited by 4
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Sarubbo, S., Vavassori, L., Zigiotto, L., Corsini, F., Annicchiarico, L., Rozzanigo, U., & Avesani, P. (2024) · Brain Science · doi:10.3390/brainsci14121232 · Cited by 4
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“…and subcortical white matter information regarding the localization of specific brain function (Vigan ` o et al. 2022; Puglisi et al., 2019; Sarubbo et al., 2020), allowing a highly comprehensive mapping finally impacting on survival and quality of life of neuro-oncological patients (Rossi…”
InfluentialRammohan, N., Ho, A., Saxena, M. V., Bajaj, A., Kruser, T., Horbinski, C., Korutz, A., Tate, M., & Sachdev, S. (2022) · Journal of Neuro-Oncology · doi:10.1007/s11060-022-04018-3 · Cited by 4
“Thus far, white matter connectivity as evaluated by MR-DTI has not been extensively explored in the context of glioma progression, even though it has been utilized for pre-operative planning for at least a decade [14, 23, 24, 26, 27].”
BackgroundSelf-citationDuffau, H. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.705135 · Cited by 4
Self-citationPreoperative Brain Mapping Predicts Language Outcomes After Eloquent Tumor Resection
Muir, M. T., Noll, K. R., Prinsloo, S., Michener, H., Traylor, J. I., Kumar, V. A., Ene, C., Ferguson, S. D., Liu, H., Weinberg, J. S., et al. (2025) · Human Brain Mapping · doi:10.1002/hbm.70340 · Cited by 3
Coletta, L., Avesani, P., Zigiotto, L., Venturini, M., Annicchiarico, L., Vavassori, L., Jamadar, S., Liang, E., Hansen, J. Y., Mišić, B., et al. (2025) · Communications Medicine · doi:10.1038/s43856-025-01121-0 · Cited by 3
Self-citationA probabilistic functional atlas based on extraoperative electrocortical stimulation mappingPreprint
Michalak, A., Yu, L.-Y., Khalilian-Gourtani, A., Seedat, A., Kazl, C., Morrison, C., Resch, Z., Doyle, W. K., Rozman, P. A., Devinsky, O., et al. (2025) · bioRxiv · doi:10.1101/2025.09.15.676264 · Cited by 3
“In contrast, prior DES studies reported disruption maps by calculating the density of positive sites or by reporting the propor-364 tion of patients with at least one positive response [3, 5, 6].”
Locating eloquent sites identified during brain tumor intraoperative mapping on reference MRI atlas
Elia, A., Roux, A., Debacker, C., Charron, S., Simboli, G., Moiraghi, A., Trancart, B., Dezamis, E., Muto, J., Chrétien, F., et al. (2025) · Communications Medicine · doi:10.1038/s43856-025-00834-6 · Cited by 3
Classifying Schizophrenia Using Functional MRI and Investigating Underlying Functional Phenomena.
Liu, Y., Wan, B., Liu, Z.-X., Zhang, S., Liu, P., Ding, N., Wang, Y., Dong, J., Ahmad, M., & Zhang, H. (2025) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2025.111279 · Cited by 3
“The MFG is a critical connection point for the dorsal speech pathway and the ventral semantic pathway (Sarubbo et al., 2020; Chang et al., 2015).”
Kram, L., Schroeder, A., Meyer, B., Krieg, S., & Ille, S. (2024) · Brain Structure and Function · doi:10.1007/s00429-024-02787-3 · Cited by 3
Grey Matter Reshaping of Language-Related Regions Depends on Tumor Lateralization
Manso-Ortega, L., de Frutos-Sagastuy, L., Gisbert-Muñoz, S., Salamon, N., Qiao, J., Walshaw, P., Quiñones, I., & Połczyńska, M. M. (2023) · Cancers · doi:10.3390/cancers15153852 · Cited by 3
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Grey matter reshaping of language-related regions depends on tumor lateralization
Manso-Ortega, L., de Frutos-Sagastuy, L., Gisbert-Muñoz, S., Salamon, N., Qiao, J., Walshaw, P., Quiñones, I., & Połczyńska, M. M. (2023) · bioRxiv · doi:10.1101/2023.02.02.526219 · Cited by 3
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“Awake brain surgery, in particular, has made it possible to preserve brain function despite removing tumours near eloquent brain regions (Paldor et al., 2016; Papagno et al., 2012; Sarubbo et al., 2020; Suarez-Meade et al., 2020; Zigiotto et al., 2020).”
BackgroundChallenges in starting an awake craniotomy project in a low resource public health system.
Albuquerque, L., Diógenes, G. S., & Pessoa, F. C. (2020) · World Neurosurgery · doi:10.1016/j.wneu.2020.12.006 · Cited by 3
Sanchez, S., & Tate, M. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1648154 · Cited by 2
“…strict interpretations of the classical model in favor of bilateral probabilistic maps for anatomic epicenters for language functions, such as phonologic and semantic hubs, subserved by parallel networks, which is more practical for consideration in neurosurgical settings (9, 29, 30).”
Self-citationNakajima, R., Ogawa, A., Kinoshita, M., Osada, T., Okita, H., Konishi, S., & Nakada, M. (2025) · NeuroImage Clinical · doi:10.1016/j.nicl.2025.103860 · Cited by 2
“” The positive responses included anomia, phonemic paraphasia, semantic paraphasia, speech arrest, and anarthria (Leonard et al., 2019; Sarubbo et al., 2020).”
Gu, L., Li, S., Qu, M., & Xi, Y. (2025) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2025.111312 · Cited by 2
“Moreover, this area is crucial for both clinical and non-clinical neuroscience investigations (Fedorenko and Blank, 2020; Sarubbo et al., 2020).”
Nassihi, A., & Duffau, H. (2024) · Acta Neurochirurgica · doi:10.1007/s00701-024-06321-6 · Cited by 2
“…potential of brain reshaping is high at the level of the cortex, it is lower when the deep white matter tracts are invaded by the tumoral cells [25, 41], thus limiting the indication of reoperation(s) in the event of diffuse patterns of recurrence mainly involving the subcortical connectivity [20,…”
Self-citationElectric stimulation using stereoelectroencephalography electrodes
Russkin, V. O., Kuznetsova, A., Solovyev, V., Levov, A., Berdinov, F. B., Livshits, M., & Sandrikov, V. A. (2024) · Russian journal of neurosurgery · doi:10.17650/1683-3295-2024-26-3-144-155 · Cited by 2
Bermudez, G., Quiñones, I., Carrasco, A., Gil-Robles, S., Amoruso, L., Mandonnet, E., Carreiras, M., Catalán, G., & Pomposo, I. (2023) · Acta Neurochirurgica · doi:10.1007/s00701-023-05755-8 · Cited by 2
“The precuneus, located in the mesial aspect of the superior parietal lobule, is often considered by neurosurgeons as a non-eloquent area [14, 26].”
BackgroundZhang, J.-Q., Jiao, Z., Huang, F.-B., Wang, X., Zhou, X., Li, Q., Zhang, Y., Long, L., Su, Y., Cao, K.-X., et al. (2026) · Frontiers in Neurology · doi:10.3389/fneur.2026.1789921 · Cited by 1
A probabilistic map of motor and cognitive functions: a meta-analysis of 4325 stimulation sites
Alexandratou, A., Sefcikova, V., Elmalem, M. S., Bisschop, J., Huet, S., Samandouras, G., & Nachev, P. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-03015-2 · Cited by 1
“(Tate et al. 2014; Chang et al. 2017; Sarubbo et al. 2020; Wu et al. 2015; Zhou et al. 2021; Zacà et al. 2018 ).”
InfluentialWu, X. X., Kong, Y., & Hu, L. (2025) · Imaging Neuroscience · doi:10.1162/imag.a.972 · Cited by 1
“…is known to be a core region in face perception ( Direito et al., 2019), (3) there is evidence of a direct fiber path between the STS and the IFG ( Sarubbo et al., 2020; Suchan et al., 2014), and (4) both the IFG and the STS have been implicated as regions in the human mirror neuron system (…”
Viola, L., Moretto, M., Zigiotto, L., Tambalo, S., Annicchiarico, L., Venturini, M., Jovicich, J., & Sarubbo, S. (2025) · Neurosurgery · doi:10.1227/neu.0000000000003613 · Cited by 1
“21 This study included a probabilistic SAN atlas derived from 142 DES-positive points for speech articulation.”
Self-citationNetworks for proper versus common name retrieval: insights from causal mapping and new hypotheses
Burkhardt, E., Duffau, H., & Herbet, G. (2025) · Brain Communications · doi:10.1093/braincomms/fcaf256 · Cited by 1
“…distributed fronto-temporo-parietal cortical network is robustly supported by findings from direct electrical stimulation (DES) studies conducted intraoperatively using a picture naming task, 84-86 which particularly underscore the causal role of the posterior part of the superior temporal gyrus.”
Self-citationNeural hierarchy for coding articulatory dynamics in speech imagery and productionPreprint
Zhao, Z.-H., Wang, Z.-J., Liu, Y., Qian, Y.-K., Yin, Y., Gao, X.-W., Yuan, B.-K., Tong, S. X., Tian, X., Chen, G., et al. (2025) · bioRxiv · doi:10.1101/2025.05.27.656311 · Cited by 1
Kahana, N., Korn, A., Friedmann, N., Richetta, C., Gurevitch, G., Artzi, M., Keren, N., Ram, Z., Shahar, T., & Grossman, R. (2025) · Journal of Neurosurgery · doi:10.3171/2025.1.jns241036 · Cited by 1
Hypnosis-Assisted Awake Craniotomy for Eloquent Brain Tumors: Advantages and Pitfalls
Cossu, G., Vandenbulcke, A., Zaccarini, S., Gaudet, J. G., Hottinger, A. F., Rimorini, N., Potié, A., Beaud, V., Guerra-Lopez, U., Daniel, R. T., et al. (2024) · Cancers · doi:10.3390/cancers16091784 · Cited by 1
“Therefore, intraoperative brain stimulation, performed in an asleep or awake setting, remains the most reliable technique for safe resections within functional boundaries [12–16].”
MethodAssociation of disruption of the right posterior arcuate fasciculus with spatial neglect
Andreoli, M., Medina‐Pizarro, M., Mackie, M., & Tate, M. C. (2024) · Journal of neurosurgery · doi:10.3171/2024.1.jns232142 · Cited by 1
Self-citationShah, K., Bhartia, V., Biswas, C., Sahu, A., Shetty, P., Singh, V., Velayutham, P., Awate, S. P., & Moiyadi, A. (2024) · Neuro-Oncology Advances · doi:10.1093/noajnl/vdae020 · Cited by 1
“As a supplementary analysis, we also analyzed the TLMs and probability maps for GBMs and LGGs separately, details of which are available in Supplementary Materials 13 and 14.”
MethodLatini, F., Jakola, A., & Rudà, R. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1100972 · Cited by 1
“The mechanisms of cortical-subcortical plasticity at the individual level are not fully understood with important anatomical-functional variability (Herbet et al., 2016; Sarubbo et al., 2020).”
BackgroundPersonal space regulation is affected by unilateral temporal lesions beyond the amygdala
Dureux, A., Zigiotto, L., Sarubbo, S., Desoche, C., Farnè, A., Bolognini, N., & Hadj‐Bouziane, F. (2022) · Cerebral Cortex Communications · doi:10.1093/texcom/tgac031
Self-citationThe vertical superior longitudinal fascicle and the vertical occipital fascicle.
Mahdy-Ali, K., & Avesani, P. (2021) · Journal of Neurosurgical Sciences · doi:10.23736/s0390-5616.21.05368-6 · Cited by 1
Beyond Task: When Experience Shapes Intuition
Duffau, H. (2021) · Intraoperative Mapping of Cognitive Networks · doi:10.1007/978-3-030-75071-8_24 · Cited by 1
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“Several research groups have explored brain functioning by mapping DES-derived stimulation sites onto standardized brain templates [9,11–15].”
A neural architecture for imagined and overt speech motor dynamics
Zhao, Z., Wang, Z., Liu, Y., Qian, Y., Yin, Y., Gao, X., Yuan, B., Tong, S. X., Tian, X., Chen, G., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02456-0 · Cited by 2
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“…neuroplasticity; transactional analysis psychotherapy; therapeutic relationship; neurorehabilitation; relational neuroscience Herbet et al., 2014; Sarubbo et al., 2020) has further demonstrated that subjective experience, emotion, and cognition can be modulated through direct brain stimulation,…”
Unveiling Functional Architecture of Human Thalamus: AStereoelectroencephalography Study
Ren, L.-K., Wu, D., Xu, C.-P., Qi, L., Jin, G.-Y., Wang, X.-Y., Cheng, Y.-Y., Du, J.-L., Wang, S.-Y., Hu, D.-M., et al. (2026) · MedComm · doi:10.1002/mco2.70931
“DES mapping was largely used to refine the selection and boundaries of cortical regions that are critical for important functions in patients with brain tumors or with intractable epilepsy to avoid neurological deficits [ 26, 27 ].”
Nave, R., Ng, S., Moritz-Gasser, S., Berger, L., Mandonnet, E., Duffau, H., & Herbet, G. (2026) · NeuroImage: Clinical · doi:10.1016/j.nicl.2026.104052
“Detailed descriptions of intraoperative tasks used for functional mapping and monitoring have been published elsewhere (Sarubbo et al., 2020; Tate et al., 2014).”
Self-citationMichalak, A., Yu, L.-Y., Khalilian-Gourtani, A., Seedat, A., Kazl, C., Morrison, C., Resch, Z., Doyle, W. K., Rozman, P. A., Devinsky, O., et al. (2026) · Neurology · doi:10.1212/wnl.0000000000218215
Probabilistic Retinotopic Parcellation of the Macaque Visual CortexPreprint
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Lozano, F. E., & Martín-Fernández, J. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03158-w · Cited by 1
“…effects of subcortical stimulation are often more reproducible across patients than those of cortical stimulation, precisely because fiber bundles con - strain communication more consistently than cortical micro-topography does (Duffau et al. 2005; Moritz-Gasser et al. 2013; Sarubbo et al. 2020).”
Role and Function of the Opercula.
Zigiotto, L., & Sarubbo, S. (2026) · Journal of clinical neurophysiology · doi:10.1097/wnp.0000000000001283
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Self-citationCameron, B. M., & Durand-López, E. M. (2026) · Bilingualism Language and Cognition · doi:10.1017/s136672892610145x
Heijink, I., Jelsma, S. B., van der Salm, S. V. D., van Klink, N. V., Ferrier, C. H., Hoogteijling, S., van Asch, C. V., van Blooijs, D., & Zijlmans, M. (2026) · Clinical Neurophysiology Practice · doi:10.1016/j.cnp.2026.06.006
“Balestrini et al., Sarubbo et al. and Michalak et al. have developed functional atlases (Balestrini et al., 2015; Michalak et al., 2025; Sarubbo et al., 2020), but the center-specific workflows have impeded the next step towards a multi-center approach (Ritaccio et al., 2018).”
In Search of the "Eloquent Brain": History, Science, and Future.
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Ramírez-Ferrer, E., Noll, K. R., Sabsevitz, D., Herbet, G., Zuluaga-García, J. P., Asman, P., Connelly, K., Lavelle, L., Raty, S., Bhavsar, S., et al. (2026) · Journal of Neurosurgery · doi:10.3171/2025.12.jns252009
Self-citationSchwendner, M. J., Markwardt, O., Meyer, B., Krieg, S. M., & Ille, S. (2026) · Clinical Neurology and Neuroscience · doi:10.11648/j.cnn.20261001.15
Ng, S., Giampiccolo, D., Moritz‐Gasser, S., Herbet, G., & Duffau, H. (2026) · Journal of neurosurgery · doi:10.3171/2025.10.jns251874
Self-citationYe, L., Zhao, W., Song, W.-Q., Yang, H.-Q., Xie, H.-X., & Cao, L. (2026) · Brain Imaging and Behavior · doi:10.1007/s11682-026-01106-0
“…to the reestablishment of communication between VAN and DAN provides definite evidence for the involvement of SLF in VSN(Berro et al., 2021; Vallar et al., 2014), while tumors reveal the consequences of structural damage and the potential for recovery if damage is reversible(Sarubbo et al., 2020 ).”
Pozo, I. T., Giménez, J. L. N., Alcántara-Bernal, R., Puntas, T. D. Á., Caro, P. C., & Martín-Schrader, I. (2026) · Interdisciplinary Neurosurgery · doi:10.1016/j.inat.2026.102210
Bockel, S., El-Aichi, M., Sun, R., Benzazon, N., de-Kermenguy, F., Veres, C., Satragno, C., Bidault, F., Garcia, G., Dhermain, F., et al. (2025) · Comput. Biol. Medicine · doi:10.1016/j.compbiomed.2025.111417
Creating a Low-Cost Brain Atlas: A Step-by-Step Guide and Historical Aspects
Gosch, G. O., & de Albuquerque, L. A. D. (2025) · Brazilian Neurosurgery · doi:10.1055/s-0046-1825969
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“27,71,72 Our study also has some limitations, due to being a retrospective study.”
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Quiñones, I., Gisbert-Muñoz, S., Bermudez, G., Pomposo, I., Robles, S. G., Carreiras, M., & Amoruso, L. (2025) · Acta Neurochirurgica · doi:10.1007/s00701-025-06508-5
“Interestingly, a recent meta-analysis of lesion-symptom mapping studies [18] highlights this region's critical involvement in the early stage of word production, namely during retrieval.”
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“IFOF is related to multi-dimensional connectivity, which is currently considered to play an important role in both semantic and non-linguistic cognition (Sarubbo et al., 2020).”
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Linguistic Specificity of the Left Temporal Cortex: Intraoperative Brain Mapping Data
Novozhilova, E., Gordeyeva, E., Stupina, E., Zelenkova, V., Zhirnova, V., Zyryanov, A., Zuev, A., Pedyash, N., Bronov, O., Medyanik, I., et al. (2020) · Social Science Research Network · doi:10.2139/ssrn.3707392
“[Sarubbo et al., 2020] intraoperative brain mapping study found activations in the middle and posterior portions of the superior and middle temporal gyri, but we did only in middle portions.”
BackgroundApplication of Neuronavigation System in Neurosurgery
Lei, D.-H., Fu, D.-L., & Yuan, Y. (2020) · Advances in Clinical Medicine · doi:10.12677/acm.2020.1012447
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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