A Network-Based Approach to Glioma Surgery: Insights from Functional Neurosurgery

Simple Summary This manuscript details the literature and discussion around revolutionizing the neurosurgeon’s approach to surgery for brain tumors by conceptualizing these tumors as entities within functional networks. We hope that the work detailed herein will aid in establishing neurosurgical paradigms to optimize planning for brain tumor surgery to improve functional outcomes for all patients. Abstract The evaluation and manipulation of structural and functional networks, which has been integral to advancing functional neurosurgery, is beginning to transcend classical subspecialty boundaries. Notably, its application in neuro-oncologic surgery has stimulated an exciting paradigm shift from the traditional localizationist approach, which is lacking in nuance and optimization. This manuscript reviews the existing literature and explores how structural and functional connectivity analyses have been leveraged to revolutionize and individualize pre-operative tumor evaluation and surgical planning. We describe how this novel approach may improve cognitive and neurologic preservation after surgery and attenuate tumor spread. Furthermore, we demonstrate how connectivity analysis combined with neuromodulation techniques can be employed to induce post-operative neuroplasticity and personalize neurorehabilitation. While the landscape of functional neuro-oncology is still evolving and requires further study to encourage more widespread adoption, this functional approach can transform the practice of neuro-oncologic surgery and improve the care and outcomes of patients with intra-axial tumors.

[1]  K. Hynynen,et al.  MR-guided focused ultrasound enhances delivery of trastuzumab to Her2-positive brain metastases , 2021, Science Translational Medicine.

[2]  A. Horn,et al.  Deep Brain Stimulation: From Sweet Spots to Sweet Networks? , 2021, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[3]  H. Duffau The death of localizationism: The concepts of functional connectome and neuroplasticity deciphered by awake mapping, and their implications for best care of brain-damaged patients. , 2021, Revue neurologique.

[4]  V. Rao,et al.  Long-term brain network reorganization predicts responsive neurostimulation outcomes for focal epilepsy , 2021, Science Translational Medicine.

[5]  Bledi C. Brahimaj,et al.  Reducing the Cognitive Footprint of Brain Tumor Surgery , 2021, Frontiers in Neurology.

[6]  H. Duffau,et al.  Language recovery through a two-stage awake surgery in an aphasic patient with a voluminous left fronto-temporo-insular glioma: case report , 2021, Acta Neurochirurgica.

[7]  Bryan M. Li,et al.  Predicting optimal deep brain stimulation parameters for Parkinson’s disease using functional MRI and machine learning , 2021, Nature Communications.

[8]  G. Fink,et al.  Lesion-Function Analysis from Multimodal Imaging and Normative Brain Atlases for Prediction of Cognitive Deficits in Glioma Patients , 2021, Cancers.

[9]  Gwenn S. Smith,et al.  Brain structures and networks responsible for stimulation‐induced memory flashbacks during forniceal deep brain stimulation for Alzheimer's disease , 2021, Alzheimer's & dementia : the journal of the Alzheimer's Association.

[10]  H. Duffau Can Non-invasive Brain Stimulation Be Considered to Facilitate Reoperation for Low-Grade Glioma Relapse by Eliciting Neuroplasticity? , 2020, Frontiers in Neurology.

[11]  H. Duffau Functional Mapping before and after Low-Grade Glioma Surgery: A New Way to Decipher Various Spatiotemporal Patterns of Individual Neuroplastic Potential in Brain Tumor Patients , 2020, Cancers.

[12]  M. Sughrue,et al.  The cortical organization of language: distilling human connectome insights for supratentorial neurosurgery. , 2020, Journal of neurosurgery.

[13]  Andreas Horn,et al.  Opportunities of connectomic neuromodulation , 2020, NeuroImage.

[14]  Jurgen Germann,et al.  Mapping the network underpinnings of central post-stroke pain and analgesic neuromodulation. , 2020, Pain.

[15]  B. Strange,et al.  A unified connectomic target for deep brain stimulation in obsessive-compulsive disorder , 2020, Nature Communications.

[16]  M. Okun,et al.  A Comprehensive Review of Brain Connectomics and Imaging to Improve Deep Brain Stimulation Outcomes , 2020, Movement disorders : official journal of the Movement Disorder Society.

[17]  T. Santarius,et al.  CONNECTIONS, TRACTS, FRACTALS, AND THE REST: A WORKING GUIDE TO NETWORK AND CONNECTIVITY STUDIES IN NEUROSURGERY. , 2020, World neurosurgery.

[18]  Jurgen Germann,et al.  Probing the circuitry of panic with deep brain stimulation: Connectomic analysis and review of the literature , 2020, Brain Stimulation.

[19]  H. Duffau,et al.  Revisiting the functional anatomy of the human brain: Toward a meta-networking theory of cerebral functions. , 2020, Physiological reviews.

[20]  Tej D. Azad,et al.  Limitations of functional neuroimaging for patient selection and surgical planning in glioma surgery. , 2020, Neurosurgical focus.

[21]  R. Wennberg,et al.  Network-basis of seizures induced by deep brain stimulation: Literature Review and Connectivity Analysis. , 2019, World neurosurgery.

[22]  Simeon M. Wong,et al.  Connectomic Profiling Identifies Responders to Vagus Nerve Stimulation , 2019, Annals of neurology.

[23]  R. Buckner,et al.  The brain’s default network: updated anatomy, physiology and evolving insights , 2019, Nature Reviews Neuroscience.

[24]  T. Kuner,et al.  Glutamatergic synaptic input to glioma cells drives brain tumour progression , 2019, Nature.

[25]  Shawn M. Gillespie,et al.  Electrical and synaptic integration of glioma into neural circuits , 2019, Nature.

[26]  Viktor Jirsa,et al.  Optimization of surgical intervention outside the epileptogenic zone in the Virtual Epileptic Patient (VEP) , 2019, PLoS Comput. Biol..

[27]  H. Duffau,et al.  Language reorganization after resection of low-grade gliomas: an fMRI task based connectivity study , 2019, Brain Imaging and Behavior.

[28]  A. Lozano,et al.  Cellular, molecular, and clinical mechanisms of action of deep brain stimulation—a systematic review on established indications and outlook on future developments , 2019, EMBO molecular medicine.

[29]  A. Lozano,et al.  Magnetic Resonance-Guided Focused Ultrasound : Current Status and Future Perspectives in Thermal Ablation and Blood-Brain Barrier Opening , 2018, Journal of Korean Neurosurgical Society.

[30]  H. Duffau,et al.  An attempt to conceptualize the individual onco-functional balance: Why a standardized treatment is an illusion for diffuse low-grade glioma patients. , 2018, Critical reviews in oncology/hematology.

[31]  T. Yanagisawa,et al.  Preservation of Motor Function After Resection of Lower-Grade Glioma at the Precentral Gyrus and Prediction by Presurgical Functional Magnetic Resonance Imaging and Magnetoencephalography. , 2017, World neurosurgery.

[32]  M. Fox,et al.  Connectivity Predicts deep brain stimulation outcome in Parkinson disease , 2017, Annals of neurology.

[33]  Antonio Oliviero,et al.  Cortical plasticity catalyzed by prehabilitation enables extensive resection of brain tumors in eloquent areas. , 2017, Journal of neurosurgery.

[34]  Anthony Boyer,et al.  Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area. , 2017, Journal of neurosurgery.

[35]  Justin K. Rajendra,et al.  A connectomic approach for subcallosal cingulate deep brain stimulation surgery: prospective targeting in treatment-resistant depression , 2017, Molecular Psychiatry.

[36]  Victor Frenkel,et al.  Focused Ultrasound: An Emerging Therapeutic Modality for Neurologic Disease , 2017, Neurotherapeutics.

[37]  B. Meyer,et al.  Cortical plasticity of motor-eloquent areas measured by navigated transcranial magnetic stimulation in patients with glioma. , 2017, Journal of neurosurgery.

[38]  S. Cash,et al.  Predicting neurosurgical outcomes in focal epilepsy patients using computational modelling , 2016, Brain : a journal of neurology.

[39]  John Suckling,et al.  Connectome analysis for pre-operative brain mapping in neurosurgery , 2016, British journal of neurosurgery.

[40]  M. Berger,et al.  Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex. , 2016, Journal of neurosurgery.

[41]  H. Duffau,et al.  Mapping neuroplastic potential in brain-damaged patients. , 2016, Brain : a journal of neurology.

[42]  H. Mayberg,et al.  Mapping the "Depression Switch" During Intraoperative Testing of Subcallosal Cingulate Deep Brain Stimulation. , 2015, JAMA neurology.

[43]  S. Petersen,et al.  Brain Networks and Cognitive Architectures , 2015, Neuron.

[44]  H. Duffau Awake mapping of the brain connectome in glioma surgery: Concept is stronger than technology. , 2015, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[45]  A. Lang,et al.  Effects of subthalamic nucleus stimulation on motor cortex plasticity in Parkinson disease , 2015, Neurology.

[46]  H. Duffau The huge plastic potential of adult brain and the role of connectomics: New insights provided by serial mappings in glioma surgery , 2014, Cortex.

[47]  H. Iseki,et al.  Functional Plasticity of Language Confirmed with Intraoperative Electrical Stimulations and Updated Neuronavigation: Case Report of Low-Grade Glioma of the Left Inferior Frontal Gyrus , 2014, Neurologia medico-chirurgica.

[48]  O. Sporns,et al.  An Anatomical Substrate for Integration among Functional Networks in Human Cortex , 2013, The Journal of Neuroscience.

[49]  A. Lozano,et al.  Probing and Regulating Dysfunctional Circuits Using Deep Brain Stimulation , 2013, Neuron.

[50]  Á. Pascual-Leone,et al.  rTMS stimulation to induce plastic changes at the language motor area in a patient with a left recidivant brain tumor affecting Broca's area , 2012, Neurocase.

[51]  Walter Schneider,et al.  Identifying the brain's most globally connected regions , 2010, NeuroImage.

[52]  A. Lozano,et al.  Efficacy and safety of motor cortex stimulation for chronic neuropathic pain: critical review of the literature. , 2009, Journal of neurosurgery.

[53]  D. Feldman Synaptic mechanisms for plasticity in neocortex. , 2009, Annual review of neuroscience.

[54]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[55]  Erwin B. Montgomery,et al.  Mechanisms of action of deep brain stimulation (DBS) , 2008, Neuroscience & Biobehavioral Reviews.

[56]  Santosh Kesari,et al.  Malignant gliomas in adults. , 2008, The New England journal of medicine.

[57]  P. Thiran,et al.  Mapping Human Whole-Brain Structural Networks with Diffusion MRI , 2007, PloS one.

[58]  Hugues Duffau,et al.  Intraoperative cortico–subcortical stimulations in surgery of low-grade gliomas , 2005, Expert review of neurotherapeutics.

[59]  J. Rothwell,et al.  Theta Burst Stimulation of the Human Motor Cortex , 2005, Neuron.

[60]  H Duffau,et al.  Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation , 2003, Journal of neurology, neurosurgery, and psychiatry.

[61]  J. Dostrovsky,et al.  Mechanisms of deep brain stimulation , 2002, Movement disorders : official journal of the Movement Disorder Society.

[62]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[63]  Jurgen Germann,et al.  Lesion network mapping analysis identifies potential cause of post-operative depression in a case of cingulate low-grade glioma. , 2019, World neurosurgery.

[64]  S. Lang,et al.  Cognitive eloquence in neurosurgery: Insight from graph theoretical analysis of complex brain networks. , 2017, Medical hypotheses.

[65]  C. Zimmer,et al.  Clinical Factors Underlying the Inter-individual Variability of the Resting Motor Threshold in Navigated Transcranial Magnetic Stimulation Motor Mapping , 2016, Brain Topography.