The impact of high grade glial neoplasms on human cortical electrophysiology

S. Kathleen Bandt, Jarod L. Roland, Mrinal Pahwa, Carl D. Hacker, David T. Bundy, Jonathan D. Breshears, Mohit Sharma, Joshua S. Shimony, Eric C. Leuthardt

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Objective The brain's functional architecture of interconnected network-related oscillatory patterns in discrete cortical regions has been well established with functional magnetic resonance imaging (fMRI) studies or direct cortical electrophysiology from electrodes placed on the surface of the brain, or electrocorticography (ECoG). These resting state networks exhibit a robust functional architecture that persists through all stages of sleep and under anesthesia. While the stability of these networks provides a fundamental understanding of the organization of the brain, understanding how these regions can be perturbed is also critical in defining the brain's ability to adapt while learning and recovering from injury. Methods Patients undergoing an awake craniotomy for resection of a tumor were studied as a unique model of an evolving injury to help define how the cortical physiology and the associated networks were altered by the presence of an invasive brain tumor. Results This study demonstrates that there is a distinct pattern of alteration of cortical physiology in the setting of a malignant glioma. These changes lead to a physiologic sequestration and progressive synaptic homogeneity suggesting that a de-learning phenomenon occurs within the tumoral tissue compared to its surroundings. Significance These findings provide insight into how the brain accommodates a region of defunctionalized cortex. Additionally, these findings may have important implications for emerging techniques in brain mapping using endogenous cortical physiology.

Original languageEnglish (US)
Article numbere0173448
JournalPloS one
Volume12
Issue number3
DOIs
StatePublished - Mar 1 2017

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Electrophysiology
electrophysiology
neuroglia
Neuroglia
Brain
brain
neoplasms
Physiology
Neoplasms
physiology
Learning
Tumors
Brain Mapping
Brain mapping
Aptitude
Craniotomy
Sleep Stages
learning
Wounds and Injuries
Brain Neoplasms

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Bandt, S. K., Roland, J. L., Pahwa, M., Hacker, C. D., Bundy, D. T., Breshears, J. D., ... Leuthardt, E. C. (2017). The impact of high grade glial neoplasms on human cortical electrophysiology. PloS one, 12(3), [e0173448]. https://doi.org/10.1371/journal.pone.0173448
Bandt, S. Kathleen ; Roland, Jarod L. ; Pahwa, Mrinal ; Hacker, Carl D. ; Bundy, David T. ; Breshears, Jonathan D. ; Sharma, Mohit ; Shimony, Joshua S. ; Leuthardt, Eric C. / The impact of high grade glial neoplasms on human cortical electrophysiology. In: PloS one. 2017 ; Vol. 12, No. 3.
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Bandt, SK, Roland, JL, Pahwa, M, Hacker, CD, Bundy, DT, Breshears, JD, Sharma, M, Shimony, JS & Leuthardt, EC 2017, 'The impact of high grade glial neoplasms on human cortical electrophysiology', PloS one, vol. 12, no. 3, e0173448. https://doi.org/10.1371/journal.pone.0173448

The impact of high grade glial neoplasms on human cortical electrophysiology. / Bandt, S. Kathleen; Roland, Jarod L.; Pahwa, Mrinal; Hacker, Carl D.; Bundy, David T.; Breshears, Jonathan D.; Sharma, Mohit; Shimony, Joshua S.; Leuthardt, Eric C.

In: PloS one, Vol. 12, No. 3, e0173448, 01.03.2017.

Research output: Contribution to journalArticle

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T1 - The impact of high grade glial neoplasms on human cortical electrophysiology

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AU - Roland, Jarod L.

AU - Pahwa, Mrinal

AU - Hacker, Carl D.

AU - Bundy, David T.

AU - Breshears, Jonathan D.

AU - Sharma, Mohit

AU - Shimony, Joshua S.

AU - Leuthardt, Eric C.

PY - 2017/3/1

Y1 - 2017/3/1

N2 - Objective The brain's functional architecture of interconnected network-related oscillatory patterns in discrete cortical regions has been well established with functional magnetic resonance imaging (fMRI) studies or direct cortical electrophysiology from electrodes placed on the surface of the brain, or electrocorticography (ECoG). These resting state networks exhibit a robust functional architecture that persists through all stages of sleep and under anesthesia. While the stability of these networks provides a fundamental understanding of the organization of the brain, understanding how these regions can be perturbed is also critical in defining the brain's ability to adapt while learning and recovering from injury. Methods Patients undergoing an awake craniotomy for resection of a tumor were studied as a unique model of an evolving injury to help define how the cortical physiology and the associated networks were altered by the presence of an invasive brain tumor. Results This study demonstrates that there is a distinct pattern of alteration of cortical physiology in the setting of a malignant glioma. These changes lead to a physiologic sequestration and progressive synaptic homogeneity suggesting that a de-learning phenomenon occurs within the tumoral tissue compared to its surroundings. Significance These findings provide insight into how the brain accommodates a region of defunctionalized cortex. Additionally, these findings may have important implications for emerging techniques in brain mapping using endogenous cortical physiology.

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Bandt SK, Roland JL, Pahwa M, Hacker CD, Bundy DT, Breshears JD et al. The impact of high grade glial neoplasms on human cortical electrophysiology. PloS one. 2017 Mar 1;12(3). e0173448. https://doi.org/10.1371/journal.pone.0173448