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May 04, 2021; 96 (18) Article

Network-Related Changes in Neurotransmitters and Seizure Propagation During Rodent Epileptogenesis

Roni Dhaher, Shaun E. Gruenbaum, Mani Ratnesh S. Sandhu, Sigrid Ottestad-Hansen, Nathan Tu, Yue Wang, Tih-Shih W. Lee, Ketaki Deshpande, Dennis D. Spencer, Niels Christian Danbolt, Hitten P. Zaveri, Tore Eid
First published March 15, 2021, DOI: https://doi.org/10.1212/WNL.0000000000011846
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Article Information

vol. 96 no. 18 e2261-e2271
DOI: 
https://doi.org/10.1212/WNL.0000000000011846
PubMed: 
33722994
Published By: 
Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology
Print ISSN: 
0028-3878
Online ISSN: 
1526-632X
History: 
  • Received May 19, 2020
  • Accepted in final form January 29, 2021
  • First Published March 15, 2021.

Article Versions

Copyright & Usage: 
© 2021 American Academy of Neurology

Author Disclosures

    1. Roni Dhaher, PhD,
    2. Shaun E. Gruenbaum, MD, PhD,
    3. Mani Ratnesh S. Sandhu, MBBS, MHS,
    4. Sigrid Ottestad-Hansen,
    5. Nathan Tu, MD,
    6. Yue Wang, MD, PhD,
    7. Tih-Shih W. Lee, MD, PhD,
    8. Ketaki Deshpande, PhD,
    9. Dennis D. Spencer, MD,
    10. Niels Christian Danbolt, MD, PhD,
    11. Hitten P. Zaveri, PhD and
    12. Tore Eid, MD, PhD
  1. Roni Dhaher, PhD,
    2. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  2. Shaun E. Gruenbaum, MD, PhD,
    3. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. Anesthesia for patients with interstitial lung disease or other restrictive disorders. UpToDate, Wolters Kluwer (Philadelphia, PA), 2018-2020

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  3. Mani Ratnesh S. Sandhu, MBBS, MHS,
    4. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. (1) The Swebillius Foundation

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  4. Sigrid Ottestad-Hansen,
    5. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  5. Nathan Tu, MD,
    6. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  6. Yue Wang, MD, PhD,
    7. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  7. Tih-Shih W. Lee, MD, PhD,
    8. Scientific Advisory Boards:

    1. None

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. None

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. None

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  8. Ketaki Deshpande, PhD,
    9. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  9. Dennis D. Spencer, MD,
    10. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. NONE

    Patents:

    1. Wireless system for epilepsy monitoring and measurement. DA Putz, BS Joshi, B Lanning, JA Nolan, GJ Nuebel, DD Spencer, HP Zaveri. United States Patent 8165684 issued 04/24/2012. Wireless system for epilepsy monitoring and measurement - Continuation in Part. B Lanning, JA Nolan, GJ Nuebel, DD Spencer, HP Zaveri. United States Patent 8738139 issued 04/17/2014. Wireless system for epilepsy monitoring and measurement - Continuation in Part. B Lanning, JA Nolan, GJ Nuebel, DD Spencer, HP Zaveri. United States Patent 9326726 B2 issued 05/03/2016. Brain cooling system. HP Zaveri, DD Spencer, B. Joshi, D. Binkley, B. Lanning. United States Patent 9849025 issued 12/26/2017. Multiplexed implantable sensor probe, Mark Reed, Dennis Spencer and Hitten Zaveri, US Patent Application 20180325386, Filing Date: May 9, 2018, Publication date: 11/15/2018. Novel 3D Silicon-Based Comb Structure Probe for Neural Sensing & Stimulation with Optimized Biocompatible Dimensions, Emily R. Kinser, Roy Yu, Hariklia Deligianni, Themis R. Kyriakides, Jason Gerrard, Dennis Spencer, Hitten Zaveri, Filed on 11/29/2018.

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. NONE

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  10. Niels Christian Danbolt, MD, PhD,
    11. Scientific Advisory Boards:

    1. None

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. None

    Editorial Boards:

    1. NONE

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. Supported by the University of Oslo

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. None

    Stock/Stock Options/Board of Directors Compensation:

    1. Owner of the company Neurotransporter AS, Oslo, Norway. This is holding company owning shares in Science Linker AS (50 %) and in Scandinavian Holding AS (<1 %). The activities of these companies are not related to the present study.

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  11. Hitten P. Zaveri, PhD and
    12. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for Travel or Speaker Honoraria:

    1. NONE

    Editorial Boards:

    1. (1) IEEE Consumer Electronics Magazine, Editorial Board, 2017-present

    Patents:

    1. (1) Wireless system for epilepsy monitoring and measurement. DA Putz, BS Joshi, B Lanning, JA Nolan, GJ Nuebel, DD Spencer, HP Zaveri. United States Patent 8165684 issued 04/24/2012. (2) Wireless system for epilepsy monitoring and measurement - Continuation in Part. B Lanning, JA Nolan, GJ Nuebel, DD Spencer, HP Zaveri. United States Patent 8738139 issued 04/17/2014. (3) Wireless system for epilepsy monitoring and measurement - Continuation in Part. B Lanning, JA Nolan, GJ Nuebel, DD Spencer, HP Zaveri. United States Patent 9326726 B2 issued 05/03/2016. (4) Fault tolerant multi-electrode array for brain implantable device. B Joshi, I Acharya, and HP Zaveri. United States Patent 9277874 issued 03/08/2016. (5) Brain cooling system. HP Zaveri, DD Spencer, B. Joshi, D. Binkley, B. Lanning. United States Patent 9849025 issued 12/26/2017. (6) System and method for diagnosis and notification regarding the onset of stroke. KN Sheth, HP Zaveri, and R Coifman. International Patent Application PCT/US2017/013149, Filing date 01/12/2017. Pending. (7) Multiplexed implantable sensor probe, Mark Reed, Dennis Spencer and Hitten Zaveri, US Patent Application 20180325386, Filing Date: May 9, 2018, Publication date: 11/15/2018. Pending. (8) Flow Sensor for Cerebral Fluidic Device, Kazunori Hoshino, Davina Jaiswal, Mengdi Bao, Garrett Soler, Ariane Garrett, Ryan Grant, Michael Diluna, Hitten Zaveri, Pub. No.: WO/2018/183737, International Patent Application No.: PCT/US2018/025238, Publication Date: 04/10/2018, International Filing Date: 03/29/2018. Pending. (9) Novel 3D Silicon-Based Comb Structure Probe for Neural Sensing & Stimulation with Optimized Biocompatible Dimensions, Emily R. Kinser, Roy Yu, Hariklia Deligianni, Themis R. Kyriakides, Jason Gerrard, Dennis Spencer, Hitten Zaveri, Filed on 11/29/2018. Pending.

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. (1) NIH, 1R01NS117904, Investigator, 4/1/2020-3/31/2025 (2) NIH, R21 NS109734-01A1, Investigator, 05/01/2020- 04/30/2022 (3) NIH, MPI, 07/01/2019-06/30/2023

    Research Support, Academic Entities:

    1. NONE

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. (1) Alva Health, Inc

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  12. Tore Eid, MD, PhD
    13. Scientific Advisory Boards:

    1. NONE

    Gifts:

    1. NONE

    Funding for travel or speaker honoraria:

    1. Dr. Eid has received travel reimbursement from University of Oslo, Norway (nonprofit).

    Editorial Boards:

    1. Dr. Eid is a scientific editorial adviser for Epilepsy Currents (Sage Publishing Company).

    Patents:

    1. NONE

    Publishing Royalties:

    1. NONE

    Employment, Commercial Entity:

    1. NONE

    Consultancies:

    1. NONE

    Speakers' Bureaus:

    1. NONE

    Other Activities:

    1. NONE

    Clinical Procedures or Imaging Studies:

    1. NONE

    Research Support, Commercial Entities:

    1. NONE

    Research Support, Government Entities:

    1. National Institutes of Health, grant numbers: NS109734 (PI), NS109062 (PI), DA036151-06 (Core director), NS094253 (co- investigator), MD010711 (core director), NS096088 (co- investigator), DK045735-28 (co-investigator)

    Research Support, Academic Entities:

    1. University of Oslo, Norway

    Research Support, Foundations and Societies:

    1. NONE

    Stock/Stock Options/Board of Directors Compensation:

    1. NONE

    License Fee Payments, Technology or Inventions:

    1. NONE

    Royalty Payments, Technology or Inventions:

    1. NONE

    Stock/Stock Options, Research Sponsor:

    1. NONE

    Stock/Stock Options, Medical Equipment & Materials:

    1. NONE

    Legal Proceedings:

    1. NONE

  1. From the Departments of Laboratory Medicine (R.D., M.R.S.S., N.T., Y.W., K.D., T.E.), Anesthesiology (S.E.G.), Neurosurgery (D.D.S.), Psychiatry (T.-S.W.L.), and Neurology (H.P.Z.), Yale School of Medicine, New Haven, CT; and Department of Molecular Medicine (S.O.-H., N.C.D.), Division of Anatomy, Institute for Basic Medical Sciences, University of Oslo, Norway.
  1. Correspondence
    Dr. Eid tore.eid{at}yale.edu
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