IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35314-1.html
   My bibliography  Save this article

Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus

Author

Listed:
  • Eric Lowet

    (Boston University, Department of Biomedical Engineering)

  • Krishnakanth Kondabolu

    (Boston University, Department of Biomedical Engineering)

  • Samuel Zhou

    (Boston University, Department of Biomedical Engineering)

  • Rebecca A. Mount

    (Boston University, Department of Biomedical Engineering)

  • Yangyang Wang

    (Boston University, Department of Biomedical Engineering)

  • Cara R. Ravasio

    (Boston University, Department of Biomedical Engineering)

  • Xue Han

    (Boston University, Department of Biomedical Engineering)

Abstract

Deep brain stimulation (DBS) is a promising neuromodulation therapy, but the neurophysiological mechanisms of DBS remain unclear. In awake mice, we performed high-speed membrane voltage fluorescence imaging of individual hippocampal CA1 neurons during DBS delivered at 40 Hz or 140 Hz, free of electrical interference. DBS powerfully depolarized somatic membrane potentials without suppressing spike rate, especially at 140 Hz. Further, DBS paced membrane voltage and spike timing at the stimulation frequency and reduced timed spiking output in response to hippocampal network theta-rhythmic (3–12 Hz) activity patterns. To determine whether DBS directly impacts cellular processing of inputs, we optogenetically evoked theta-rhythmic membrane depolarization at the soma. We found that DBS-evoked membrane depolarization was correlated with DBS-mediated suppression of neuronal responses to optogenetic inputs. These results demonstrate that DBS produces powerful membrane depolarization that interferes with the ability of individual neurons to respond to inputs, creating an informational lesion.

Suggested Citation

  • Eric Lowet & Krishnakanth Kondabolu & Samuel Zhou & Rebecca A. Mount & Yangyang Wang & Cara R. Ravasio & Xue Han, 2022. "Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35314-1
    DOI: 10.1038/s41467-022-35314-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35314-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-35314-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Kiryl D. Piatkevich & Seth Bensussen & Hua-an Tseng & Sanaya N. Shroff & Violeta Gisselle Lopez-Huerta & Demian Park & Erica E. Jung & Or A. Shemesh & Christoph Straub & Howard J. Gritton & Michael F., 2019. "Population imaging of neural activity in awake behaving mice," Nature, Nature, vol. 574(7778), pages 413-417, October.
    2. Christopher D. Harvey & Forrest Collman & Daniel A. Dombeck & David W. Tank, 2009. "Intracellular dynamics of hippocampal place cells during virtual navigation," Nature, Nature, vol. 461(7266), pages 941-946, October.
    3. Jessica A. Cardin & Marie Carlén & Konstantinos Meletis & Ulf Knoblich & Feng Zhang & Karl Deisseroth & Li-Huei Tsai & Christopher I. Moore, 2009. "Driving fast-spiking cells induces gamma rhythm and controls sensory responses," Nature, Nature, vol. 459(7247), pages 663-667, June.
    4. Yoav Adam & Jeong J. Kim & Shan Lou & Yongxin Zhao & Michael E. Xie & Daan Brinks & Hao Wu & Mohammed A. Mostajo-Radji & Simon Kheifets & Vicente Parot & Selmaan Chettih & Katherine J. Williams & Benj, 2019. "Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics," Nature, Nature, vol. 569(7756), pages 413-417, May.
    5. Shuang Hao & Bin Tang & Zhenyu Wu & Kerstin Ure & Yaling Sun & Huifang Tao & Yan Gao & Akash J. Patel & Daniel J. Curry & Rodney C. Samaco & Huda Y. Zoghbi & Jianrong Tang, 2015. "Forniceal deep brain stimulation rescues hippocampal memory in Rett syndrome mice," Nature, Nature, vol. 526(7573), pages 430-434, October.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Bastijn J. G. Boom & Alfredo Elhazaz-Fernandez & Peter A. Rasmussen & Enny H. Beest & Aishwarya Parthasarathy & Damiaan Denys & Ingo Willuhn, 2023. "Unraveling the mechanisms of deep-brain stimulation of the internal capsule in a mouse model," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Changjia Cai & Johannes Friedrich & Amrita Singh & M Hossein Eybposh & Eftychios A Pnevmatikakis & Kaspar Podgorski & Andrea Giovannucci, 2021. "VolPy: Automated and scalable analysis pipelines for voltage imaging datasets," PLOS Computational Biology, Public Library of Science, vol. 17(4), pages 1-28, April.
    2. Yuki Bando & Michael Wenzel & Rafael Yuste, 2021. "Simultaneous two-photon imaging of action potentials and subthreshold inputs in vivo," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Hironobu Osaki & Moeko Kanaya & Yoshifumi Ueta & Mariko Miyata, 2022. "Distinct nociception processing in the dysgranular and barrel regions of the mouse somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    5. Jianian Lin & Zongyue Cheng & Guang Yang & Meng Cui, 2022. "Optical gearbox enabled versatile multiscale high-throughput multiphoton functional imaging," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    6. Federico Rocchi & Carola Canella & Shahryar Noei & Daniel Gutierrez-Barragan & Ludovico Coletta & Alberto Galbusera & Alexia Stuefer & Stefano Vassanelli & Massimo Pasqualetti & Giuliano Iurilli & Ste, 2022. "Increased fMRI connectivity upon chemogenetic inhibition of the mouse prefrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Amelie C. F. Bergs & Jana F. Liewald & Silvia Rodriguez-Rozada & Qiang Liu & Christin Wirt & Artur Bessel & Nadja Zeitzschel & Hilal Durmaz & Adrianna Nozownik & Holger Dill & Maëlle Jospin & Johannes, 2023. "All-optical closed-loop voltage clamp for precise control of muscles and neurons in live animals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Xin Fu & Eric Teboul & Grant L. Weiss & Pantelis Antonoudiou & Chandrashekhar D. Borkar & Jonathan P. Fadok & Jamie Maguire & Jeffrey G. Tasker, 2022. "Gq neuromodulation of BLA parvalbumin interneurons induces burst firing and mediates fear-associated network and behavioral state transition in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    10. Yide Zhang & Binglin Shen & Tong Wu & Jerry Zhao & Joseph C. Jing & Peng Wang & Kanomi Sasaki-Capela & William G. Dunphy & David Garrett & Konstantin Maslov & Weiwei Wang & Lihong V. Wang, 2022. "Ultrafast and hypersensitive phase imaging of propagating internodal current flows in myelinated axons and electromagnetic pulses in dielectrics," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    11. Vadivel, R. & Hammachukiattikul, P. & Gunasekaran, Nallappan & Saravanakumar, R. & Dutta, Hemen, 2021. "Strict dissipativity synchronization for delayed static neural networks: An event-triggered scheme," Chaos, Solitons & Fractals, Elsevier, vol. 150(C).
    12. Li, Jiajia & Zhang, Xuan & Du, Mengmeng & Wu, Ying, 2022. "Switching behavior of the gamma power in the neuronal network modulated by the astrocytes," Chaos, Solitons & Fractals, Elsevier, vol. 159(C).
    13. Sanaya N. Shroff & Eric Lowet & Sudiksha Sridhar & Howard J. Gritton & Mohammed Abumuaileq & Hua-An Tseng & Cyrus Cheung & Samuel L. Zhou & Krishnakanth Kondabolu & Xue Han, 2023. "Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Nozomu H. Nakamura & Hidemasa Furue & Kenta Kobayashi & Yoshitaka Oku, 2023. "Hippocampal ensemble dynamics and memory performance are modulated by respiration during encoding," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Florian Raudies & Michael E Hasselmo, 2012. "Modeling Boundary Vector Cell Firing Given Optic Flow as a Cue," PLOS Computational Biology, Public Library of Science, vol. 8(6), pages 1-17, June.
    16. Arita Silapetere & Songhwan Hwang & Yusaku Hontani & Rodrigo G. Fernandez Lahore & Jens Balke & Francisco Velazquez Escobar & Martijn Tros & Patrick E. Konold & Rainer Matis & Roberta Croce & Peter J., 2022. "QuasAr Odyssey: the origin of fluorescence and its voltage sensitivity in microbial rhodopsins," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    17. Kai Zhou & Wei Wei & Dan Yang & Hui Zhang & Wei Yang & Yunpeng Zhang & Yingnan Nie & Mingming Hao & Pengcheng Wang & Hang Ruan & Ting Zhang & Shouyan Wang & Yaobo Liu, 2024. "Dual electrical stimulation at spinal-muscular interface reconstructs spinal sensorimotor circuits after spinal cord injury," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    18. Brent Kevin Young & Jayden Nicole Brennan & Ping Wang & Ning Tian, 2018. "Virtual reality method to analyze visual recognition in mice," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-14, May.
    19. Lou T. Blanpain & Eric R. Cole & Emily Chen & James K. Park & Michael Y. Walelign & Robert E. Gross & Brian T. Cabaniss & Jon T. Willie & Annabelle C. Singer, 2024. "Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    20. Yang, Pengbo & Shang, Pengjian & Lin, Aijing, 2017. "Financial time series analysis based on effective phase transfer entropy," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 468(C), pages 398-408.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35314-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.