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

Author

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  • 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
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    References listed on IDEAS

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    Cited by:

    1. Sudiksha Sridhar & Eric Lowet & Howard J. Gritton & Jennifer Freire & Chengqian Zhou & Florence Liang & Xue Han, 2024. "Beta-frequency sensory stimulation enhances gait rhythmicity through strengthened coupling between striatal networks and stepping movement," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. 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.

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