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Articles, Neurobiology of Disease

Propagation of Epileptiform Activity Can Be Independent of Synaptic Transmission, Gap Junctions, or Diffusion and Is Consistent with Electrical Field Transmission

Mingming Zhang, Thomas P. Ladas, Chen Qiu, Rajat S. Shivacharan, Luis E. Gonzalez-Reyes and Dominique M. Durand
Journal of Neuroscience 22 January 2014, 34 (4) 1409-1419; https://doi.org/10.1523/JNEUROSCI.3877-13.2014
Mingming Zhang
Neural Engineering Center, Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
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Thomas P. Ladas
Neural Engineering Center, Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
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Chen Qiu
Neural Engineering Center, Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
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Rajat S. Shivacharan
Neural Engineering Center, Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
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Luis E. Gonzalez-Reyes
Neural Engineering Center, Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
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Dominique M. Durand
Neural Engineering Center, Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
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Abstract

The propagation of activity in neural tissue is generally associated with synaptic transmission, but epileptiform activity in the hippocampus can propagate with or without synaptic transmission at a speed of ∼0.1 m/s. This suggests an underlying common nonsynaptic mechanism for propagation. To study this mechanism, we developed a novel unfolded hippocampus preparation, from CD1 mice of either sex, which preserves the transverse and longitudinal connections and recorded activity with a penetrating microelectrode array. Experiments using synaptic transmission and gap junction blockers indicated that longitudinal propagation is independent of chemical or electrical synaptic transmission. Propagation speeds of 0.1 m/s are not compatible with ionic diffusion or pure axonal conduction. The only other means of communication between neurons is through electric fields. Computer simulations revealed that activity can indeed propagate from cell to cell solely through field effects. These results point to an unexpected propagation mechanism for neural activity in the hippocampus involving endogenous field effect transmission.

  • neural
  • activity
  • propagation
  • electric field
  • hippocampus
  • epileptiform

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The Journal of Neuroscience: 34 (4)
Journal of Neuroscience
Vol. 34, Issue 4
22 Jan 2014
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Propagation of Epileptiform Activity Can Be Independent of Synaptic Transmission, Gap Junctions, or Diffusion and Is Consistent with Electrical Field Transmission
Mingming Zhang, Thomas P. Ladas, Chen Qiu, Rajat S. Shivacharan, Luis E. Gonzalez-Reyes, Dominique M. Durand
Journal of Neuroscience 22 January 2014, 34 (4) 1409-1419; DOI: 10.1523/JNEUROSCI.3877-13.2014

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Propagation of Epileptiform Activity Can Be Independent of Synaptic Transmission, Gap Junctions, or Diffusion and Is Consistent with Electrical Field Transmission
Mingming Zhang, Thomas P. Ladas, Chen Qiu, Rajat S. Shivacharan, Luis E. Gonzalez-Reyes, Dominique M. Durand
Journal of Neuroscience 22 January 2014, 34 (4) 1409-1419; DOI: 10.1523/JNEUROSCI.3877-13.2014
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Keywords

  • neural
  • activity
  • propagation
  • electric field
  • hippocampus
  • epileptiform

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  • Finally! The extracellular vacuum meets the press!
    Damir Janigro
    Published on: 23 January 2014
  • Published on: (23 January 2014)
    Page navigation anchor for Finally! The extracellular vacuum meets the press!
    Finally! The extracellular vacuum meets the press!
    • Damir Janigro, Professor
    • Other Contributors:
      • Philip H. Iffland II

    It has been suspected by many and pursued by few that epileptiform activity does not require synaptic or gliotransmission. This concept can be summarized by saying that the way you break it is not the way you make it! Studying normal brain function, interictal spikes, seizure onset or propagation are different aspects of "epilepsy" and should not be clumped together in "models of seizures". Finally, the size of extracell...

    Show More

    It has been suspected by many and pursued by few that epileptiform activity does not require synaptic or gliotransmission. This concept can be summarized by saying that the way you break it is not the way you make it! Studying normal brain function, interictal spikes, seizure onset or propagation are different aspects of "epilepsy" and should not be clumped together in "models of seizures". Finally, the size of extracellular space and its regulation by the BBB is also a mechanism to be more aggressively pursued.

    Marchi N, Granata T, Janigro D. Inflammatory pathways of seizure disorders. Trends Neurosci. 2013 PubMed PMID: 24355813

    Conflict of Interest:

    None declared

    Show Less
    Competing Interests: None declared.

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