Propagation of epileptiform activity can be independent of synaptic transmission, gap junctions, or diffusion and is consistent with electrical field transmission

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...

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Published inThe Journal of neuroscience Vol. 34; no. 4; pp. 1409 - 1419
Main Authors Zhang, Mingming, Ladas, Thomas P, Qiu, Chen, Shivacharan, Rajat S, Gonzalez-Reyes, Luis E, Durand, Dominique M
Format Journal Article
LanguageEnglish
Published United States Society for Neuroscience 22.01.2014
Subjects
Animals
Computer Simulation
Disease Models, Animal
Electromagnetic Fields
Electrophysiology
Epilepsy - physiopathology
Female
Gap Junctions - physiology
Hippocampus - physiopathology
Male
Mice
Models, Neurological
Neural Pathways - physiopathology
Seizures - physiopathology
Synaptic Transmission - physiology
electric field
propagation
activity
hippocampus
neural
epileptiform
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Summary: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.
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Author contributions: M.Z. and D.M.D. designed research; M.Z., C.Q., and R.S.S. performed research; M.Z., T.P.L., and L.E.G.-R. contributed unpublished reagents/analytic tools; M.Z., T.P.L., and R.S.S. analyzed data; M.Z., T.P.L., C.Q., L.E.G.-R., and D.M.D. wrote the paper.
ISSN:0270-6474
1529-2401
DOI:10.1523/JNEUROSCI.3877-13.2014