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Research ArticleResearch Article: New Research, Neuronal Excitability

Propagating Activity in Neocortex, Mediated by Gap Junctions and Modulated by Extracellular Potassium

Christoforos A. Papasavvas, R. Ryley Parrish and Andrew J. Trevelyan
eNeuro 25 February 2020, 7 (2) ENEURO.0387-19.2020; DOI: https://doi.org/10.1523/ENEURO.0387-19.2020
Christoforos A. Papasavvas
Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne NE2 4HH, United Kingdom
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R. Ryley Parrish
Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne NE2 4HH, United Kingdom
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Andrew J. Trevelyan
Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne NE2 4HH, United Kingdom
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Abstract

Parvalbumin-expressing interneurons in cortical networks are coupled by gap junctions, forming a syncytium that supports propagating epileptiform discharges, induced by 4-aminopyridine. It remains unclear, however, whether these propagating events occur under more natural states, without pharmacological blockade. In particular, we investigated whether propagation also happens when extracellular K+ rises, as is known to occur following intense network activity, such as during seizures. We examined how increasing [K+]o affects the likelihood of propagating activity away from a site of focal (200–400 μm) optogenetic activation of parvalbumin-expressing interneurons. Activity was recorded using a linear 16-electrode array placed along layer V of primary visual cortex. At baseline levels of [K+]o (3.5 mm), induced activity was recorded only within the illuminated area. However, when [K+]o was increased above a threshold level (50th percentile = 8.0 mm; interquartile range = 7.5–9.5 mm), time-locked, fast-spiking unit activity, indicative of parvalbumin-expressing interneuron firing, was also recorded outside the illuminated area, propagating at 59.1 mm/s. The propagating unit activity was unaffected by blockade of GABAergic synaptic transmission, but it was modulated by glutamatergic blockers, and was reduced, and in most cases prevented altogether, by pharmacological blockade of gap junctions, achieved by any of the following three different drugs: quinine, mefloquine, or carbenoxolone. Washout of quinine rapidly re-established the pattern of propagating activity. Computer simulations show qualitative differences between propagating discharges in high [K+]o and 4-aminopyridine, arising from differences in the electrotonic effects of these two manipulations. These interneuronal syncytial interactions are likely to affect the complex electrographic dynamics of seizures, once [K+]o is raised above this threshold level.

  • electrotonic
  • excitability
  • gap junction
  • parvalbumin
  • potassium
  • seizure

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by project grants from Epilepsy Research UK (Grant P1504) and Medical Research Council (UK) (Grants MR/J013250/1 and MR/R005427/1). A.J.T. was the recipient of a Schaefer Scholarship from Columbia University. C.A.P. was supported by a Wellcome Trust PhD Studentship (099755/Z/12/Z). We would like also to acknowledge the technical assistance provided by Neela Codadu and Eike Joest, when we were starting this project.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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eneuro: 7 (2)
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Vol. 7, Issue 2
March/April 2020
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Propagating Activity in Neocortex, Mediated by Gap Junctions and Modulated by Extracellular Potassium
Christoforos A. Papasavvas, R. Ryley Parrish, Andrew J. Trevelyan
eNeuro 25 February 2020, 7 (2) ENEURO.0387-19.2020; DOI: 10.1523/ENEURO.0387-19.2020

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Propagating Activity in Neocortex, Mediated by Gap Junctions and Modulated by Extracellular Potassium
Christoforos A. Papasavvas, R. Ryley Parrish, Andrew J. Trevelyan
eNeuro 25 February 2020, 7 (2) ENEURO.0387-19.2020; DOI: 10.1523/ENEURO.0387-19.2020
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Keywords

  • electrotonic
  • excitability
  • gap junction
  • parvalbumin
  • potassium
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