Extracellular DC electric fields induce nonuniform membrane polarization in rat hippocampal CA1 pyramidal neurons

Hiroki Akiyama, Yuki Shimizu, Hiroyoshi Miyakawa, Masashi Inoue

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Non-synaptic interactions among neurons via extracellular electric fields may play functional roles in the CNS. Previously in a study using voltage-sensitive dye imaging, we reported characteristic membrane polarization profiles in the CA1 region of hippocampal slices during exposure to extracellular DC fields: slow monophasic polarization in somatic region and biphasic polarization (fast polarization and following slow repolarization) in mid-dendritic region. Here, using optical imaging and patch-clamp recordings, we showed that CA1 pyramidal neurons indeed show the characteristic polarization in response to DC fields, and investigated the mechanism underlying the profiles. Both the monophasic and biphasic polarization could be fitted with a double exponential function. The τs (ms) were 12.6 ± 2.5 and 56.0 ± 4.7 for the monophasic polarization, and 14.2 ± 1.2 and 42.2 ± 2.8 for the biphasic polarization. Based on our previous theoretical studies, we hypothesized that lower resistivity in the distal apical dendrites is responsible for generating the characteristic polarization profiles. We tested this hypothesis by removing the distal apical dendrites or by blocking ion channel-mediated conductance. Removal of distal dendrites caused drastic changes in the polarization profiles, e.g. biphasic polarization was damped. However, none of the blockers tested had a marked effect on the biphasic polarization. Our results demonstrate the importance of the apical dendrite for generating the characteristic polarization profiles, and suggest that voltage-activated conductance, including HCN channel-mediated conductance, had only minor contributions to these profiles. These findings provide a better understanding of how neurons in the CNS respond to extracellular electric fields.

Original languageEnglish
Pages (from-to)22-35
Number of pages14
JournalBrain Research
Volume1383
DOIs
Publication statusPublished - 2011 Apr 6
Externally publishedYes

Fingerprint

Pyramidal Cells
Dendrites
Membranes
Voltage-Sensitive Dye Imaging
Hippocampal CA1 Region
Neurons
Optical Imaging
Ion Channels
Theoretical Models

Keywords

  • Dendrite
  • Electric fields
  • Passive membrane property
  • Voltage-sensitive dye

ASJC Scopus subject areas

  • Neuroscience(all)
  • Clinical Neurology
  • Developmental Biology
  • Molecular Biology

Cite this

Extracellular DC electric fields induce nonuniform membrane polarization in rat hippocampal CA1 pyramidal neurons. / Akiyama, Hiroki; Shimizu, Yuki; Miyakawa, Hiroyoshi; Inoue, Masashi.

In: Brain Research, Vol. 1383, 06.04.2011, p. 22-35.

Research output: Contribution to journalArticle

Akiyama, Hiroki ; Shimizu, Yuki ; Miyakawa, Hiroyoshi ; Inoue, Masashi. / Extracellular DC electric fields induce nonuniform membrane polarization in rat hippocampal CA1 pyramidal neurons. In: Brain Research. 2011 ; Vol. 1383. pp. 22-35.
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