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Research Article

Synaptic plasticity by antidromic firing during hippocampal network oscillations

Olena Bukalo, Emilie Campanac, Dax A. Hoffman, and R. Douglas Fields
PNAS first published March 11, 2013; https://doi.org/10.1073/pnas.1210735110
Olena Bukalo
aNervous System Development and Plasticity Section, and
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Emilie Campanac
bMolecular Neurophysiology and Biophysics Section, Program in Development Neuroscience, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
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Dax A. Hoffman
bMolecular Neurophysiology and Biophysics Section, Program in Development Neuroscience, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
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R. Douglas Fields
aNervous System Development and Plasticity Section, and
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  • For correspondence: fieldsd@mail.nih.gov
  1. Edited* by Nancy J. Kopell, Boston University, Boston, MA, and approved February 11, 2013 (received for review June 25, 2012)

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Abstract

Learning and other cognitive tasks require integrating new experiences into context. In contrast to sensory-evoked synaptic plasticity, comparatively little is known of how synaptic plasticity may be regulated by intrinsic activity in the brain, much of which can involve nonclassical modes of neuronal firing and integration. Coherent high-frequency oscillations of electrical activity in CA1 hippocampal neurons [sharp-wave ripple complexes (SPW-Rs)] functionally couple neurons into transient ensembles. These oscillations occur during slow-wave sleep or at rest. Neurons that participate in SPW-Rs are distinguished from adjacent nonparticipating neurons by firing action potentials that are initiated ectopically in the distal region of axons and propagate antidromically to the cell body. This activity is facilitated by GABAA-mediated depolarization of axons and electrotonic coupling. The possible effects of antidromic firing on synaptic strength are unknown. We find that facilitation of spontaneous SPW-Rs in hippocampal slices by increasing gap-junction coupling or by GABAA-mediated axon depolarization resulted in a reduction of synaptic strength, and electrical stimulation of axons evoked a widespread, long-lasting synaptic depression. Unlike other forms of synaptic plasticity, this synaptic depression is not dependent upon synaptic input or glutamate receptor activation, but rather requires L-type calcium channel activation and functional gap junctions. Synaptic stimulation delivered after antidromic firing, which was otherwise too weak to induce synaptic potentiation, triggered a long-lasting increase in synaptic strength. Rescaling synaptic weights in subsets of neurons firing antidromically during SPW-Rs might contribute to memory consolidation by sharpening specificity of subsequent synaptic input and promoting incorporation of novel information.

  • long-term depression
  • long-term potentiation
  • network plasticity
  • excitability

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: fieldsd{at}mail.nih.gov.
  • Author contributions: O.B., D.A.H., and R.D.F. designed research; O.B. and E.C. performed research; O.B., E.C., and R.D.F. analyzed data; and O.B. and R.D.F. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1210735110/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Antidromically induced plasticity
Olena Bukalo, Emilie Campanac, Dax A. Hoffman, R. Douglas Fields
Proceedings of the National Academy of Sciences Mar 2013, 201210735; DOI: 10.1073/pnas.1210735110

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Antidromically induced plasticity
Olena Bukalo, Emilie Campanac, Dax A. Hoffman, R. Douglas Fields
Proceedings of the National Academy of Sciences Mar 2013, 201210735; DOI: 10.1073/pnas.1210735110
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