Dendritic spikes induce ripples in parvalbumin interneurons during hippocampal sharp waves

Neuron. 2014 May 21;82(4):908-24. doi: 10.1016/j.neuron.2014.04.004.

Abstract

Sharp-wave ripples are transient oscillatory events in the hippocampus that are associated with the reactivation of neuronal ensembles within specific circuits during memory formation. Fast-spiking, parvalbumin-expressing interneurons (FS-PV INs) are thought to provide fast integration in these oscillatory circuits by suppressing regenerative activity in their dendrites. Here, using fast 3D two-photon imaging and a caged glutamate, we challenge this classical view by demonstrating that FS-PV IN dendrites can generate propagating Ca(2+) spikes during sharp-wave ripples. The spikes originate from dendritic hot spots and are mediated dominantly by L-type Ca(2+) channels. Notably, Ca(2+) spikes were associated with intrinsically generated membrane potential oscillations. These oscillations required the activation of voltage-gated Na(+) channels, had the same frequency as the field potential oscillations associated with sharp-wave ripples, and controlled the phase of action potentials. Furthermore, our results demonstrate that the smallest functional unit that can generate ripple-frequency oscillations is a segment of a dendrite.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Brain Waves / drug effects
  • Brain Waves / physiology*
  • Calcium / metabolism
  • Dendrites / drug effects
  • Dendrites / physiology*
  • Glutamic Acid / pharmacology
  • Green Fluorescent Proteins / genetics
  • Hippocampus / cytology*
  • Hippocampus / physiology*
  • Imaging, Three-Dimensional
  • In Vitro Techniques
  • Interneurons / cytology*
  • Interneurons / drug effects
  • Interneurons / metabolism
  • Mice, Inbred C57BL
  • Parvalbumins / metabolism*
  • Photic Stimulation

Substances

  • Parvalbumins
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Glutamic Acid
  • Calcium