Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation

Nat Commun. 2017 Apr 6:8:15039. doi: 10.1038/ncomms15039.

Abstract

Activity in hippocampal area CA1 is essential for consolidating episodic memories, but it is unclear how CA1 activity patterns drive memory formation. We find that in the hours following single-trial contextual fear conditioning (CFC), fast-spiking interneurons (which typically express parvalbumin (PV)) show greater firing coherence with CA1 network oscillations. Post-CFC inhibition of PV+ interneurons blocks fear memory consolidation. This effect is associated with loss of two network changes associated with normal consolidation: (1) augmented sleep-associated delta (0.5-4 Hz), theta (4-12 Hz) and ripple (150-250 Hz) oscillations; and (2) stabilization of CA1 neurons' functional connectivity patterns. Rhythmic activation of PV+ interneurons increases CA1 network coherence and leads to a sustained increase in the strength and stability of functional connections between neurons. Our results suggest that immediately following learning, PV+ interneurons drive CA1 oscillations and reactivation of CA1 ensembles, which directly promotes network plasticity and long-term memory formation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • CA1 Region, Hippocampal / metabolism
  • CA1 Region, Hippocampal / physiology*
  • Electric Stimulation / methods
  • Interneurons / metabolism
  • Interneurons / physiology*
  • Learning / physiology
  • Male
  • Memory / physiology*
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nerve Net / metabolism
  • Nerve Net / physiology*
  • Neuronal Plasticity / physiology
  • Parvalbumins / genetics
  • Parvalbumins / metabolism*
  • Synaptic Transmission / physiology

Substances

  • Parvalbumins