Sharp wave ripples during learning stabilize the hippocampal spatial map

Nat Neurosci. 2017 Jun;20(6):845-853. doi: 10.1038/nn.4543. Epub 2017 Apr 10.

Abstract

Cognitive representation of the environment requires a stable hippocampal map, but the mechanisms maintaining a given map are unknown. Because sharp wave-ripples (SPW-R) orchestrate both retrospective and prospective spatial information, we hypothesized that disrupting neuronal activity during SPW-Rs affects spatial representation. Mice learned new sets of three goal locations daily in a multiwell maze. We used closed-loop SPW-R detection at goal locations to trigger optogenetic silencing of a subset of CA1 pyramidal neurons. Control place cells (nonsilenced or silenced outside SPW-Rs) largely maintained the location of their place fields after learning and showed increased spatial information content. In contrast, the place fields of SPW-R-silenced place cells remapped, and their spatial information remained unaltered. SPW-R silencing did not impact the firing rates or proportions of place cells. These results suggest that interference with SPW-R-associated activity during learning prevents stabilization and refinement of hippocampal maps.

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • CA1 Region, Hippocampal / physiology*
  • Electric Stimulation
  • Learning / physiology*
  • Male
  • Maze Learning / physiology
  • Mice
  • Mice, Transgenic
  • Neural Inhibition / physiology*
  • Place Cells / physiology*
  • Pyramidal Cells / physiology*
  • Sleep
  • Spatial Memory / physiology*