Cholinergic plasticity of oscillating neuronal assemblies in mouse hippocampal slices

PLoS One. 2013 Nov 18;8(11):e80718. doi: 10.1371/journal.pone.0080718. eCollection 2013.

Abstract

The mammalian hippocampus expresses several types of network oscillations which entrain neurons into transiently stable assemblies. These groups of co-active neurons are believed to support the formation, consolidation and recall of context-dependent memories. Formation of new assemblies occurs during theta- and gamma-oscillations under conditions of high cholinergic activity. Memory consolidation is linked to sharp wave-ripple oscillations (SPW-R) during decreased cholinergic tone. We hypothesized that increased cholinergic tone supports plastic changes of assemblies while low cholinergic tone favors their stability. Coherent spatiotemporal network patterns were measured during SPW-R activity in mouse hippocampal slices. We compared neuronal activity within the oscillating assemblies before and after a transient phase of carbachol-induced gamma oscillations. Single units maintained their coupling to SPW-R throughout the experiment and could be re-identified after the transient phase of gamma oscillations. However, the frequency of SPW-R-related unit firing was enhanced after muscarinic stimulation. At the network level, these changes resulted in altered patterns of extracellularly recorded SPW-R waveforms. In contrast, recording of ongoing SPW-R activity without intermittent cholinergic stimulation revealed remarkably stable repetitive activation of assemblies. These results show that activation of cholinergic receptors induces plasticity at the level of oscillating hippocampal assemblies, in line with the different role of gamma- and SPW-R network activity for memory formation and -consolidation, respectively.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Animals
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / physiology
  • CA3 Region, Hippocampal / drug effects
  • CA3 Region, Hippocampal / physiology
  • Carbachol / pharmacology
  • Cholinergic Agonists / pharmacology
  • Hippocampus / drug effects
  • Hippocampus / physiology
  • Male
  • Mice
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Receptors, Cholinergic / metabolism

Substances

  • Cholinergic Agonists
  • Receptors, Cholinergic
  • Carbachol

Grants and funding

Grant sponsor: German Research Foundation (DFG) and German Ministry of Education and Science (BMBF); Grant number SFB 636 and BCCN B3. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.