Nicotinic acetylcholine receptors contribute to learning-induced metaplasticity in the hippocampus

J Cogn Neurosci. 2013 Jul;25(7):986-97. doi: 10.1162/jocn_a_00383. Epub 2013 Mar 7.

Abstract

Hippocampal learning is thought to induce metaplasticity, which can facilitate subsequent learning. Administered at single low doses, the N-methyl-d-aspartate-type glutamate receptor antagonist memantine predominantly blocks α7 nicotinic acetylcholine receptors (α7 nAChRs). Placebo-controlled administration of a single low dose of memantine in a pharmaco-fMRI experiment may thus help characterize the role of α7 nAChRs in hippocampal metaplasticity. We hypothesized that if α7 nAChRs contribute to learning-induced metaplasticity in the hippocampus, blockade of these receptors with low-dose memantine would selectively interfere with a facilitation of subsequent learning without impairing hippocampal learning per se. To specifically test this hypothesis, we devised a randomized controlled trial in which healthy volunteers were administered a 20-mg single oral dose of memantine or placebo and scanned on three subsequent runs of a hippocampal learning task. Our results indicate no discrepancies in behavioral learning between low-dose memantine- and placebo-treated participants in the first and second run of this task. In the third run, however, only the placebo-treated group showed facilitated behavioral learning, an effect paralleled by decreased neural responses in the hippocampal cornu ammonis region. Our findings suggest that blockade of α7 nAChRs selectively interfered with a learning-induced facilitation of subsequent learning while leaving unimpaired hippocampal learning per se. Taken together, our results provide support for a relevant contribution of α7 nAChRs to learning-associated metaplasticity in the hippocampus.

Publication types

  • Randomized Controlled Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Analysis of Variance
  • Association Learning / drug effects
  • Association Learning / physiology*
  • Double-Blind Method
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • Hippocampus / blood supply
  • Hippocampus / drug effects
  • Hippocampus / physiology*
  • Humans
  • Image Processing, Computer-Assisted
  • Magnetic Resonance Imaging
  • Male
  • Mathematics
  • Memantine / pharmacology
  • Memory, Short-Term / drug effects
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Neuropsychological Tests
  • Oxygen / blood
  • Pattern Recognition, Visual / drug effects
  • Photic Stimulation
  • Receptors, Nicotinic / metabolism*
  • Young Adult

Substances

  • Excitatory Amino Acid Antagonists
  • Receptors, Nicotinic
  • Oxygen
  • Memantine